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doi:10.1016/j.ccr.2006.03.003    = ;3D"How  =20

Article

Neuronal and glioma-derived stem cell factor induces angiogenesis = within the=20 brain

Lixin Sun1,=20 Ai-Min Hui1,=20 Qin Su1,=20 Alexander Vortmeyer2,=20 Yuri Kotliarov1,=20 Sandra Pastorino1,=20 Antonino Passaniti3,=20 Jayant Menon1,=20 4,=20 Jennifer Walling1,=20 Rolando Bailey1,=20 Marc Rosenblum5,=20 Tom Mikkelsen5=20 and Howard A. Fine1,=20 ,
1Neuro-Oncology=20 Branch, National Cancer Institute/National Institute of Neurological = Disorders=20 and Stroke, National Institutes of Health, Bethesda, Maryland = 20892
2Neurosurgery Department, National Institute = of=20 Neurological Disorders and Stroke, National Institutes of Health, = Bethesda,=20 Maryland 20892
3Greenebaum Cancer = Center,=20 University of Maryland School of Medicine, Baltimore, Maryland = 21201
4Howard Hughes Medical Institute-National = Institutes of=20 Health Research Scholars Program, 1 Cloister Court, Bethesda, Maryland=20 20814
5Hermelin Brain Tumor Center, = Departments=20 of Neurology and Neurosurgery, Henry Ford Hospital, Detroit, Michigan = 48202=20
Received 27 June 2005;  revised 26 January 2006;  accepted = 3 March=20 2006.  Published: April 10, 2006.  Available online 10 April = 2006.=20

Summary

Stem cell factor (SCF) is overexpressed by neurons following brain = injury as=20 well as by glioma cells; however, its role in gliomagenesis remains = unclear.=20 Here, we demonstrate that SCF directly activates brain microvascular = endothelial=20 cells (ECs) in vitro and induces a potent angiogenic response in vivo. = Primary=20 human gliomas express SCF in a grade-dependent manner and induce normal = neurons=20 to express SCF in brain regions infiltrated by glioma cells, areas that=20 colocalize with prominent angiogenesis. Downregulation of SCF inhibits=20 tumor-mediated angiogenesis and glioma growth in vivo, whereas = overexpression of=20 SCF is associated with shorter survival in patients with malignant = gliomas.=20 Thus, the SCF/c-Kit pathway plays an important role in tumor- and normal = host=20 cell-induced angiogenesis within the brain.


Author Keywords:CELLCYCLE


Article Outline

SIGNIFICANCE
Introduction
Results
Aberrant=20 expression of SCF in gliomas
Effects=20 of SCF on brain microvascular EC
SCF/c-Kit=20 activates signal transduction in EC
SCF=20 promotes angiogenesis in vivo
Silencing=20 SCF attenuates glioma angiogenesis
SCF=20 effects on survival in intracranial tumor model
Biological=20 and clinical significance of SCF in glioma-infiltrated human = cerebral=20 cortex
Discussion
Experimental=20 procedures
Cell=20 culture
Thymidine=20 incorporation
EC=20 proliferation
EC=20 differentiation assay
Wound=20 healing assay
Flow=20 cytometry analysis
Immunoprecipitation=20 and immunoblotting
ELISA
Microarray=20 analysis
Real-time=20 RT-PCR
Expression=20 vector and transduction
In=20 vivo angiogenesis assay and intracranial tumor model
Immunohistochemistry
In=20 situ hybridization
Statistical=20 analysis
Acknowledgements
Supplemental=20 data
Accession=20 numbers
References

SIGNIFICANCE

Tumor angiogenesis is a hallmark of malignant gliomas and is = thought=20 to play an important role in glioma progression. SCF expression in = glioma cells=20 has been reported, but its significance remains unclear. We have now=20 demonstrated that SCF expression, both by neurons as well as by = infiltrating=20 glioma cells, results in a marked angiogenic response in vivo. = Downregulation of=20 SCF expression in vivo results in improved survival in orthotopic mouse = glioma=20 models, whereas overexpression of SCF is associated with a worse = prognosis in=20 patients with glioblastoma. This work, therefore, shows that SCF, = expressed by=20 both tumor and normal host cells, is an important antiangiogenic target = in=20 malignant gliomas and possibly other SCF-expressing tumors.

Introduction

Malignant gliomas are among the most lethal tumors, with median = survivals of=20 less than a year for patients with the most common type of glioma, = glioblastoma,=20 despite aggressive surgery, radiation, and chemotherapy. In an attempt = to=20 identify novel therapeutic targets, many investigators have focused on = the=20 profound angiogenic response associated with malignant gliomas (Plate=20 and Risau, 1995). Tumor-induced angiogenesis is one of the = pathological=20 hallmarks of malignant gliomas and has been demonstrated experimentally = to be=20 important for glioma progression. Thus, antiangiogenic strategies have = great=20 potential as a treatment approach for gliomas (Stratmann=20 et al., 1997, Tanaka=20 et al., 1998 and Purow=20 and Fine, 2004). Identification of the most important angiogenic = pathways=20 utilized by gliomas is therefore of interest and significance.

It has been shown that many putative angiogenic factors are expressed = by=20 glioma cell lines in vitro; however, few of these factors (with the = possible=20 exception of vascular endothelial growth factor [VEGF]), have been = conclusively=20 demonstrated to have any pathophysiological role in glioma progression = in vivo=20 (Goldbrunner=20 et al., 2000, Dunn=20 et al., 2000 and Lamszus=20 et al., 2004). This is important, for it is known that tumor = angiogenesis=20 involves a complex interplay between tumor cells, endothelial cells = (ECs), and=20 other host cells as well as their surrounding extracellular matrix (host = stroma)=20 (Liotta=20 et al., 1991, Carmeliet=20 and Jain, 2000, Tlsty=20 and Hein, 2001 and Kalluri,=20 2003). Thus, a putative angiogenic factor may have very different = functions=20 in diverse tissue types and vascular beds. Given the unique = microenvironment and=20 microvascular architecture within the central nervous system (CNS), it = would=20 therefore not be surprising that various cytokines might have very = different=20 biological effects on the angiogenic process within the CNS compared to = that in=20 systemic capillary beds.

Stem cell factor (SCF) expression has been demonstrated in the past = in a=20 number of glioma cell lines, although its significance remains unclear. = We and=20 others have recently reported that various forms of brain injury induce = neuronal=20 expression of SCF, and that SCF mediates neural stem cell (NSC) = migration to the=20 site of cerebral injury (Zhang=20 and Fedoroff, 1999, Jin=20 et al., 2002, Sun=20 et al., 2004 and Erlandsson=20 et al., 2004). Likewise, recent data demonstrate that hepatic injury = induces=20 SCF production and that SCF in turn promotes liver regeneration, an=20 angiogenesis-dependent process (Ren=20 et al., 2003 and Greene=20 et al., 2003). Consistent with a potential role in angiogenesis, the = SCF=20 receptor c-Kit is found on circulating endothelial precursor cells and = human=20 umbilical vein EC (HUVEC) (Broudy=20 et al., 1994, Peichev=20 et al., 2000 and Matsui=20 et al., 2004). We hypothesized that, as an adoptive response to=20 tumor-induced brain injury, CNS host cell (i.e., neuron)-mediated SCF = expression=20 contributes to glioma-derived SCF expression in inducing a proangiogenic = environment within the CNS that is conducive to tumor progression.

