From: Subject: Breakdown of the Endothelial Barrier Function in Tumor Cell Transmigration -- Mierke et al. 94 (7): 2832 -- Biophysical Journal Date: Sat, 29 Mar 2008 12:22:08 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_00C5_01C89197.81C46480" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_00C5_01C89197.81C46480 Content-Type: text/html; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.biophysj.org/cgi/content/full/94/7/2832 Breakdown of the Endothelial Barrier Function in = Tumor Cell Transmigration -- Mierke et al. 94 (7): 2832 -- Biophysical = Journal 3D"help3D"home=20
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Originally published as = Biophys=20 J. BioFAST on December 20, 2007.
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Biophysical Journal 94:2832-2846 (2008)
=A9 2008 = The Biophysical=20 Society

This is an Open Access article distributed under the = terms of=20 the Creative Commons-Attribution Noncommercial License (http://creativeco= mmons.org/licenses/by-nc/2.0/),=20 which permits unrestricted noncommercial use, distribution, and = reproduction in=20 any medium, provided the original work is properly cited.

Breakdown of the Endothelial Barrier Function in Tumor Cell=20 Transmigration

Claudia Tanja=20 Mierke *, Daniel Paranhos=20 Zitterbart *, Philip=20 Kollmannsberger *, Carina=20 Raupach *, Ursula=20 Schl=F6tzer-Schrehardt 3D{dagger}=20,=20 Tamme Weyert Goecke 3D{ddagger}=20,=20 J=FCrgen Behrens 3D=A7=20 = and Ben=20 Fabry *

* Biophysik, Zentrum f=FCr medizinische = Physik und=20 Technik, 3D{dagger} Augenklinik, 3D{ddagger}=20 = Frauenklinik,=20 3D=A7=20 Nikolaus-Fiebiger Zentrum f=FCr Molekulare Medizin, Universit=E4t = Erlangen-N=FCrnberg,=20 91052 Erlangen, Germany

Correspondence: Address reprint requests to Dr. = Claudia Tanja=20 Mierke, University of Erlangen-Nuremberg, Center for Medical Physics and = Technology, Biophysics Group, Henkestrasse 91, 91052 Erlangen, Germany. = Tel.:=20 49-9131-85-25607; Fax: 49-9131-85-25601; E-mail: claudia.mierke{at}t-online.de .


3D"   =20 ABSTRACT
TOP
3D"ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
SUPPLEMENTARY MATERIAL
ACKNOWLEDGEMENTS
REFERENCES
 
T= he=20 ability of tumor cells to metastasize is associated with a = poor=20 prognosis for cancer. During the process of metastasis, tumor = cells=20 circulating in the blood or lymph vessels can adhere to, and=20 potentially transmigrate through, the endothelium and invade = the=20 connective tissue. We studied the effectiveness of the = endothelium as=20 a barrier against the invasion of 51 tumor cell lines into a=20 three-dimensional collagen matrix. Only nine tumor cell lines = showed=20 attenuated invasion in the presence of an endothelial cell = monolayer,=20 whereas 17 cell lines became invasive or showed a = significantly=20 increased invasion. Endothelial cells cocultured with = invasive tumor=20 cells increased chemokine gene expression of IL-8 and = Gro-β.=20 Expression of the IL-8 and Gro-β receptor, CXCR2, = was=20 upregulated in invasive tumor cells. Addition of IL-8 or = Gro-β=20 increased tumor cell invasiveness by more than twofold. Tumor = cell=20 variants selected for high CXCR2 expression were fourfold = more=20 invasive in the presence of an endothelial cell layer, = whereas=20 CXCR2 siRNA knock-down cells were fivefold less invasive. We=20 demonstrate that Gro-β and IL-8 secreted by = endothelial cells,=20 together with CXCR2 receptor expression on invasive tumor = cells,=20 contribute to the breakdown of the endothelial barrier by = enhancing=20 tumor cell force generation and cytoskeletal remodeling=20 dynamics.


3D"   =20 INTRODUCTION
TOP
ABSTRACT
3D"INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
SUPPLEMENTARY MATERIAL
ACKNOWLEDGEMENTS
REFERENCES
 
M= ost=20 cancer-related deaths are caused by metastasis formation, a = process=20 that starts with dissociation of tumor cells from the primary = tumor=20 and is followed by tissue invasion, entrance into blood or = lymph=20 vessels (intravasation), and transport to remote sites. It is = widely=20 assumed that tumor cells can then escape from the = microvasculature=20 (extravasation), invade the target tissue, and form secondary = tumors=20 in distant organs (13DGo=9633DGo). A potentially rate-limiting step in = metastasis=20 formation, therefore, would be the extravasation process that = involves adhesion of tumor cells to endothelial cells and = their=20 transmigration through the endothelial cell monolayer and = basement=20 membrane (33DGo=9663DGo). Certain tumor cell types have indeed been = shown, both=20 in vitro and in vivo, to be able to overcome the endothelial=20 barrier (63DGo=96113DGo).=20 But extravasation need not be the only mechanism for = metastasis=20 formation, as has recently been pointed out by Al-Mehdi et = al. (123DGo),=20 who reported that tumor cells can adhere and grow onto the=20 endothelial layer and form a metastasis without ever leaving = the=20 blood or lymph vessel. Either way, the role of the = endothelial=20 monolayer in this process is thought to be crucial in that it = can=20 actively modulate metastasis formation by either allowing or = blocking=20 the adhesion, and possibly transmigration, of tumor cells = (83DGo=96103DGo).=20 The details of endothelial cell functions in this process, = however,=20 are poorly understood, and the extent to which the = endothelium=20 impedes or promotes metastasis formation is still = unclear.=20

Transmigrating tumor cells are thought to be able to overcome = the=20 endothelial barrier by inducing changes within endothelial = cells,=20 including the upregulation of adhesion molecule receptor = expression=20 (13), the reorganization of the cytoskeleton (143DGo), Src-mediated disruption of endothelial=20 VE-cadherin-β-catenin cell-cell adhesions (73DGo),=20 the formation of "holes" within the endothelial layer (153DGo),=20 and the induction of apoptosis (163DGo). Tumor cell invasion may bear a close = resemblance to=20 leukocyte trafficking for which the endothelium acts as a = barrier=20 and greatly reduces invasion rates (173DGo).=20 For example, the function of the endothelial cell barrier = against=20 both leukocyte trafficking and tumor cell transmigration is = reduced=20 in the presence of inflammatory cytokines such as tumor = necrosis=20 factor-3D{alpha} and interleukin-1β (83DGo,133DGo,183DGo,193DGo).=20 These cytokines are known to trigger an upregulation of the = adhesion=20 molecule E-selectin (133DGo).=20 The subsequent adhesion of tumor cells to E-selectin leads to = an=20 upregulation of stress-activated protein kinase-2 (SAPK2/p38) = in=20 endothelial cells (133DGo)=20 and triggers actin polymerization and reorganization into = stress=20 fibers (143DGo).

Chemokines and their receptors are also important for leukocyte=20 trafficking (203DGo,213DGo)=20 and tumor cell invasion (223DGo).=20 Chemokines are a superfamily of small cytokine-like proteins = that=20 induce cytoskeletal rearrangements in endothelial cells and=20 leukocytes, the firm adhesion of leukocytes to endothelial = cells, and=20 the directional migration of leukocytes (203DGo).=20 The involvement of chemokines in tumor-endothelial = interactions and=20 their effect on tumor cell mechanics during invasion are = considerably=20 less well understood, however.