In this study, we demonstrate that SCF is a potent angiogenic factor = in vitro=20 and in vivo. Furthermore, SCF expression is upregulated in gliomas in a=20 grade-dependent manner, and tumor cells with the strongest SCF = expression, as=20 well as normal SCF-expressing neurons, are found predominantly within = the=20 infiltrating tumor border, an area that colocalizes with prominent = angiogenesis.=20 High SCF expression is associated with shorter patient survival, and=20 downregulation of SCF expression in glioma cells suppresses = glioma-induced=20 angiogenesis and improves survival of the mice bearing intracranial = glioma=20 xenografts. Thus, the SCF/c-Kit pathway plays a prominent role in = pathological=20 angiogenesis within the CNS and may provide a promising molecular target = for=20 glioma treatment.

Results

Aberrant expression of SCF in gliomas

Under normal conditions, little or no SCF expression is detectable in = the=20 normal brain (Zhang=20 and Fedoroff, 1999 and Manova=20 et al., 1992). To evaluate whether SCF is associated with the = prominent=20 angiogenesis seen in malignant gliomas, we first determined SCF = expression=20 levels in human malignant glioma cell lines. Quantitative real-time = RT-PCR=20 revealed high levels of both the secreted SCF (sSCF) and = membrane=20 bound SCF (mSCF) mRNA splicing isoforms in all glioma = cells=20 examined (Figure=20 1A). We further demonstrate by ELISA that high levels of SCF protein = are=20 secreted into the conditioned media (CM) by glioma cell lines in = contrast to=20 very low levels found in the CM from normal human astrocytes in vitro = (Figure=20 1B). Additionally, lysates of glioma cell lines reveal high levels = of SCF=20 protein as detected by immunoblotting (Figure=20 1C). The three bands seen on the Western blot correspond to the sSCF = (33=20 kDa), cleaved fraction of sSCF (19 kDa), and mSCF (29 kDa).=20

Display=20 Full Size version of this image = (96K)

Figure 1. Aberrant expression of SCF in gliomas

A=E2=80=93C: Expression of the two splicing = isoforms of SCF in=20 human glioma cell lines. A: sSCF and = mSCF were=20 determined by real-time PCR with isoform-specific probe sets, = respectively.=20 B: Secreted SCF in cell conditioned media was = measured using=20 ELISA and normalized by total protein. C: Western = blot=20 analysis of SCF expression. Tubulin was used as a loading control. = Note that=20 both SCF isoforms are expressed at higher levels by glioma = cells than=20 by normal astrocytes.

D and E: SCF mRNA is overexpressed in = primary human=20 high-grade glioma specimens. D: cDNA microarray = analysis of=20 differential SCF expression in gliomas according to WHO grades. = Note=20 the positive correlation of SCF expression with increasing = grade (grade=20 III and IV gliomas compared to nontumor brain [NB]; **p = <=20 0.001). E: Increased SCF mRNA in high-grade = gliomas=20 was confirmed by real-time RT-PCR. Grade II oligodendroglioma (n =3D = 9) and=20 astrocytoma (n =3D 9); grade III, anaplastic oligodentrocytoma (n =3D = 8),=20 anaplastic astrocytoma (n =3D 9); grade IV (n =3D 28); NB (n =3D 9). = (*p=20 < 0.05). Relative message indicates the ratio of SCF to=20 =CE=B2-actin.

Columns and bars show the mean and SEM, respectively.=20

In order to evaluate the level of SCF expression in primary = human=20 gliomas, rather than in just cell lines, we performed mRNA expression = profiling=20 of 157 primary human gliomas and 23 nontumor human brain samples using = the=20 Affymetrix Human Genome U-133 plus 2.0 GeneChip. A total of four probe = sets=20 corresponding to the SCF gene are present, and Figure=20 1D demonstrates the data from a typical probe set showing a = significant=20 elevation of SCF message in gliomas in comparison to nontumor = brain (p=20 < 0.001). High-grade gliomas differ significantly from low-grade = gliomas both=20 biologically and genetically. Thus, we investigated the levels of = SCF=20 expression in gliomas of different grades. The results revealed a = statistically=20 significant higher level of SCF expression in high-grade gliomas = (grade=20 III or anaplastic astrocytoma, n =3D 31; grade IV astrocytoma or = glioblastoma, n =3D=20 81) compared to low-grade gliomas (grade II astrocytoma, n =3D 45) or = normal brain=20 (n =3D 23) (p < 0.001) (Figure=20 1D). The microarray expression data were confirmed by quantitative = real-time=20 RT-PCR demonstrating a significant elevation of SCF in grade IV = gliomas=20 compared to low-grade gliomas or nontumor brain (p < 0.05) (Figure=20 1E). Since high-grade gliomas are characterized by a much greater = amount of=20 tumor-associated angiogenesis compared to low-grade gliomas, the = positive=20 correlation of SCF expression with increasing glioma grade is consistent = with a=20 potential role for SCF in glioma-associated angiogenesis.

Effects of SCF on brain microvascular EC

Even though the SCF receptor c-Kit is often expressed on glioma cells = in=20 vitro (Natali=20 et al., 1992, Tada=20 et al., 1994 and Stanulla=20 et al., 1995), even high concentrations of SCF failed to induce=20 proliferation in our glioma cells in vitro, consistent with previous=20 observations (data not shown) (Berdel=20 et al., 1992 and Stanulla=20 et al., 1995). Given the lack of effect of SCF on glioma cell growth = in=20 vitro, yet the positive correlation between glioma grade and higher = levels of=20 SCF expression, we reasoned that SCF might be involved in glioma = progression in=20 vivo through some indirect or paracrine mechanism. To explore the = possibility=20 that this indirect effect was a proangiogenic one, we first set out to = determine=20 whether c-Kit was expressed on primary ECs in vitro. All ECs examined = exhibited=20 c-Kit protein on their cell surfaces by FACS analysis, including bovine = brain=20 microvascular EC (BMVEC-b), HUVEC, and human dermal microvascular EC = (HMVEC-d)=20 (Figure=20 2A). By contrast, all of seven glioma cell lines demonstrated the = presence=20 of intracytoplasmic but little membrane bound c-Kit (Figures=20 S1A and S1B in the Supplemental=20 Data available with this article online; Table=20 S1).=20

Display=20 Full Size version of this image = (241K)

Figure 2. SCF promotes angiogenesis in vitro

A: c-Kit expression in ECs was determined by FACS = in=20 BMVEC-b, HUVEC, and HMVEC-d cells. The blue shaded histograms = represent the=20 fluorescence intensity of c-Kit, and the black line indicates the = control IgG=20 isotype staining. SK-N-SH and NIH3T3 cells were used as positive and = negative=20 controls, respectively (NIH3T3 not shown).

B: SCF alone sustained EC proliferation and = survival as=20 determined by thymidine incorporation.

C: HBMEC also showed dose-dependent growth in the = presence=20 of SCF.

D=E2=80=93F: SCF activates brain microvascular = ECs.=20 D: In the presence of SCF, BMVEC-b migrated into the = denuded=20 zone 18 hr after scraping. Arrows indicate the wound edge. = E:=20 Total cells in denuded zone were counted from three separate fields in = each=20 well from triplicates. F: BMVEC-b formed tubular = structures=20 on Matrigel in the presence of SCF but not in controls.

G: The U251-derived CM significantly increased = HUVEC=20 proliferation in culture, an effect nearly completely blocked by = neutralizing=20 antibodies to either SCF or VEGF. Scale bar, 200 =CE=BCM.

Columns and bars show the mean and SEM, respectively.=20

We next exposed BMVEC-b, HUVEC, and HMVEC-d in basal medium to SCF = and=20 determined the rate of thymidine incorporation at 48 hr or 72 hr. SCF = stimulated=20 proliferation in all three primary ECs in a dose-dependent manner even = at low=20 concentrations (i.e., BMVEC-b proliferation increased approximately = 6-fold and=20 7-fold following exposure to 1 ng or 10 ng of SCF per ml for 72 hr,=20 respectively) (Figure=20 2B). Additionally, we exposed human brain microvascular EC (HBMEC) = to=20 various concentrations of SCF (from 0.1 to 10 ng per ml) and = demonstrated a=20 similar dose-dependent pro-proliferative response to that seen with the = BMVEC-b=20 (Figure=20 2C). It is particularly noteworthy that SCF alone, without the = addition of=20 other cytokines such as VEGF, was sufficient to sustain human brain=20 microvascular EC and other EC cell growth and survival.

We next used a wound healing assay and Matrigel tube formation assay = to=20 further characterize the effects of SCF on BMVEC-b migration and = differentiation=20 in vitro. SCF induced a 2- to 3-fold increase in BMVEC-b migration = compared to=20 control in a dose-dependent manner (Figures=20 2D and 2E). Additionally, SCF induced BMVEC-b and HBMEC to migrate = in=20 Matrigel within 4 hr of exposure and to form mature appearing = capillary-like=20 structures by 18 hr. By contrast, these primary human and bovine brain = ECs=20 exposed to the vehicle control neither migrated nor formed = capillary-like=20 structures (Figure=20 2F). In order to establish whether glioma cells could be exerting a=20 proangiogenic effect on neighboring ECs through SCF and other angiogenic = proteins, we evaluated the effects of glioma cell CM on EC = proliferation. EC=20 proliferation increased 5-fold following exposure to glioma CM compared = to basal=20 media. Blocking antibodies to both SCF and VEGF were able to abolish the = mitogenic effects of the glioma CM on EC proliferation (Figure=20 2G). These data demonstrate the ability of SCF to induce = proliferation,=20 migration, and differentiation of primary brain microvascular ECs in = vitro.

SCF/c-Kit activates signal transduction in EC

SCF-mediated c-Kit signaling has been shown to induce activation of = the=20 mitogen-activated protein kinase (MAPKs) and phosphoinositide 3-kinase=20 (PI3K)/Akt pathways in known SCF target cells (Jin,=20 2005). A recent report suggests that SCF stimulates a HUVEC = angiogenic=20 response through activation of these pathways (Matsui=20 et al., 2004). We investigated whether SCF could induce these two = pathways=20 specifically in primary brain ECs rather than just in HUVEC. Confluent = BMVEC-b=20 and HUVEC cells were treated with SCF after serum starvation. SCF = rapidly=20 induced c-Kit auto-tyrosine-phosphorylation, which peaked at = 10=E2=80=9315 min and=20 lasted for 30 min following exposure (Figure=20 3A). Additionally, phosphorylation of MEK1/2, as well as its = downstream=20 p44/42 MAPK, was dramatically increased. SAPK/JNK was similarly = activated 10=E2=80=9315=20 min following SCF exposure, whereas p38 MAPK exhibited a prolonged = activation=20 for over 30 min.=20

Display=20 Full Size version of this image = (124K)

Figure 3. SCF/c-Kit activates MAPKs and Akt pathways in brain=20 microvascular ECs

Cell lysates were collected at the indicated times after SCF = stimulation of=20 BMVEC-b and HUVEC (A) as well as HBMEC = (B)=20 and analyzed by Western blot with the indicated anti-phosphorylated = protein=20 antibodies as well as anti-total protein antibodies. Arrows: red,=20 phosphorylated protein; blue, total protein. Tubulin was used as an = equal=20 loading control.=20

Like the MAPK pathway, the PI3K pathway was activated following = BMVEC-b and=20 HUVEC exposure to SCF. Phosphorylation of Akt was significantly enhanced = by SCF=20 treatment, which in turn resulted in phosphorylation of mTOR. Activation = of mTOR=20 increased phosphorylation of 4E-BP1 consistent with a possible = diminished=20 inhibition of 4E-BP1 on eIF4E, which could result in diminished = cap-dependent=20 translation. Thus, SCF activates the MAPK and PI3K pathways in BMVEC-b = in a=20 manner similar to its effects on HUVEC.

Additionally, SCF (50 ng/ml) induced immediate phosphorylation of the = c-Kit,=20 p44/42 MAPK, and Akt proteins in HBMECs (Figure=20 3B). Thus, SCF-induced activation of the MAPK and PI3K pathways = appears to=20 occur in ECs from both systemic capillary beds as well as from the = brain. In=20 contrast to BMVEC-b, SCF could not induce phosphorylation of p38 MAPK = and=20 SAPK/JNK in HBMEC (data not shown). Whether this represents a = species-specific=20 difference in SCF-mediated signaling or reflects different subtypes of = ECs from=20 the brain remains to be determined.

SCF promotes angiogenesis in vivo

We next evaluated whether SCF has proangiogenic activity in vivo by=20 subcutaneously implanting Matrigel impregnated with SCF, =CE=B2-FGF = (positive=20 control), or vehicle alone into the adult SCID mice. Newly formed blood = vessels=20 in the Matrigel plugs were visualized by hematoxylin/eosin (H&E) = staining=20 and confirmed by immunofluorescent staining for factor VIII-related = antigen=20 (vWF)-positive ECs. In addition, Tie2 protein levels in the Matrigel = plugs were=20 determined. Fourteen days after injection, vehicle control-impregnated = Matrigel=20 plugs demonstrated few vWF-positive vessels and had essentially no = detectable=20 Tie2 protein expression (Figure=20 4). By contrast, SCF (as well as the positive control =CE=B2-FGF) = induced=20 substantial angiogenesis, as demonstrated by abundant intact blood = vessels as=20 well as high Tie2 expression within the SCF-containing Matrigel plug. = These data=20 demonstrate that SCF can promote angiogenesis in vivo.=20

Display=20 Full Size version of this image = (205K)

Figure 4. A high density of blood vessels was induced in SCF- = or=20 =CE=B2-FGF-supplemented Matrigel plugs

A: H&E staining. Scale bars, 500 =CE=BCM (LP), = 50 =CE=BCM (HP).