The aim of this study was to investigate the ability of the=20 endothelium to regulate the transmigration and invasion of = tumor=20 cells into an extracellular matrix. We measured the invasion = of=20 human tumor cell lines into a three-dimensional collagen gel = matrix=20 that was covered with an endothelial cell monolayer. In the = presence=20 of an endothelium, the invasion of some tumor cell lines = increased=20 significantly. Gene expression analysis of endothelial cells=20 cocultured with invasive tumor cells revealed an upregulation = of=20 Gro-β and IL-8 chemokines compared with = endothelial cells=20 cocultured with noninvasive tumor cells. Finally, we = demonstrate that=20 the Gro-β and IL-8 receptor (CXCR2) expression on = tumor cells=20 serves as a key mediator responsible for the breakdown of the = endothelial barrier function by enhancing tumor cell force = generation=20 and cytoskeletal remodeling dynamics.


3D"   =20 MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
3D"MATERIALS AND METHODS
RESULTS
DISCUSSION
SUPPLEMENTARY MATERIAL
ACKNOWLEDGEMENTS
REFERENCES
 
<= STRONG>Three-dimensional=20 collagen assay
All chemicals were purchased from Sigma = (Taufkirchen,=20 Germany) unless otherwise noted. Collagen R (Serva, = Heidelberg,=20 Germany) and G (Biochrom, Berlin, Germany) were mixed at a = ratio=20 1:1, 25 mM sodium bicarbonate and 10 vol % of 10x DME (Biochrom) was added. The = solution=20 was neutralized with 1 N sodium hydroxide, and 1.2 ml = collagen=20 solution was placed into each well of a six-well plate, = polymerized,=20 incubated with Endothelial Cell Growth Medium 2 (Promocell,=20 Heidelberg, Germany) containing 2% low-endotoxin FCS, and = 600,000=20 endothelial cells (first passage) were seeded onto the gel.=20 Polymerized collagen gels were 474 =B5m =B1 7 (mean = =B1 SE, n=20 =3D 12) thick. After 24 h, the cells had formed a closed = monolayer, and=20 100,000 tumor cells were added per 3.5-cm dish. To study = invasion in=20 the absence of endothelial cells, tumor cells were added = directly to=20 the gels. Before seeding, tumor cells were stained with 5=20 =B5g/ml carboxyfluorescein diacetate (Invitrogen, = Karlsruhe,=20 Germany) and 1 =B5g/ml Hoechst 33342 dye to = distinguish them=20 from endothelial cells. Coculture times ranging from 8 h to 5 = d=20 were tested. Staining was stable over the course of the=20 experiment; the Hoechst dye was found to exhibit only = insignificant=20 photobleaching, and the carboxyfluorescein diacetate, = although it was=20 prone to photobleaching, was adequate for confirming that=20 endothelial cells did not invade the collagen matrix. A = coculture=20 time of 72 h was found to be optimal because differences in = the=20 invasiveness of tumor cell lines were clearly visible while = the=20 endothelial monolayer was still confluent, with no signs of = tube=20 formation or invasion. After fixation with 2.5% = glutaraldehyde=20 solution, the number of invaded tumor cells and their = invasion depth=20 were determined in 12 randomly selected fields of view. = Invasion=20 depth was determined by focusing the microscope on the center = of the nucleus; the value was read from the motorized = z-drive=20 of the microscope and was corrected for the refractive index = of=20 water (1.33). The z-focus at the gel surface was taken as=20 reference. Images were taken using a CCD camera (ORCA ER, = Hamamatsu,=20 DMI6000 Leica microscope, Wetzlar, Germany, 40x HCX fluotar objective, NA = 0.6, Wasabi=20 software).

Cell isolation and culture
Endothelial cells were = isolated from the veins of human umbilical cords (HUVECs) = (233DGo).=20 The vein was washed with PBS buffer, and endothelial cells = were=20 isolated using trypsin/EDTA solution (0.25%/0.2%) in PBS for = 20 min=20 at 37=B0C. HUVECs were maintained in endothelial medium (see = above).=20 HUVEC purity was determined by FACS analysis using = VE-cadherin=20 (Coulter, Krefeld, Germany) and PECAM-1 (Biozol, Eching, = Germany).=20 Isolations contained less than 0.3% contaminating cells. = Human=20 pulmonary endothelial cells (HPMECs, Promocell) were used in = passage=20 4=966 and cultured in Endothelial Cell Growth Medium MV 2=20 (Promocell) containing 5% FCS.

Tumor cells (ATCC-LGC-Promochem, Wesel, Germany) were cultured = in=20 DMEM (containing 1g/liter D-glucose, 10% low = endotoxin=20 FCS, 100 U/ml penicillin, 100 =B5g/ml streptomycin) to = 80%=20 confluency and used in passages 5 to 30. All cells were = cultured at=20 37=B0C, 95% humidity, and 5% CO2, harvested using = Accutase=20 (PAA, Linz, Austria) and tested for mycoplasma contamination = using a=20 Mycoplasma-Detection-Kit (Roche, Penzberg, Germany). Primary = tumor=20 cells were isolated from kidney clear cell carcinomas using=20 collagenase D and were used in passages 3=9610. Primary tumor = cells=20 expressed E-cadherin (Coulter) and MUC-18 (Coulter) and did = not=20 express PECAM-1 or VE-Cadherin.

Transmission EM
Cells were fixed in 4%=20 paraformaldehyde/0.1% glutaraldehyde in 0.1 M phosphate = buffer,=20 postfixed in 2% buffered osmium tetroxide, dehydrated through = a=20 graded ethanol series and embedded in epoxy resin. The = 1.0-=B5m=20 sections for orientation were stained with toluidine blue. = Ultrathin=20 sections (70 nm) were stained with uranyl acetate and lead = citrate=20 and examined with a transmission electron microscope (EM906E; = Zeiss,=20 Oberkochen, Germany).

Scanning EM
Fixed cells and gels were dehydrated = through=20 a graded ethanol series, washed with hexadimethylsilazane = reagent=20 (Electron-Microscopy-Science, Hatfield, PA), and air-dried. = Cells=20 were sputter-coated with gold and analyzed using a scanning = electron=20 microscope (ISI-SX-40, International Scientific Instruments,=20 Milpitas, CA).

Cell sorting for gene expression=20 analysis
Carboxyfluorescein-diacetate-stained tumor cells = were=20 cultured onto a HUVEC monolayer for 16 h. Cells were = harvested,=20 stained with a mouse anti PECAM-1 antibody and a secondary=20 R-PE-labeled anti mouse IgG (F(ab)2 fragment) = antibody=20 (Dianova, Hamburg, Germany) to detect endothelial cells, and=20 separated using a cell sorter (Moflow, DakoCytomation). The = purity of=20 sorted endothelial cells and tumor cells was better than = 99%.=20

RNA isolation and DNA microarray = hybridization
After cell=20 sorting, endothelial cells from mono- or coculture with = MDA-MB-231,=20 786-O, MCF-7, and SW480 tumor cells were centrifuged (250 = x g, 5 min, 4=B0C). The pellet was = resuspended=20 in Trizol reagent (5 min, RT, Invitrogen), and total RNA was=20 isolated according to the manufacturer's instructions. RNA = was=20 digested with RNase-free DNase I and purified using the = RNAeasyKit=20 (Qiagen, Hilden, Germany) according to the manufacturer's=20 instructions. RNA quality was checked by gel electrophoresis = and=20 spectrophotometric measurement of OD at 260/280 nm. cDNA = synthesis=20 and synthesis of biotinylated cRNA were performed as = described by=20 Thomas et al. (243DGo).=20 Human genome HG-U133A GeneChips (containing 22,283 open = reading=20 frames/genes, Affymetrix, Santa Clara, CA) were hybridized, = washed,=20 and scanned with the G2500A GeneArray scanner (Affymetrix) in = cooperation with Dr. M=F6r=F6y and Dr. Klein-Hitpass, = Institute of Cell=20 Biology (Tumor Research), University of Essen Medical = School.=20