B: Immunofluorescence staining for vWF. Scale = bars, 100 =CE=BCM=20 (LP), 50 =CE=BCM (HP).

C: Western blot for Tie2 in homogenates of = Matrigel plugs.=20 Arrows: neovasculature containing red blood cells. LP, low power; HP, = high=20 power; M, muscle; S, skin; G, gel.=20

Silencing SCF attenuates glioma angiogenesis

To evaluate the effect of SCF on glioma angiogenesis and progression, = we=20 engineered glioma cells expressing low levels of SCF by retrovirally = transducing=20 an antisense SCF construct or a SCF shRNA into wild-type = U373,=20 U87, and U251 glioma cells expressing high levels of SCF. The resulting = U373=20 cell line (U373/as-SCF), U87 cell line (U87/as-SCF), and U251 cell line=20 (U251/shRNA SCF) were expanded, and then stable low level-expressing = clones were=20 selected by antibiotics and verified by Western blot (Figure=20 5A). To avoid the confounding variable of concurrent VEGF = expression, we=20 verified by Western blots that suppression of SCF expression in our = cloned=20 glioma cell lines had no effects on VEGF expression (Figure=20 5A). Next, we implanted U373/as-SCF or U373/vector cell lines = together with=20 Matrigel subcutaneously into SCID mice in order to assess glioma-induced = angiogenesis in vivo with and without SCF stimulation. Within 2 weeks, a = profound angiogenic response was seen in the Matrigel containing the = control=20 U373/vector cells with multiple vWF-positive perfused vessels and = abundant Tie2=20 protein in the Matrigel plug homogenates. By contrast, Matrigel = containing the=20 U373/as-SCF cells demonstrated far fewer capillaries with vWF staining = and=20 significantly less Tie2 protein in the plug homogenates (Figures=20 5B=E2=80=935D). Thus, suppression of SCF in glioma cells results in = significant=20 inhibition of glioma-induced angiogenesis in vivo. Consistent with these = observations, U251/as-SCF did not form palpable subcutaneous tumors = several=20 weeks after implantation, in contrast to their matched U251/vector = cells, which=20 formed tumors so large that animals needed to be euthanized (Figure=20 S2). Likewise, systemically administered bevacizumab (Genentech, San = Francisco, CA) inhibited U251/vector produced VEGF resulting in profound = tumor=20 growth suppression. We could not, however, demonstrate an additive or=20 synergistic effect of SCF knockdown and VEGF inhibition, since SCF = knockdown=20 alone resulted in complete tumor growth inhibition (Figure=20 S2).=20

Display=20 Full Size version of this image = (167K)

Figure 5. Suppression of SCF in U373 glioma cells attenuates=20 U373-mediated angiogenesis

A: Downregulation of SCF in U373/as-SCF, = U87/as-SCF, and=20 U251/shRNA SCF was verified by Western blot. Downregulation of SCF = resulted in=20 no effects on VEGF expression from the cells.

B and C: Immunofluorescence staining for vWF=20 (B) and H&E staining (C) in an = in vivo=20 tumor-angiogenesis assay using U373/as-SCF and U373/vector glioma = cells. Scale=20 bars, 100 =CE=BCM (LP in B), 500 =CE=BCM (LP in = C), 50=20 =CE=BCM (HP).

D: Tie2 protein in homogenates of Matrigel plugs = (40 mg=20 total protein in each sample) was immunoprecipitated with Tie2 = antibody and=20 then detected by Western blot in duplicate. The comparative = quantitative=20 intensities of the amount of Tie2 protein were measured by = densitometry.=20 Arrows: neovasculature containing red blood cells. LP, low power; HP, = high=20 power; M, muscle; S, skin; G, gel. Columns and bars show the mean and = SEM,=20 respectively.=20

SCF effects on survival in intracranial tumor model

We next evaluated whether suppression of SCF would affect the = survival of=20 animals with intracranial gliomas. U373/as-SCF or U373/vector cells, = U87/as-SCF=20 or U87/vector cells, and U251/shRNA SCF or U251/vector cells were=20 stereotactically implanted into the cerebral subcortex of adult athymic=20 nu/nu mice. Log-rank analysis of the Kaplan-Meier survival curves = demonstrated a significant survival advantage for the SCF low-expression = glioma-bearing mice compared to their matched SCF high-expression = parental=20 vector-infected glioma-bearing animals (p < 0.05) (Figure=20 6A). Examination of 4-week-old U373/vector intracranial tumors = demonstrated=20 significant SCF expression within the tumor cells and a robust = angiogenic=20 response. By contrast, there was significantly lower SCF expression = within the=20 tumor cells of the intracranial U373/as-SCF tumors with an attenuated = angiogenic=20 response within the tumor (Figure=20 6B).=20

Display=20 Full Size version of this image = (263K)

Figure 6. Downregulation of SCF expression in glioma cells = impedes=20 tumor angiogenesis and prolongs survival in an intracranial tumor = model

A: Kaplan-Meier survival curve shows that = downregulation=20 of SCF expression in U373/as-SCF, U87/as-SCF, and U251/shRNA SCF = tumors=20 significantly improves survival of tumor-bearing mice compared with = their=20 vector controls, respectively (log-rank test p < 0.05).

B: Downregulation of SCF expression attenuates = SCF-induced=20 angiogenesis in implanted glioma tumors. In contrast to U373/vector = gliomas,=20 the U373/as-SCF gliomas demonstrate little SCF staining and a markedly = lower=20 density of blood vessels. Scale bars, 200 =CE=BCM (LP); 50 =CE=BCM = (HP).

C: Colocalization of neovasculature with SCF in=20 U373/vector tumors. Tumor tissue shows strong SCF expression and a = high=20 density of collapsed vessels (upper panels). Along the tumor invasion = border=20 (middle panels), abundant SCF surrounds tumor cluster with multiple = small=20 vessels in the center. In brain tissue adjacent to the tumor mass = (lower=20 panels), SCF is expressed both by tumor cells and normal cells within = the=20 brain. Scale bar, 50 =CE=BCM.