DNA-Microarray data analysis
Microarray data were = analyzed using MicroarraySuite 5.1 and DataMiningTool 3.0=20 (Affymetrix). Gene expression levels of cocultured = endothelial cells=20 were normalized by the expression levels of monocultured = cells (same=20 isolation). Mono- and cocultured endothelial cells were = stained and=20 sorted equally to eliminate bias. Statistical analyses were = performed=20 using Student's t-test. The expression of a HUVEC gene = was=20 considered to be correlated with tumor invasiveness when the=20 following criteria were met: the expression level was higher = than 500=20 Affymetrix units in at least one of the culture conditions = (the=20 median expression level of all genes was 273 Affymetrix = units); the=20 expression level after coculture with invasive versus = noninvasive=20 tumor cells was at least 1.8-fold different; and the = expression=20 levels of that gene did not overlap between noninvasive and = invasive=20 coculture conditions. Genes expressed in tumor cells at = levels higher=20 than 5000 Affymetrix units were disregarded to avoid = contamination=20 artifacts. We confirmed the microarray data for IL-8, = Gro-β,=20 ICAM-1, and VCAM-1 using RT-PCR.

Flow cytometry
Tumor cells were harvested and = resuspended=20 in Hepes buffer (20 mM Hepes, 125 mM NaCl, 45 mM glucose, 5 = mM KCl,=20 0.1% albumin, pH 7.4). Cells were incubated with mouse = antibodies=20 directed against CXCR1, CXCR2, CXCR3, CCR2 (all R&D = systems,=20 Minneapolis, MN), or CXCR4 (Dianova). Appropriate isotype = controls=20 (mouse IgG1, IgG2a, and = IgG2b) were=20 used (Invitrogen). After 30 min of incubation at 4=B0C, the = cells were=20 washed and stained with a secondary R-PE-labeled anti-mouse = IgG=20 antibody. FACS analysis was performed using a FACSCalibur = system=20 (Becton Dickinson, Heidelberg, Germany).

Isolation of tumor cell variants
For the = isolation of=20 tumor cell variants expressing low and high amounts of CXCR2, = tumor=20 cells were stained as described above under flow cytometry. = Low and=20 high CXCR2-expressing tumor cell variants were separated = using a cell=20 sorter. Cells were expanded in culture, and the isolation and = sorting=20 procedures were repeated three times.

siRNA transfection
A quantity of 200,000 = MDA-MB-231 cells=20 were seeded into each six-well plate. Ten minutes later, a=20 transfection mixture containing 2.4 =B5l of a 20 = =B5M=20 Alexafluor546-labeled CXCR2 RNAi solution (target-sequence=20 AGGATTTAAGTTTACCTCAAA) and 12 =B5l HiPerFect Reagent = (Qiagen) in=20 100 =B5l DMEM, was added and incubated at room = temperature for=20 10 min. RNAi-mediated CXCR2-knockdown and transfection = efficiency=20 were determined by FACS-analysis using an anti-CXCR2 antibody = and a=20 Cy2-labeled anti-mouse antibody (Dianova).

CXCR2 inhibition
CXCR2 inhibitor SB255002=20 (Calbiochem, San Diego, CA) was added together with tumor = cells=20 (100,000 per six-well plate) at concentrations ranging from = 2.2 nM to=20 28.4 =B5M. Invasiveness was determined after 3 days of = coculture.

Cell mechanics
For creep measurements, a = staircase-like=20 sequence of step forces ranging from 0.5 to 10 nN was applied = to=20 superparamagnetic 4.5-=B5m epoxylated, = fibronectin-coated beads=20 (Invitrogen) using magnetic-tweezers as described by Alenghat = et al.=20 (25) and Mierke et al. (263DGo). After 30 min of bead incubation, = measurements were=20 performed at 37=B0C on an inverted microscope (DMI Leica) = with 40x magnification using = monocultured=20 MDA-MB-231 wild type and CXCR2 siRNA knockdown cells. = Bright-field=20 images were taken by a CCD camera (ORCA ER) at 40 frames/s. = The bead=20 positions were tracked using an intensity-weighted = center-of-mass=20 algorithm (273DGo).=20 The creep response J(t) of the cells followed a = power=20 law in time, J(t) =3D=20 a(t/t0)b, where the prefactor a = and the=20 power-law exponent b were both force dependent, and = the=20 reference time t0 was set to 1 s. The bead=20 displacement in response to a staircase-like force followed a = superposition of power laws (283DGo)=20 (see Fig. 7=20 A), from which the power-law exponent b was = determined by a least-squares fit. In addition, the position = of=20 unforced beads was tracked over 5 min. These beads moved=20 spontaneously with a mean-square displacement (MSD) that also = followed a power law in time, MSD =3D D*(3D{Delta}=20t/t0)3D{alpha}=20 + c = using low=20 and high CXCR2-expressing tumor cell variants (see Fig. 7=20 B). The power-law exponent 3D{alpha}=20 was = determined=20 by a least-squares fit (293DGo,303DGo).=20 Cell tractions (see Fig. 7, = C=20 and D) were computed from the deformation field of = an=20 elastic fibronectin-coated (50 =B5m/ml) 6-kPa = polyacrylamide gel=20 during cell adhesion using low and high CXCR2-expressing = tumor cell=20 variants (263DGo,313DGo).



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  = 		FIGURE 7  CXCR2 expression = modulates=20 cell mechanics, cytoskeletal dynamics, and tractions in = MDA-MB-231=20 breast carcinoma cells. (A) Assay 1: The = displacements of=20 integrin-bound magnetic beads to step forces between 0.5 and = 10 nN=20 (creep response) followed a superposition of power laws in = time with=20 exponents that were significantly higher in CXCR2 wild-type = cells=20 compared with CXCR2 knockdown cells (see inset, = p <=20 0.05). (B) Assay 2: Mean square displacement (MSD) of = unforced beads attached to CXCR2-high cells revealed a more=20 superdiffusive behavior (see inset, p < = 0.05).=20 (C) Assay 3: Elastic strain energy generated by = CXCR2-high=20 cells during adhesion on a polyacrylamide gel was eightfold = higher=20 than that by CXCR2-low cells. (D) Example of a = traction map=20 beneath a CXCR2-low cell (top) and a CXCR2-high cell=20 (bottom) after 2, 36, and 100 min of adhesion time. = Maximum=20 tractions were substantially higher in CXCR2-high cells. = Scale bars=20 are 20 =B5m. =

 = ;
Statistics
Data=20 were expressed as mean values =B1 SE if not indicated = otherwise.=20 Statistical analysis was performed using the two-tailed = paired=20 t-test. A p < 0.05 was considered to be = statistically=20 significant.

Online supplementary material
Table S1 shows all = genes=20 up- or downregulated in endothelial cells after coculture = with=20 invasive compared with noninvasive tumor cells. Fig. S2 shows = the=20 effect of CXCR2 (mean =B1 SE) antagonist SB222005=20 on tumor cell transmigration; *p < 0.05. =


3D"   =20 RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
3D"RESULTS
DISCUSSION
SUPPLEMENTARY MATERIAL
ACKNOWLEDGEMENTS
REFERENCES
 
<= STRONG>Overcoming=20 the endothelial barrier
To study tumor-transendothelial = migration=20 and tissue invasion, a three-dimensional collagen assay was = developed=20 (Fig. 1=20 A). Freshly isolated HUVECs were cultured onto a = collagen=20 gel and formed a confluent monolayer within 24 h (Fig. 1=20 B). Adjacent endothelial cells overlapped by 3D~=202 =B5m = (Fig. 1=20 B inset). Collagen fibers formed a mesh = with an=20 average pore size of 0.6 =B1 0.2 =B5m (mean =B1 SE); = the gels had a=20 shear modulus of 58 Pa and a thickness of 474 =B1 7 = =B5m=20 (mean =B1 SE) (Fig. 1=20 C).



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  = 		FIGURE 1  Transendothelial = migration=20 and collagen invasion of tumor cells. (A) Schematic = diagram=20 of the tumor cell transmigration and invasion assay. = (B) TEM=20 image of the endothelial cell monolayer. (C) SEM = image of the=20 three-dimensional collagen gel fiber network. (D and=20 E) MDA-MB-231 breast carcinoma cells on plastic = surface=20 (D) showed an elongated spindle-shaped morphology in = a=20 three-dimensional collagen culture (E). (F) = Same cell=20 stained with carboxyfluorescein-diacetate. (G) The = number of=20 invaded MDA-MB-231 cells and their invasion depth were = increased in=20 the presence of an endothelium (dark gray) compared = with=20 endothelium-free culture (light gray). (H) = Adhesion of=20 an MDA-MB-231 cell and (I) of an SW480 cell onto the=20 endothelium. Arrows indicate caveolae of tumor and = endothelial=20 cells. (J) Transmigration of an MDA-MB-231 cell = through the=20 endothelium. (K) An enlarged detail of the close = contact=20 between tumor and endothelial cells. (L) Invasion of = an=20 MDA-MB-231 cell, and (M) stack of three invaded = MDA-MB-231=20 cells. Tumor cells transmigrated without destroying or = disrupting=20 the endothelium. Scale bars are 2 =B5m where = unspecified. =

 = ;
With=20 this assay, the transmigration and invasion behavior was = tested for=20 51 tumor cell lines derived from a broad spectrum of tissues = (Table = 1).=20 Before the tumor cells were added to the assay, they were=20 fluorescently labeled with carboxyfluorescein diacetate (to=20 distinguish them from endothelial cells, Fig. 1=20 F) and with Hoechst 33342 vital stain (for cell = counting=20 and quantification of the invasion depth). All tumor cells = were able=20 to attach to the endothelium or the collagen gel surface, = even those=20 that are unable to attach tightly to a pure plastic cell = culture=20 surface such as Colo201 and Colo205. After 3 days, the number = of tumor cells that had transmigrated through the endothelium = was counted, and their invasion depth was measured. All tumor = cell lines that invaded into the collagen gel assumed an = elongated,=20 spindle-shaped morphology that was drastically different from = the fibroblast-like morphology seen in a two-dimensional = plastic=20 cell culture flask (Fig. 1=20 D). Furthermore, tumor cells in the gels formed = long=20 filopodia (Fig. 1=20 E).


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  = 		TABLE 1  Classification of = tumor cell=20 invasiveness =

 = ;
As=20 introduced above, several pathways of tumor cell transmigration = are=20 possible: disruption of cell-cell adhesion sites, "hole" = formation,=20 and induction of apoptosis in endothelial cells. To determine = which=20 pathway the tumor cells chose, we analyzed TEM sections of = collagen=20 gels taken after 4, 10, 16, and 24 h of tumor-endothelial = cell=20 coculture with noninvasive SW480 and MCF-7 tumor cells and = with=20 invasive MDA-MB 231, A125, 786-O, and A375 tumor cells. Fig. 1, = H=96M, illustrates the three steps of tumor cell=20 extravasation: tumor cell adhesion (Fig. 1, = H=20 and I), transmigration (Fig. 1=20 J), and matrix invasion (Fig. 1 = L=20 and M). The adhesion process was completed after 4 = h of=20 coculture, and transmigration was detectable after 8 h. Among = 1000 = analyzed=20 TEM sections in which tumor cells were present, 20 tumor = cells=20 were in the process of transmigration, and 3D~=20100 cells had = invaded=20 into the collagen gel. For all transmigrating tumor cells, = adjacent=20 TEM sections were obtained to ensure that endothelial cells=20 were present on either side of the transmigrating tumor cell. = This finding indicates that the tumor cells transmigrated not = by "hole" formation but by disrupting the endothelial = cell-cell=20 contacts. Moreover, neighboring endothelial cells did not = show=20 morphological signs indicative of apoptosis such as membrane=20 blebbing, cell shrinkage, or rounding. During tumor cell = adhesion=20 and transmigration, the contact regions of tumor and = endothelial=20 cells were decorated with multiple vacuoles and caveolae (Fig. 1, = I=20 and K, arrows). In all TEM sections of = invaded=20 tumor cells (Fig. 1, = L=20 and M), the endothelial monolayer completely = resealed and=20 appeared intact (Fig. 1, = L=20 and M). This was verified in multiple adjacent sections=20 around each invaded tumor cell. We repeatedly found stacks of = invaded tumor cells at different invasion depths at the same=20 location (Fig. 1, = L=20 and M), suggesting that these tumor cells had used = the=20 same transmigration and invasion path.

Classification of tumor cell invasiveness
All = cell lines=20 were classified into invasive and noninvasive tumor cells = according=20 to their ability to invade the collagen gel. The invasion = depth for=20 all the tumor cells was measured in multiple randomly chosen = fields=20 of view. From the density (number of invaded cells per square = millimeter) plotted against invasion depth, an invasion = profile was=20 obtained (Fig.=20 1 G). Invasiveness was quantified by an invasion = score,=20 defined as cell density multiplied by the average invasion = depth.=20 Tumor cell lines with an invasion score 3D≤=200.1 = mm=961 were=20 defined as noninvasive; a score >0.1 mm=961 was = defined=20 as invasive. This threshold was chosen to avoid an erroneous=20 classification of noninvasive cells. Twenty-four of 51 tumor = cell=20 lines were able to invade into the collagen gel when no = endothelial=20 cells were present (Table = 1). All=20 cell lines derived from skin (five lines), prostate (two), = bladder=20 (two), and kidney (two) were invasive; among cell lines = derived from=20 breast (14 lines), cervix (two), colon (16 lines), lung = (four), and=20 pancreas (two) were both invasive and noninvasive lines (Table=20 1).

Endothelial cells enhance tumor cell invasion
A=20 conspicuous question is to what degree does the endothelial = layer=20 impede tumor cell invasion in a collagen matrix? In the = presence of=20 an endothelial monolayer, invasiveness was reduced in 9 of 24 = invasive cell lines (Table = 1),=20 unchanged in 9 cell lines, and, surprisingly, significantly = increased=20 in 6 cell lines (Table = 1).=20 Eleven of 27 noninvasive tumor cell lines became weakly = invasive in=20 the presence of an endothelial layer (Table=20 1). We also studied primary tumor cells isolated from = four=20 patients with kidney clear cell carcinomas. In contrast to = Caki-1=20 and 786-O kidney tumor cell lines, which did not alter their=20 invasiveness, all four primary kidney carcinoma cells showed=20 increased matrix invasion in the presence of an endothelium = (data not=20 shown).

The findings that the presence of the endothelium promoted = invasion=20 of some of the tumor cells and even induced invasion were = unexpected=20 and new. A possible interpretation of these results is that = the=20 endothelium promotes tumor cell proliferation. However, this=20 interpretation is ruled out by the finding that the number of = tumor=20 cells after 16 h of monoculture compared with coculture on an = endothelium was equal.

The collagen invasion assay was repeated in MDA-MB-231 tumor=20 cells, but this time the endothelial layer was replaced by a=20 closed monolayer of MCF-7 epithelial cells. MDA-MB-231 cell=20 invasion was fully blocked by MCF-7 cells, indicating that = the=20 modulation of tumor cell invasion seen in our data was = specific=20 for the presence of endothelial cells. Experiments on all = tumor=20 cell lines were repeated with endothelial cells isolated from = three to six different donors (250 in total) and were = performed=20 over 3 years with more than 10 batches of bovine and rat = collagen.=20 The standard deviation of the invasion scores within a tumor=20 cell line was typically 30% of the mean, suggesting that = effects=20 of individual HUVEC isolations or variations among collagen=20 batches were minimal.