D and E: Intracranial tumor induces SCF expression = in=20 affected neurons. D: SCF-positive neurons = (arrows) are=20 seen in the cerebral cortex infiltrated by tumor (T) as detected by in = situ=20 hybridization using a SCF antisense probe (left). The negative = control=20 using a hybridized sense probe is seen on the right. = E:=20 SCF-expressing cells are present in the cerebral cortex close to = U373/as-SCF=20 injection (left) as compared to the contralateral side of the brain = (right) as=20 analyzed by immunohistochemistry. Arrows: red, SCF staining; blue, = vWF+ blood=20 vessels. Scale bars, 50 =CE=BCM.=20

Immunohistological staining demonstrated that, although SCF is = generally=20 expressed in most tumor cells within the central U373/vector tumor mass, = SCF=20 expression was most marked in tumor cells within the tumor border and in = the few=20 infiltrating glioma cells at the invasion front. Increased SCF = expression was=20 also observed in the normal brain tissue adjacent to the tumor mass (Figure=20 6C). In situ hybridization for SCF mRNA revealed that it was = the=20 normal host neurons within the cerebral cortex, adjacent to the invading = tumor=20 mass, that accounted for the non-tumor cell-associated high-level = SCF=20 expression (Figure=20 6D). Additionally, a similar pattern and level of normal neuronal=20 overexpression of SCF was seen in cortex immediately adjacent to = U373/as-SCF=20 tumors despite the fact that the actual tumor cells made very little SCF = (in=20 contrast to the U373/vector cells). Normal neurons at increasingly = farther=20 distances from the tumor site, however, demonstrated progressively less = SCF=20 expression, such that SCF expression was barely detectable in neurons = within the=20 cortex contralateral to the growing tumor mass (Figure=20 6E). Together, these results support a role for tumor cell and = normal host=20 neuron-mediated SCF-induced tumor angiogenesis in glioma progression.

Biological and clinical significance of SCF in = glioma-infiltrated=20 human cerebral cortex

To evaluate whether the patterns of glioma-associated SCF expression = in the=20 intracranial mouse xenograft model reflected patterns seen in human = brains with=20 malignant gliomas, we performed extensive immunohistochemical analysis = of=20 surgical specimens from patients with glioblastoma. We observed = generally four=20 important features of the heterogeneous SCF expression in the brains of = patients=20 with glioblastoma. In some areas, close to the center of tumor mass, = very little=20 or no SCF was detected (Figure=20 7A). SCF was generally expressed at high levels by glioma cells = infiltrating=20 into the cerebral white matter (Figure=20 7B). In the glioma-infiltrated cerebral cortex abundant SCF = expression was=20 seen not only in the tumor cells, but also in normal host neurons (Figure=20 7C). Thus, there was profound expression of SCF in cerebral cortex=20 infiltrated by glioma cells secondary to both tumor- and normal host=20 neuron-associated SCF expression (Figure=20 7D). In summary, SCF expression appears to reside most prominently = in the=20 invasive front of the infiltrating glioma, suggesting its roles in tumor = progression. Most notably, this area of high SCF expression colocalizes = with=20 areas of dense microvasculature sprouting and branching, consistent with = a role=20 for SCF in glioma- and normal host neuron-mediated angiogenesis (Figure=20 7E). In addition, abundant c-Kit expression was also detected on the = glioblastoma-associated ECs but little on the actual tumor cells, = consistent=20 with our in vitro data (Figure=20 7F). The clinical significance of these findings is reflected by the = fact=20 that patients with glioblastoma (grade IV; n =3D 64), otherwise matched = for known=20 prognostic factors (i.e., age, treatment), who had tumors that expressed = high=20 levels of SCF experienced significantly shorter survival than = patients=20 with tumors expressing relatively low levels of SCF (p =3D 0.0004 = by=20 log-rank analysis; Figure=20 7G). By contrast, VEGF expression levels did not correlate = with=20 survival in patients with glioblastoma (p =3D 0.24).=20

Display=20 Full Size version of this image = (271K)

Figure 7. Distribution of SCF expression in human brain = harboring a=20 glioblastoma

A=E2=80=93D: SCF-expressing cells by = immunohistochemistry in=20 representative regions of brain and tumor. A: Center = of tumor=20 mass. B: Cerebral white matter infiltrated by tumor = cells.=20 C: Cerebral cortex with infiltration of tumor cells.=20 D: Cellular tumor adjacent to white matter. Scale = bars (shown=20 in D), 100 =CE=BCM (LP), 50 =CE=BCM (HP).

E: SCF-expressing tumor cells surrounding new = blood=20 vessels are shown at higher magnification (800=C3=97). The top panels = show the=20 SCF-expressing tumor cells (left) and SCF-negative cells (right) = lining blood=20 vessels, respectively. The middle and bottom panels show = SCF-expressing cells=20 lining the full-length of the blood vessels. Arrowheads indicate = cytoplasmic=20 staining of SCF in tumor cells (black), neuron (red), and the boundary = between=20 tumor mass (TM) and tumor-infiltrating white matter (WM) (green). Note = that=20 SCF-expressing tumor cells are more pronounced in the tumor regions = adjacent=20 to normal brain and along the new blood vessels. Scale bars, 25 = =CE=BCM.

F: c-Kit-positive endothelial cells on the=20 glioblastoma-associated vasculature colocalized with CD31-positive = endothelial=20 cells (left panels) throughout the tumor, including in areas adjacent = to=20 necrosis (N, right panel). Scale bars, 50 =CE=BCM (left panels), 100 = =CE=BCM (right=20 panel).

G: Kaplan-Meier survival curve demonstrating = survival of=20 patients with glioblastoma (grade IV gliomas) stratified by tumors = expressing=20 either low or high levels of SCF (log-rank analyses p =3D = 0.0004) and=20 expressing low or high levels of VEGF (log-rank analyses p =3D = 0.2458).=20

Discussion

The work reported here describes a role for SCF in tumor-associated=20 angiogenesis and specifically in glioma progression. SCF has been long=20 recognized as an important growth factor for a number of cell types, = including=20 hematopoietic stem cell, mast cells, melanocytes, and germ cells (Zsebo=20 et al., 1990, Galli=20 et al., 1992 and Mackenzie=20 et al., 1997). In these divergent cell types, SCF has been shown to = have a=20 number of different biological properties. A role for SCF as a potential = angiogenic factor, however, has not been previously entertained until a = recent=20 report demonstrated its mitogenic effects on HUVEC cells in vitro (Matsui=20 et al., 2004). We have now expanded on those observations by = demonstrating=20 that SCF has potent mitogen, differentiation, and chemotactic properties = on a=20 variety of primary EC lines in vitro, and furthermore can induce a = robust=20 angiogenic response and contribute to tumor-associated angiogenesis in = vivo.

It has been previously reported that glioma cell lines can express = SCF and=20 c-Kit, implicating SCF as an autocrine growth factor for gliomas (Hamel=20 and Westphal, 2000). Previous observations, however, could not = demonstrate a=20 mitogenic effect of SCF on glioma cells. Thus, the role for SCF in = glioma=20 pathogenesis remained unclear until now. Our data now confirm that SCF=20 expression is not a direct glioma mitogen but rather a potent = glioma-associated=20 angiogenic factor. Although SCF has been previously implicated in = angiogenesis=20 through its ability to regulate mast cell migration with subsequent = release of=20 VEGF (Zhang=20 et al., 2000), no direct role for SCF in angiogenesis had been = previous=20 described except for a recent report of its ability to induce HUVEC=20 proliferation and migration in vitro (Matsui=20 et al., 2004). We have extended those observations by showing that = not only=20 HUVECs, but also primary ECs (including human brain microvascular ECs) = express=20 c-Kit and that SCF-mediated c-Kit signaling in ECs results in activation = of the=20 MAPK and AKT pathway, leading to enhanced proliferation, survival, and = migration=20 of ECs even in the absence of VEGF, =CE=B2-FGF, or other, thought to be = obligate, EC=20 growth factors.