Both macrovascular and microvascular endothelial cells = enhance tumor=20 cell invasion
We replaced macrovascular HUVECs with primary = HPMECs=20 isolated from lung resections and analyzed 11 different tumor = cell=20 lines for their ability to overcome the endothelial cell = barrier=20 and to invade the three-dimensional collagen gels. In = agreement=20 with the data obtained with HUVECs, MCF-7, CX-1, Caco-2, and=20 MDA-MB-468 cells remained completely noninvasive in the = presence=20 of a microvascular endothelial cell layer, the invasion of = HeLa=20 cells was significantly impeded, and the invasion of = MDA-MB-231,=20 T24, EJ-28, A375, and DU145 were significantly enhanced (Fig. = 2).=20 Note that the control experiments without endothelial cells=20 were carried out in both HUVEC and HPMEC cell culture medium, = which differ in their serum and hydrocortisone content, but = the=20 invasiveness of tumor cells was not markedly different.=20 Interestingly, pulmonary microvascular ECs enhanced the = invasion=20 of MDA-MB-231 breast and T24 skin carcinoma cell to a = markedly=20 larger extent than HUVECs, and they induced the invasion of=20 A431 lung carcinoma into the collagen matrix (Fig. = 2).=20 Despite these important differences, HUVECs provide an = appropriate=20 and convenient model system to study breakdown of the=20 endothelial barrier function against tumor cell = invasion.



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  = 		FIGURE 2  Microvascular and = macrovascular endothelial cells enhanced tumor cell = transmigration=20 and invasion. Invasion score (mean =B1 SE) of selected tumor = cells in=20 the presence and absence of a HPMEC or HUVEC monolayer (ML). = Note=20 that the HPMEC medium contained 5% FCS, and the HUVEC medium = contained only 2% FCS. Accordingly, the endothelial = cell-free=20 controls were performed with 2% and 5% FCS. Independent of = the=20 endothelial cell type used, the invasion score of cocultured = cells=20 was significantly increased for MDA-MB-231, T24, EJ-28, = A375, DU145,=20 or in the case of HeLa significantly decreased (p = < 0.05).=20 For the A431 lung carcinoma cells, the HPMECs significantly = induced=20 the invasion score compared with HUVECs (p < = 0.05).=20 (inset) Invasiveness of MDA-MB-231 cells cultured in = the=20 presence of a HPMEC monolayer (ML) or cocultured with HPMECs = that=20 were seeded at the same with the tumor cells but did not = form a=20 monolayer (w/o ML). Numbers are expressed as fold increase = of the=20 invasion score compared with MDA-MB-231 in monoculture. = HPMECs=20 increased MDA-MB-231 cell invasion in both cases, but the = effect of=20 a monolayer was more pronounced. =

 = ;
Endothelial=20 chemokines enhance transmigration and invasion of some tumor=20 cells
Gene expression analysis of endothelial cells was=20 performed to identify candidate genes responsible for the=20 enhancement of tumor cell transmigration and invasion. The = expression=20 profile of endothelial cells in monoculture or after 16 h of=20 coculture with tumor cells was analyzed using DNA = microarrays. For=20 coculture, two noninvasive cell lines (MCF-7 and SW480) and = two=20 invasive cell lines (MDA-MB-231 and EJ-28) were chosen. Our = choice=20 of MDA-MB-231 and EJ-28 cells was guided by their highly=20 invasive behavior and their pronounced increase in = invasiveness in=20 the presence of an endothelium (Table=20 1).

Comparison of the gene expression profile under monoculture = and=20 coculture revealed 257 genes with expression levels that = correlated=20 with invasiveness (Fig. = 3 and=20 Table S1). Seventy-six genes were decreased, and 182 genes = were=20 increased in endothelial cells when cocultured with invasive = tumor=20 cells. Among the genes with increased expression were the = chemokines=20 Gro-β, IL-8, and I-TAC (Fig. 3=20 A). The expression of another chemokine, MCP-1, = was=20 increased in endothelial cells (by 6.5-fold) only during = coculture=20 with EJ-28 bladder carcinoma cells. Because MCP-1 has been = described=20 as enhancer for PC-3 prostate carcinoma cell invasiveness = (323DGo),=20 it was included in a subsequent invasion assay, which was = performed=20 to determine whether tumor cell transmigration and invasion = were=20 altered by Gro-β, IL-8, I-TAC, and MCP-1 = stimulation.=20



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  = 		FIGURE 3  Chemokines = enhanced tumor=20 cell transmigration and invasion. (A) Expression = profiles of=20 genes that were upregulated (red) or downregulated=20 (green) in endothelial cells cocultured with two = invasive and=20 two noninvasive tumor cells. Among the 257 regulated genes = were=20 numerous cytoskeletal proteins, adhesion molecules, and=20 cytokines/chemokines. (B) Addition of the chemokines=20 Gro-β (100 ng/ml) and IL-8 (25 ng/ml) = significantly increased=20 the invasion score (mean =B1 SE, *p < 0.05) of = 786-O kidney=20 carcinoma cells both in the presence (dark gray) and = absence=20 of endothelial cells (light gray). No significant = increase of=20 invasiveness was seen after addition of the chemokines I-TAC = (20=20 ng/ml) and MCP-1 (20 ng/ml). (C) Modulation contrast = image of=20 786-O kidney carcinoma cells (invasion depth 50 =B5m) = show=20 similar morphology under control conditions and under = chemokine=20 stimulation. Scale bars are 50 =B5m. =

 = ;
Gro-β=20 and IL-8 addition to 786-O kidney carcinoma cells increased=20 transmigration and invasion significantly (Fig. 3=20 B). The effect of Gro-β and IL-8 was = particularly=20 pronounced in the presence of an endothelial cell monolayer. = The=20 chemokine concentrations of 100 ng/ml for Gro-β, = 25 ng/ml for=20 IL-8, and 20 ng/ml for I-TAC and MCP-1 were chosen according = to=20 Lu et al. (323DGo)=20 and Youngs et al. (333DGo);=20 twofold higher concentrations were also tested, and in the = case of=20 Gro-β, 10-fold lower and higher concentrations as = well, but no=20 further increase of invasiveness was found. I-TAC or MCP-1 = did not=20 enhance tumor cell invasion (Fig. 3=20 B). Gro-β, IL-8, I-TAC, and MCP-1 = stimulation of=20 noninvasive MDA-MB-468 breast carcinoma cells had no effect = (data not=20 shown). The morphology of tumor cells or HUVECs was not = altered after=20 chemokine stimulation (Fig. 3=20 C).

To distinguish between the potentially invasiveness-enhancing=20 effect of chemokine secretion by the endothelial cells and = the=20 physical barrier function of a closed endothelial monolayer, = we=20 co-plated MDA-MB-231 breast carcinoma cells with microvascular=20 endothelial cells that were both added onto native collagen=20 gels at the same time. After 3 days of coculture, the = presence=20 of endothelial cells increased MDA-MB-231 cell invasion by = threefold=20 (Fig.=20 2, inset). This increase, however, was less pronounced=20 than the ninefold increase of invasiveness seen in the case=20 where an endothelial monolayer had already formed before the=20 addition of tumor cells (Fig. = 2,=20 inset). This result points to a complete breakdown of = the=20 endothelial barrier function against the invasion of = MDA-MB-231=20 cells, although it remains an open question why endothelial = cells in=20 a monolayer can promote tumor cell invasion to a higher = degree than=20 an equal number of endothelial cells that have not yet formed = a=20 monolayer.

CXCR2 expression on tumor cells increases transmigration and=20 invasion
The diverse effects of those chemokines suggest = that=20 invasive and noninvasive tumor cells express the chemokine=20 receptors at different levels. The expression levels of the=20 following chemokine receptors were analyzed for all 51 tumor = cell=20 lines: CXCR1 (IL-8 receptor), CXCR2 (IL-8 and = Gro-β=20 receptor), CXCR3 (I-TAC receptor), and CCR2 (MCP-1 receptor). = For=20 example, the histograms show the expression levels of the = invasive=20 MDA-MB-231 breast carcinoma cells and the noninvasive MCF-7 = breast=20 carcinoma cells (Fig. 4, = A=20 and B).



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  = 		FIGURE 4  Chemokine = receptor=20 expression on tumor and endothelial cells. (A) = Chemokine=20 receptor expression on invasive MDA-MB-231 breast carcinoma = cells,=20 (B) noninvasive MCF-7 breast carcinoma cells, and = (C)=20 freshly isolated HUVECs in passage 0 were measured using = FACS=20 analysis. (D) Chemokine receptor expression (mean =B1 = SE) on=20 invasive (dark gray, n =3D 24), and = noninvasive tumor=20 cells (light gray, n =3D 27) and HUVECs = (black,=20 n =3D 3 different isolations). Invasive tumor cells = expressed=20 2.3-fold higher levels of CXCR2 compared with noninvasive = tumor=20 cells (*p < 0.05). =

 = ;
In=20 addition, the expression level of the CXCR4 receptor was = studied=20 because CXCR4 has been reported to correlate with metastasis=20 formation (343DGo).=20 FACS analysis on all 51 tumor cell lines showed that CXCR2 = receptor=20 expression (mean values averaged over 24 invasive cell lines = and over=20 27 noninvasive tumor cell lines) was increased by 2.3-fold in = invasive compared with noninvasive tumor cells (Figs. 4 = D). All 24 invasive tumor cell lines expressed the = CXCR2=20 receptor, although the expression level in A875 melanoma = cells was=20 low. The other receptors tested did not correlate with = invasiveness=20 (Fig. 4=20 D). Expression of CXCR1, CXCR2, or CXCR3 on = freshly=20 isolated HUVECs was low; expression of CXCR4 and CCR2 was = detectable=20 (Fig. 4=20 C). In agreement with the literature, expression = levels of=20 CXCR2 increased in higher passages of some endothelial cell=20 isolations (353DGo,363DGo).=20 To rule out that CXCR2 autocrine stimulation of endothelial = cells=20 affected the transmigration and invasion assays, only freshly = isolated cells were used, and the CXCR2 expression levels of = each=20 endothelial cell isolation were determined.

To analyze the role of CXCR2 in the transmigration and invasion=20 process, variants of invasive cell lines were isolated that=20 expressed low and high amounts of CXCR2. Variants from the = following=20 tumor cell lines were generated using cell sorting after = staining=20 with an anti-CXCR2 antibody (numbers in parentheses give the=20 CXCR2 expression ratio of the high/low variant): MDA-MB-231=20 (breast, 5.3), 786-O (kidney, 12.3), and DU145 (prostate, = 4.0)=20 (Fig. 5, = A=96C).



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  = 		FIGURE 5  Analysis of = CXCR2-low and=20 CXCR2-high carcinoma cell variants. CXCR2 expression of = CXCR2-low=20 and CXCR2-high variants in (A) MDA-MB-231 breast, = (B)=20 786-O kidney, and (C) DU145 prostate carcinoma cells = after=20 four cycles of sorting and subsequent culturing. In each = histogram,=20 left curves are isotype controls, and filled gray curves are = CXCR2=20 expression on tumor cells. (D=96I) Transmigration and = invasion=20 of MDA-MB-231 (left), 786-O (middle), and = DU145=20 (right) variants expressing low and high amounts of = CXCR2.=20 (D=96F) Modulation contrast images of CXCR2-low = variants=20 (left) and CXCR2-high variants (right) in a = collagen=20 gel (50=9680 =B5m depths) in the absence = (bottom) or=20 presence (top) of an endothelial cell monolayer. = Scale bars=20 are 50 =B5m. (G=96I) Invasion scores (mean =B1 = SE) of=20 CXCR2-low and -high variants in the presence (dark gray = bars)=20 or absence of an endothelial cell monolayer (light gray=20 bars). In the presence of a HUVEC monolayer, all = CXCR2-high=20 variants are significantly more invasive than CXCR2-low = variants=20 (*p < 0.05). =

 = ;
The=20 transmigration and invasion behaviors of low and high = CXCR2-expressing=20 variants were analyzed in the three-dimensional collagen = assay=20 in the absence or presence of an endothelial monolayer. = Invasiveness=20 of the CXCR2-high MDA-MB-231 variant was increased by twofold = in the absence of endothelial cells, and increased by = threefold=20 in the presence of endothelial cells (Fig. 5=20 G). Invasiveness of the CXCR2-high 786-O variant = was=20 marginally increased in the absence of endothelial cells but=20 increased by fourfold in the presence of endothelial cells = (Fig. 5=20 H). Invasiveness of the CXCR2-high DU145 variant = was=20 marginally increased in the absence of endothelial cells but=20 increased by fourfold in the presence of endothelial cells = (Fig. 5=20 I).

To verify that tumor cell transendothelial migration and = invasion=20 were enhanced by high expression levels of CXCR2, an = RNAi-mediated=20 transient knock-down of CXCR2 was performed in MDA-MB-231 = cells=20 using fluorescently labeled CXCR2 siRNA. The transfection = efficiency=20 was 99.2% as analyzed by counting transfected and = nontransfected=20 cells and by FACS analysis (Fig. 6, = A,=20 D, and E). CXCR2 receptor expression after = siRNA=20 knock-down was not detectable by FACS analysis (Fig. 6, = B=20 and C). Also, the cell morphology was not altered = by CXCR2=20 siRNA transfection (Fig. 6, = G=96J). In the absence of an endothelial = monolayer, the=20 invasion of the CXCR2 knock-down cells was not reduced = significantly,=20 but importantly, the endothelium failed to increase the = invasiveness=20 in these cells (Fig. 6=20 F). This result is consistent with the observation = that=20 the CXCR2 inhibitor SB225002=20 (28.4 =B5M) completely blocked transendothelial = migration and=20 invasion of MDA-MB-231 cells (Fig. S2).



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  = 		FIGURE 6  CXCR2 siRNA = mediated=20 knock-down significantly reduced tumor cell transendothelial = migration and invasion. (A) FACS analysis of = transfection=20 efficiency. MDA-MB-231 breast carcinoma cells were = transfected with=20 CXCR2 siRNA fluorescently labeled with Alexa 546 (dark = gray)=20 and compared with nontransfected cells (light gray).=20 (B) FACS analysis of CXCR2 expression levels in = MDA-MB-231=20 control cells and (C) of cells transiently = transfected with=20 CXCR2 siRNA. (D) Modulation contrast image and = (E)=20 fluorescence image of MDA-MB-231 cells transiently = transfected with=20 CXCR2 siRNA. (F) In the presence of endothelial cells = (dark gray bars), CXCR2 knock-down in MDA-MB-231 = cells showed=20 significantly reduced invasiveness (*p < 0.05).=20 (G=96J) Modulation contrast image of nontransfected = MDA-MB-231=20 cells (G and H) and CXCR2 siRNA-transfected = MDA-MB-231=20 cells in a collagen gel (50 =B5m depth) in the = absence=20 (H and J) or presence (G and I) = of an=20 endothelial cell monolayer. Scale bars are 50 =B5m. =

 = ;
Chemokine-CXCR2=20 interactions increase tumor cell invasion by enhancing cytoskeletal = dynamics and=20 cell tractions
CXC receptor-ligand interactions can initiate = a large=20 number of signal transduction pathways that could contribute = to=20 invasive and motile behavior of tumor cells by increasing=20 actomyosin motor activity, adhesion/de-adhesion, and = cytoskeletal=20 remodeling events (373DGo).=20 The role of CXCR2 was explored using three cell-mechanical = assays.=20 The first was measuring the creep response of integrin-bound=20 fibronectin-coated magnetic beads to step forces between 0.5 = nN=20 and 10 nN (Fig. 7=20 A). The creep response for all forces followed a = power law=20 over time. The exponent of the power-law creep response is a = measure=20 of bond stability. Exponents close to zero indicate stable = bonds that=20 result in an elastic, solid-like cell-mechanical behavior. = Exponents=20 close to unity indicate unstable bonds with high cycling or = turnover=20 rates that result in a viscous, fluid-like cell-mechanical = behavior=20 (27). In MDA-MB-231 wild-type cells, the = power-law creep=20 exponent was significantly higher, closer to a fluid-like = behavior,=20 than in CXCR2 knock-down cells.