Our data clearly demonstrate the ability of SCF to induce a potent = angiogenic=20 response both subdermally and within the brain. Furthermore, we show = using=20 several different cell lines and using several different methodologies = that=20 downregulation of SCF expression in an orthotopic glioma model results = in=20 diminished angiogenesis and prolongation of animal survival. We believe = that=20 these observations have clinical significance based on our demonstration = that=20 the level of SCF expression in primary human gliomas directly = correlates=20 with the grade of the tumor and patient survival. These data = demonstrating that=20 high-grade gliomas express significantly more SCF than low-grade = gliomas=20 or nontumor human brain tissue are fully consistent with the fact that=20 high-grade gliomas are significantly more angiogenic than low-grade = gliomas. In=20 fact, endothelial proliferation is one of the pathological criteria for = grading=20 a glioma high grade (Kleihues=20 and Cavenee, 2000). Additionally, our demonstration of increased = angiogenic=20 activity colocalizing with increased SCF expression in surgical sections = of=20 human brains with malignant gliomas further supports the relevance of=20 SCF-induced angiogenesis in the pathogenesis of malignant gliomas.

It is becoming increasingly clear that tumorigenesis in vivo involves = not=20 just the biology of the tumor cell itself, but rather a complex = interplay=20 between tumor cells and the deregulation of normal host physiological = functions=20 that ultimately aid in tumor progression (Tlsty=20 and Hein, 2001 and Liotta=20 and Kohn, 2001). Others and we have previously demonstrated that SCF = expression is induced in normal neurons in vivo following various types = of brain=20 trauma (Zhang=20 and Fedoroff, 1999 and Sun=20 et al., 2004). Gliomas cause significant damage to normal brain = parenchyma=20 through numerous mechanisms including disruption of the blood-brain = barrier with=20 resultant increased cerebral edema and increased intracranial pressure,=20 glioma-mediated degradation of the extracellular matrix through = overexpression=20 of metalloproteases, and release of neurotoxic excitatory molecules such = as=20 glutamate (Forsyth=20 et al., 1999, Takano=20 et al., 2001, VanMeter=20 et al., 2001, Davies,=20 2002 and Chantrain=20 et al., 2004). Thus, we wondered whether, along with the direct = release of=20 SCF from glioma cells, tumor growth could be eliciting expression of SCF = from=20 normal brain tissue in a manner analogous to that seen in our brain = injury=20 models. Data from both our orthotopic model and the surgical sections = from human=20 brains with malignant gliomas demonstrate that normal host neurons = within the=20 area of cerebral cortex, adjacent to the tumor mass and within the = invading=20 front of glioma cells, do express SCF to very high levels, whereas = neurons in=20 areas of cortex away from the growing tumor do not. These areas of = neuronal and=20 glioma SCF overexpression overlap precisely with areas of sprouting and=20 branching angiogenesis. Thus, normal host cells within the brain appear = to have=20 been coopted to induce pathological angiogenesis in support of the = infiltrating=20 tumor cells. The expression of SCF by normal host tissue may also help = explain=20 why downregulation of direct glioma SCF expression through our antisense = and=20 siRNA constructs in our orthotopic models decreased glioma-mediated = angiogenesis=20 but did not abolish it and only led to moderately prolonged animal = survival.=20 Full angiogenesis inhibition will likely depend on inhibition of all SCF = expression (or c-Kit inhibition), including both tumor- and normal host=20 neuron-mediated expression, possibly in conjunction with inhibition of = other=20 angiogenic pathways.

These data strongly implicate SCF as an important angiogenic factor = in=20 pathogenesis of malignant gliomas. Among the relatively large number of = factors=20 that have been implicated in glioma-mediated angiogenesis, the most = commonly=20 cited are =CE=B2-FGF, PDGF, and VEGF (Dunn=20 et al., 2000 and Lamszus=20 et al., 2004). Although gliomas clearly express =CE=B2-FGF in a = grade-dependent=20 manner, various studies have failed to find =CE=B2-FGF receptors on = glioma-associated=20 endothelium, leading some to speculate that =CE=B2-FGF is acting more as = a glioma=20 autocrine growth factor rather than an angiogenic factor (Zagzag=20 et al., 1990 and Morrison=20 et al., 1994). The various heterodimer PDGF receptors have been = demonstrated=20 on glioma-associated endothelium; however, PDGF overexpression tends to = occur in=20 low-grade gliomas and higher-grade gliomas that have transformed from = low-grade=20 gliomas rather than in the more common primary glioblastomas (Westermark=20 et al., 1995, Ribom=20 et al., 2002 and Dai=20 et al., 2001). Thus, PDGF may also be playing a largely mitogenic = autocrine=20 role in glioma growth and may not have a major angiogenic function in = the=20 majority of high-grade gliomas. VEGF is the one angiogenic factor that = has=20 clearly been implicated in glioma angiogenesis, as it is highly = overexpressed in=20 most high-grade gliomas and especially in glioblastoma, where its = receptor is=20 overexpressed on glioma-associated endothelium (Berkman=20 et al., 1993 and Hatva=20 et al., 1995). VEGF expression, however, has been demonstrated to be = most=20 pronounced in glioblastoma cells adjacent to areas of necrosis, = consistent with=20 its known hypoxia inducibility (Plate=20 et al., 1992 and Shweiki=20 et al., 1992). These areas of necrosis and relative tumor hypoxia, = however,=20 are not the areas of the most pronounced angiogenesis or most rapid = tumor cell=20 proliferation within a malignant glioma. Rather, it is the invading = border of=20 the tumor that harbors the most prominent angiogenic reaction and tumor = cell=20 proliferation (VanMeter=20 et al., 2001). This is the area that corresponds to the highest SCF=20 expression.

Our interpretation of these data leads us to believe that SCF, along = with=20 VEGF, may have complementary roles in the robust angiogenic response = seen in=20 malignant gliomas. To date, there have been a number of clinical trials = with=20 small molecule inhibitors of FLK-1 (the VEGF receptor); however, none = have yet=20 to show definitive clinical benefit. Although the lack of clinical = success may=20 be secondary to the failings of the individual molecules tested, it is = also=20 plausible to postulate that angiogenic pathways other than or in = addition to=20 VEGF will need to be targeted for clinical success. As such, SCF may = prove to be=20 an important therapeutic target in high-grade gliomas. There has already = been=20 one clinical trial of Imatinib (Gleevec), a small molecular inhibitor of = ABL,=20 PDGF, and c-Kit, in patients with malignant gliomas primarily based on = the=20 premise of targeting PDGF as an autocrine growth factor (Kilic=20 et al., 2000; P.Y. Wen et al., 2002, Proc. Am. Soc. Clin. Oncol., = abstract).=20 The investigators in this trial did not observe any clinical activity = from=20 Imatinib; however, the lack of activity may have been the result of the=20 inability of Imatinib to cross the BBB. Although it has been argued that = one of=20 the theoretical appeals of antivascular and antiangiogenic therapy for = brain=20 tumors is the nonnecessity for molecules to cross the BBB, the reality = is that=20 many of the endothelial targets may not be accessible to BBB-impermeable = molecules within the bloodstream if such targets are present on the = adluminal=20 side of the EC. Indeed, given that the BBB works in both directions, a = large=20 protein such as SCF would not easily cross out of the brain back into = the=20 bloodstream. Thus, it is possible that c-Kit expression may not be = expressed on=20 the side of the endothelial cell facing the blood vessel lumen, thereby = making=20 the receptor inaccessible to BBB-impermeable drugs such as Imatinib. It = remains=20 to be seen whether some of antitumor effects of Imatinib activity = against=20 certain systemic solid tumors, such as gastrointestinal stromal tumors = (GIST),=20 and chronic myelogenous leukemia (CML) may be in part a result of its=20 antiangiogenic as well as its direct antitumor effects (Demetri=20 et al., 2002, Kantarjian=20 et al., 2002 and Sawyers=20 et al., 2002).

In conclusion, we have presented data that demonstrate SCF to be a = potent=20 angiogenic factor both in systemic tissue and within the brain. = Additionally,=20 SCF appears to be an important angiogenic factor in high-grade gliomas, = both=20 through direct tumor cell expression of SCF and through the induction of = its=20 expression by normal host neurons within areas of brain infiltrated by = tumor.=20 Normal neuronal expression of SCF in response to traumatic brain injury = also=20 raises the disturbing possibility that standard invasive procedures such = as=20 surgical biopsies or partial tumor resections may be inducing a = proangiogenic=20 response, or trigger, within the brain. As such, SCF represents a = potentially=20 important therapeutic target for malignant gliomas. Finally, the ability = of=20 normal host neurons to express SCF in response to injury, as well as the = potent=20 angiogenic properties of SCF within the brain, leads one to speculate = that SCF=20 may have important therapeutic potential as a proangiogenic factor in=20 regenerative tissue repair strategies for various disease states such as = stroke=20 and brain and spinal cord injury as well as neurodegenerative = diseases.

Experimental procedures

Cell culture

Primary ECs (Clonetics, Walkersville, MD) and human astrocytes = (Sciencell=20 Research Laboratories, San Diego, CA) were used at passage 8 or earlier. = HBMEC=20 (Sciencell Research Laboratories) was used at passage 1 or 2. All = malignant=20 glioma cells except for 1321N (Europe collection of cell cultures, = Sigma-Aldrich=20 Corp., St. Louis, MO), bone marrow neuroblastoma cell, SK-N-SH, and NIH = 3T3 were=20 purchased from American Type Culture Collection (Manassas, VA). All = cells were=20 passaged and cultured in conditions recommended by their suppliers.

Thymidine incorporation

After ECs (3 =C3=97 103/well) were adhered to 96-well = gelatin-coated=20 plates (BD Discovery Labware, Bedford, MA), the EC growth medium was = replaced by=20 SCF (1.10 ng/ml) (R&D Systems, Minneapolis, MN) suspended in = treatment=20 medium (basal medium with 0.1% BSA) for an additional 48 hr (HUVEC and = HMVEC-d)=20 or 72 hr (BMVEC-b) with renewal of medium at 24 hr interval. ECs were = cultured=20 for 4 hr in 0.25 =CE=BCCi of [3H]thymidine (Amersham = Pharmacia Biotech,=20 Piscataway, NJ) at the end. High molecular mass = [3H]-radioactivity=20 was precipitated and counted.

EC proliferation

The HBMEC and HUVEC were seeded on 48-well and 24-well plates=20 (poly-L-lysine-coated plates for HBMEC) at 5 =C3=97 103 or 2 = =C3=97=20 104 per well, respectively. After cells adhered to the well = (6 hr),=20 growth medium was replaced by CM. The CM collected from U251 glioma cell = cultures were pretreated with SCF or VEGF neutralized antibodies = (R&D=20 systems) at the indicated concentrations for 1 hr at 37=C2=B0C before = being added to=20 the HUVEC. After 48 hr culture in the treated media, dead floating cells = were=20 washed away, and attached living cells were trypsinized and counted with = hematocytometer.

EC differentiation assay

After the Matrigel (BD Biosciences) formed a solid gel in 24-well = plates,=20 serum-starved BMVEC-b cells were seeded on the gel surface at = 105=20 cells per well and cultured in treatment medium in the presence or = absence of=20 SCF (20 ng/ml). Primary HBMEC were placed on the gel directly at 24 = =C3=97=20 103 per well. Tubular formation was observed using an = inverted phase=20 contrast microscope, and images were captured at 4 and 18 hr after cell = seeding.=20 Each experiment was repeated two or three times.

Wound healing assay

The BMVEC-b (3 =C3=97 105/well) was seeded on collagen = I-coated plates=20 (24-well). After cells adhered to the plates (3 hr), growth medium was = replaced=20 by SCF and =CE=B2-FGF (R&D Systems) or vehicle in treatment medium. = After 6 hr of=20 incubation, confluent monolayers of BMVEC-b were wounded with a pipette = tip and=20 incubated in the same condition. The cells were fixed with 4% = paraformaldehyde=20 18 hr after being wounded, and images were captured. The cells that had = migrated=20 across the edge of the wound were observed microscopically = (magnification, =C3=9720)=20 and counted in three fields for each well. All assays were repeated = three times=20 in duplicates or triplicates.

Flow cytometry analysis

Cells were incubated with Cy-Chrome conjugated anti-human c-Kit = (CD117)=20 antibody or PE-Cy5 mouse IgG1 as a negative control (BD Pharmingen, San = Diego,=20 CA), respectively. Dead cells were excluded by propidium iodide staining = (Sigma=20 Chemie), and expression of c-Kit on the cell surface was analyzed by = FACS=20 (Becton Dickinson, San Jose, CA). For the detection of total c-Kit = including=20 that in the cytosol, permeabilization was performed with BD = cytofix/cytoperm=20 solution (Kit from BD Biosciences) for 15 min prior to the incubation = with c-Kit=20 antibody.