In the second assay, the random walk of unforced, spontaneously=20 diffusing fibronectin-coated beads was analyzed (Fig. 7=20 B). These beads cannot move unless the = microstructure to=20 which they are attached rearranges (293DGo).=20 ATP-driven cytoskeletal rearrangements can be quantified by = the=20 superdiffusive power-law exponent of the MSD of the bead = (293DGo,303DGo).=20 The power-law exponent of the MSD in CXCR2-high cell variants = was=20 significantly more superdiffusive (Fig. 7=20 B), indicative of a higher rate of ATP-driven = cytoskeletal=20 rearrangements.

The third assay explored actomyosin motor activity of MDA-MB-231 = cells that expressed low or high amounts of CXCR2 using = traction=20 microscopy (313DGo).=20 In both variant cell lines, the tractions increased steadily = on=20 seeding during adhesion on an elastic fibronectin-coated=20 polyacrylamide matrix. The strain energy and the tractions = generated=20 by CXCR2-high cells were eightfold higher than those = generated=20 by CXCR2-low cells (Fig. 7, = C=20 and D). Taken together, the mechanical effects of=20 increased CXCR2 expression, such as increased cytoskeletal = remodeling=20 dynamics and force-generating capability, provide a plausible = mechanism for the more invasive behavior seen in these tumor=20 cells.


3D"   =20 DISCUSSION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
3D"DISCUSSION
SUPPLEMENTARY MATERIAL
ACKNOWLEDGEMENTS
REFERENCES
 
W= e=20 developed a simple and reproducible assay consisting of a = collagen=20 matrix covered with an endothelial cell monolayer and = measured the=20 ability of 51 tumor cell lines derived from different tissues = to=20 transmigrate through the endothelium and invade the matrix = (Fig. = 1).=20 Twenty-four cell lines were able to invade the collagen when = an=20 endothelial monolayer was absent (Table=20 1). To quantify and compare the invasiveness of the cell=20 lines, an invasion score was used, which was computed as = tumor=20 cell density per square millimeter multiplied by the average=20 invasion depth. The invasion scores presented here are = consistent=20 with the invasiveness of some of the cell lines previously=20 tested by others (343DGo,383DGo).

To compare the invasiveness of tumor cell lines in the absence = and=20 presence of endothelial cells, collagen gels for both conditions = were=20 prepared at the same time and with the same collagen batch. = Type I=20 collagen is the most abundant matrix protein in connective = tissue: it=20 is easy to polymerize and forms a fiber network structure = with a=20 defined pore size and reproducible mechanical properties (Fig. = 1).=20 However, for reasons of simplicity and reproducibility, this = assay=20 was limited in several ways. First, the collagen gels were = not=20 covered with a realistic basal lamina, and the passive = barrier=20 function of the basal lamina laid down by the endothelial = cells needs=20 to be investigated further. However, endothelial cells = adhered well=20 to the gels and formed a confluent monolayer within 24 h. = Second, the=20 macrovascular HUVECs used in this assay differ from = microvascular=20 endothelial cells with respect to their adhesion molecule = expression=20 levels and chemokine secretion (213DGo,393DGo).=20 Such differences, however, have been reported to be no = greater than=20 those seen between microvascular endothelial cells from = different=20 organs (213DGo,403DGo).

We tested the transmigration and invasion behavior of 11 tumor=20 cells cultured on HPMECs and could largely replicate the = findings=20 obtained on HUVECs, but with one notable exception: A431 lung = carcinoma cells that remain noninvasive on HUVECs became = clearly=20 invasive when cultured on HPMECs (Fig. = 2). This=20 finding suggests that endothelial cells from different organs = differ=20 in their barrier function against specific tumor cell types = and=20 thereby guide these tumor cells to metastasize preferentially = in=20 different organs (413DGo).=20 However, given the large diversity of tumor cell lines tested = in this=20 study, any arbitrary choice of an organ-specific = microvascular=20 endothelial cell would unnecessarily complicate the = transmigration=20 assay for reasons of limited supply, reduced proliferation, = and=20 longer culture time, poorer monolayer formation, need for = increased=20 serum and growth factor concentrations in the culture medium, = and the=20 need to use cells in higher passages. For our experiments, = especially=20 for the formation of a closed monolayer, it was crucial that = HUVECs=20 were freshly isolated for each experiment and that they were = not=20 previously frozen and were unpassaged.

The most important finding of our study is that the endothelium=20 formed a barrier only against 9 of 24 invasive cell lines.=20 Unexpectedly, in six other cell lines, the endothelium = substantially=20 increased tumor cell invasion. Previous studies have reported = only a=20 barrier function but not an enhancing function (163DGo).=20 Moreover, 11 cell lines that were noninvasive in the absence = of an=20 endothelium became invasive in its presence (Table = 1).=20 These data support the hypothesis that the endothelium may = act as a=20 key modulator for metastasis formation (93DGo,153DGo,163DGo).=20 We also showed that single or clustered microvascular = endothelial=20 cells that were co-plated at the same time with MDA-MB-231 = tumor cell=20 increased invasiveness, but interestingly, invasiveness = increased=20 even more when an endothelial cell monolayer had already = formed=20 before the addition of tumor cells (Fig. = 2,=20 inset). This raises the question of the mechanism by = which the=20 endothelium is able to selectively modulate tumor cell=20 transmigration.

The degree of tumor cell invasiveness in the absence or presence = of endothelial cells did not depend on the tissue type from=20 which the tumor cells were derived (Table = 1). In=20 contrast to several reports, we found that none of the = invasive tumor=20 cells destroyed or disrupted the endothelial monolayer or=20 induced apoptosis in endothelial cells (73DGo,163DGo,423DGo)=20 (Fig. = 1).=20 Microarray analysis revealed that endothelial cells altered = their=20 gene expression when they were cocultured with tumor cells = (Fig. = 3).=20 The regulation of some of the endothelial cell genes depended = on the ability of the tumor cells to transmigrate through the = endothelium (Fig. = 3).=20 Endothelial cell genes that were upregulated in the presence = of=20 invasive tumor cells included cytoskeletal proteins, = cell-cell=20 adhesion molecules, and the CXC chemokines Gro-β, = IL-8, and=20 I-TAC. This study focused on chemokines and their receptors = as=20 modulators for the interaction between tumor cells and = endothelial=20 cells.

As expected from the microarray data (Fig. = 3), the=20 addition of exogenous Gro-β and IL-8 = significantly increased=20 tumor cell transmigration and invasion. Gro-3D{alpha}=20, = Gro-β, and=20 Gro-3D{gamma} all bind to the same CXCR2 chemokine receptor = and have=20 been reported to enhance melanoma tumor growth (433DGo=96453DGo).=20 IL-8 also binds to the CXCR2 chemokine receptor and = reportedly=20 increases invasiveness of PC-3 prostate carcinoma cells (223DGo).=20 FACS analysis of all 51 tumor cell lines revealed that = invasive tumor=20 cells expressed significantly more CXCR2 than noninvasive = tumor=20 cells (Fig. = 5). This=20 is consistent with previous studies that have shown that = malignant=20 PC-3 prostate carcinoma cells and prostate tumors at an = advanced=20 disease stage express increased levels of CXCR2 (223DGo,463DGo,473DGo).

Interactions between the CXCR2 receptor on endothelial cells = and=20 CXCR2 ligand secretion by tumor cells have been reported to = increase=20 metastasis formation by enhancing angiogenesis (453DGo,483DGo). However, the HUVECs and HPMECs used in our=20 experiments did not express detectable amounts of CXCR2 (Fig. = 4).=20 Therefore, in contrast to the previously identified = interaction=20 pathway, we attribute the increased tumor cell transmigration = and=20 invasion to an increased CXCR2 expression on tumor cells that = are=20 being stimulated by increased concentrations of = Gro-β and=20 IL-8 produced by endothelial cells. Other chemokines and = their=20 receptors, including the I-TAC receptor CXCR3, as well as the = MCP-1=20 receptor CCR2, were expressed in noninvasive and invasive = tumor=20 cells at similar levels (Fig. = 4). This=20 is consistent with our finding that exogenous I-TAC and MCP-1 = chemokines did not enhance tumor cell invasion, and indeed, = I-TAC=20 even reduced tumor cell invasion in the absence of an = endothelium (Fig. = 3). Of=20 all the tumor cells tested, only the interactions between = CXCR2 and=20 its chemokine ligands were conspicuous and provide, = therefore, a=20 common mechanism for enhancing tumor cell invasion in the = presence of=20 endothelial cells.

To further analyze the function of the CXCR2 chemokine receptor, = variants of MDA-MB-231, 786-O, and DU145 carcinoma cells were = established that expressed high and low levels of CXCR2 (Fig. = 5).=20 In the absence of an endothelial monolayer, the invasion of=20 CXCR2 high-expressing carcinoma cells was only slightly = increased,=20 but in the presence of an endothelial monolayer, the invasion = was strongly increased (Fig. = 5).=20 MDA-MB-231 cells treated with the CXCR2 inhibitor = SB225002=20 showed nearly complete inhibition of any invasion (Fig. S2). = When=20 CXCR2 was knocked down in MDA-MB-231 cells by siRNA, the = presence of=20 an endothelial cell layer failed to enhance tumor cell = invasiveness=20 (Fig.=20 6).

CXC receptor-ligand interactions are known to initiate a large=20 number of signal transduction pathways involving activation = of=20 Rho, Rac, Cdc42, Erk, Akt, phospholipase C, and=20 inositol-1,4,5-trisphosphate (493DGo,503DGo).=20 This raises the question of possible downstream effects of = pathways=20 that may contribute to a more invasive and motile behavior of = tumor=20 cells. Recent studies have shown that the invasion speed of = tumor=20 cells through a three-dimensional matrix is governed by a = dynamic=20 equilibrium among traction forces, adhesion forces, and = matrix=20 deformation forces (373DGo).=20 In this work, the dynamics and stability of the force = transfer=20 between adhesion receptors and the cytoskeleton were = investigated=20 by analyzing the motion of magnetically forced and unforced=20 fibronectin-coated microbeads. The beads were attached to = integrin=20 receptors of tumor cell variants that expressed low and high = amounts=20 of CXCR2 chemokine receptors (513DGo).=20 Beads on the cells with high CXCR2 expression displayed = behavior that=20 was indicative of an increased rate of adhesion/de-adhesion = and=20 cytoskeletal remodeling events, both of which promote cell = invasion=20 (37) (Fig. 7, = A=20 and B). At the same time, high-CXCR2 cells = generated=20 substantially higher contractile and adhesive forces and = hence should=20 be able to propel themselves more forcefully through an = extracellular=20 matrix (Fig. 7, = C=20 and D).

In summary, we found that, in the presence of invasive tumor=20 cells, Gro-β and IL-8 chemokines were upregulated in=20 endothelial cells and that CXCR2 receptors were highly = expressed on=20 invasive tumor cells, regardless of the tissue origin of the = tumor.=20 The interactions between CXCR2 and Gro-β or IL-8 = lead to=20 higher tractions and enhanced dynamics of cytoskeletal = remodeling=20 processes in tumor cells and represent a generic mechanism = for the=20 breakdown of the endothelial barrier function against tumor = cell=20 invasion.


3D"   =20 SUPPLEMENTARY MATERIAL
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
3D"SUPPLEMENTARY MATERIAL
ACKNOWLEDGEMENTS
REFERENCES
 
T= o view=20 all of the supplemental files associated with this article, = visit http://www.biophysj.org/. =


3D"   =20 ACKNOWLEDGEMENTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
SUPPLEMENTARY MATERIAL
3D"ACKNOWLEDGEMENTS
REFERENCES
 
W= e thank=20 Ludger Klein-Hitpass for help with the microarray analysis, = Peter=20 Altevogt for the kind gift of A125 and KS cells, Barbara = Reischl for=20 excellent technical assistance, Robert Schmiedl for help with = scanning EM imaging, Julia Resch and Joachim Kaschta for = rheology=20 measurements of collagen gels, and Wolfgang H. Goldmann for = critical=20 comments. This work was supported by Deutsche Krebshilfe = (107384),=20 DFG (MA 534/20-4), and NIH (HL65960).


3D"   =20 FOOTNOTES
 
Editor: Cristobal G. dos Remedios. =

Submitted on June 11, 2007; accepted for publication = November 6,=20 2007.


3D"   =20 REFERENCES
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
SUPPLEMENTARY MATERIAL
ACKNOWLEDGEMENTS
3D"REFERENCES
&nb= sp;
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2. Langley, R. R., and I. J. Fidler. = 2007.=20 Tumor cell-organ microenvironment interactions in the pathogenesis of = cancer=20 metastasis. Endocr. Rev. 28:297=96321.[Abstract/Free Full Text]

3. Steeg, P. S. 2006. Tumor = metastasis:=20 mechanistic insights and clinical challenges. Nat. Med. = 12:895=96904.[CrossRef][Medline]

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To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_00C5_01C89197.81C46480 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.biophysj.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-type") {=0A= e.style.layoutGridType =3D value;=0A= }=0A= else if (name =3D=3D "left") {=0A= e.style.left =3D value;=0A= }=0A= else if (name =3D=3D "letter-spacing") {=0A= e.style.letterSpacing =3D value;=0A= }=0A= else if (name =3D=3D "line-break") {=0A= e.style.lineBreak =3D value;=0A= }=0A= else if (name =3D=3D "line-height") {=0A= e.style.lineHeight =3D value;=0A= }=0A= else if (name =3D=3D "list-style") {=0A= e.style.listStyle =3D value;=0A= }=0A= else if (name =3D=3D "list-style-image") {=0A= e.style.listStyleImage =3D value;=0A= }=0A= else if (name =3D=3D "list-style-position") {=0A= e.style.listStylePosition =3D value;=0A= }=0A= else if (name =3D=3D "list-style-type") {=0A= e.style.listStyleType =3D value;=0A= }=0A= else if (name =3D=3D "margin") {=0A= e.style.margin =3D value;=0A= }=0A= else if (name =3D=3D "margin-bottom") {=0A= e.style.marginBottom =3D value;=0A= }=0A= else if (name =3D=3D "margin-left") {=0A= e.style.marginLeft =3D value;=0A= }=0A= else 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