Immunoprecipitation and immunoblotting

Confluent-grown ECs were treated with 50 ng/ml of SCF for 5, 10, 15, = and 30=20 min after 24 hr of serum starvation. The ECs were collected with RIPA = lysis=20 buffer (Upstate, Charlottesville, VA) containing 50 mM NaF, 1 mM=20 Na3VO4, 50 mM PMSF, and Protease Inhibitor = Cocktail=20 (Roche). The antibodies were purchased from Cell Signaling Technology, = Inc.=20 (Beverly, MA) or as mentioned otherwise. All the primary antibodies were = used in=20 a 1:1000 dilution except for the anti-SCF antibody, which was used in a = 1:2000=20 dilution. The primary antibodies were anti-phospho-c-Kit, = anti-phospho-MEK1/2=20 and anti-MEK1/2, anti-phospho-p44/42 MAPK and anti-p44/42 MAPK,=20 anti-phospho-SAPK/JNK and anti-SAPK/JNK, anti-phospho-p38 MAPK and = anti-p38=20 MAPK, anti-phospho-Akt and anti-Akt, anti-phospho-mTOR and anti-mTOR,=20 anti-phospho-4E-BP1 and anti-4E-BP1, anti-SCF and anti-VEGF (Chemicon, = Temecula,=20 CA), and anti-=CE=B2-tubulin (Sigma). Reblotting was done after = membranes were=20 stripped by reblot kit (Chemicon). Tie2 detection in Matrigel plugs from = the in=20 vivo Matrigel assay was carried out by immunoprecipitation and = immunoblotting.=20 The gel plugs were carefully separated from muscle and skin and = homogenized with=20 RIPA lysis buffer. The resulting total tissue lysates (40 mg of protein) = were=20 immunoprecipitated with Tie2 antibody (Santa Cruz Biotechnology, Inc., = Santa=20 Cruz, CA) and then analyzed by immunoblot with Tie2 antibody (Zadeh=20 et al., 2004).

ELISA

Cells were seeded at 80% of confluence, and the growth medium was = changed 24=20 hr later to basal medium containing 0.1% BSA after washing with PBS. = Forty-eight=20 hours later, the CM were collected, and supernates were obtained by = centrifuge=20 at 2K RPM for 5 min. SCF in the CM was measured using the human SCF = ELISA kit=20 (R&D System) in triplicate following the protocol provided by the=20 manufactory and normalized by the total protein levels in the media of = each=20 individual sample.

Microarray analysis

All gliomas (grade II, III, and IV) were pathologically diagnosed = according=20 to WHO standard. All tumors and nontumor brain tissues of epilepsy were = obtained=20 from surgery patients and frozen immediately after operation (clinical = protocol=20 approved by the NCI IRB committee with informed consent obtained from = all=20 subjects). The frozen samples were disrupted and homogenized with TRIZOL = (Invitrogen Corp., Carlsbad, CA), and the total RNA isolated from each = sample=20 was further purified using RNeasy Mini Kit (Qiagen, Valencia, CA). The = integrity=20 and quality of the RNA met the quality requirements for Human Genome = U133 Plus=20 2.0 arrays (Affymetrix, Inc., Santa Clara, CA) recommended by the = company. All=20 experimental=20 procedures for labeling, array hybridization, and scanning were = performed=20 using protocols recommended by Affymetrix. CEL files were generated by=20 Affymetrix GCOS 1.2 software, and the present/absent calls were defined = with=20 global scaling to target value of 500. By dChip software (Li=20 and Wong, 2001), the CEL files were normalized to a median-intensity = array,=20 and model-based expression values were calculated using PM/MM difference = model.=20 Based on the latest annotation from Affymetrix NETAFFX service, four = probe sets=20 for SCF (KITLG) gene were present in each chip. The signal = intensities of each probe set were used for analyzing SCF = (KITLG)=20 expressions. The significance in differential SCF (KITLG)=20 expressions in different grades of gliomas versus human nontumor brains = was=20 determined using log2-transformed expression values by standard unpaired = two-tailed Student's t test of two groups without assuming equal = variance=20 between groups. The microarray data have been submitted to the Gene = Expression=20 Omnibus (GEO) public database at NCBI, and the accession number is = GSE4290.

Real-time RT-PCR

RNA isolation and cDNA synthesis were performed as described above. A = human=20 probe set covering exon 8 of SCF gene was purchased from Applied=20 Biosystems (Foster City, CA). Isoform-specific probe sets were selected = in the=20 connecting region of exons 5 and 7 (for mSCF) and in exon 6 (for=20 sSCF) (Table=20 S1). Two-step real-time PCR was performed in duplicates or = triplicates. Data=20 were analyzed on the basis of threshold cycle values of each sample and=20 normalized with =CE=B2-actin.

Expression vector and transduction

SCF cDNA was synthesized by RT-PCR and subcloned into the=20 pLenti6/V5-DEST vector (Invitrogen Corp.) in the antisense orientation = following=20 the supplier's protocol. The 293FT package cell was cotransfected with = the=20 expression vector and ViralPower Packaging Mixture (Invitrogen Corp.). = The=20 supernatants containing infectious virus particles from transfected = 293FT were=20 used to transduce U373 and U87 glioma cells. The stably transduced U373 = and U87=20 cell lines were selected with 5 ug/ml of blasticidin for over 2 weeks, = and the=20 amount of SCF protein expression was assayed by immunoblot. The = retroviral=20 expression vector pSM2 with the SCF shRNA insert and the LinX = retroviral=20 packaging cells were purchased from Open Biosystems (Hunstsville, AL). = The=20 retrovirus was obtained from plasmid transfected LinX cells and was used = to=20 transduce U251 cells following the manufacturer's protocol. The stable = shRNA=20 expression cells were selected with puromycin at 1 ng/ml for over 2 = weeks, and=20 downregulation of SCF was verified by immunoblot.

In vivo angiogenesis assay and intracranial tumor = model

All adult mice (6=E2=80=938 weeks of age) were from NCI-Fredrick, and = the animal=20 experiments were conducted on an animal experimentation protocol = approved by the=20 NCI's animal protection committee (the =E2=80=9CACUC=E2=80=9D). For the = in vivo angiogenesis=20 assay (Capogrossi=20 and Passaniti, 1999), Matrigel with 150 ng of SCF and controls or 5 = =C3=97=20 103 cells was injected into a SCID mouse, and the plugs with = skin and=20 muscle were collected 2 weeks later. For the intracranial implantation = of glioma=20 cells, stereotactic surgery was performed (1 mm anterior to the bregma = and 2.5=20 mm lateral to the midline) using athymic nu/nu mice under = anesthesia.=20 U373/vector or U373/as-SCF (106 cell) were suspended in 5 = =CE=BCl of HANK=20 and injected into the caudate nucleus. For immunohistochemical analysis, = mice=20 were sacrificed 4 weeks later, and brains were carefully recovered after = perfusion.

Immunohistochemistry

The fixed brains and Matrigel plugs were prepared for paraffin = sectioning and=20 immunohistochemical analysis. The human GBM tissues were obtained from = surgery=20 patients following the clinical protocol approved by the NCI IRB = committee with=20 informed consent obtained from all subjects. After being deparaffinized, = the=20 sections were processed for immunohistochemistry with the following = primary=20 antibodies: anti-vWF (1:500 dilution), anti-c-Kit (1:200 dilution), = anti-CD31=20 (1:20 dilution), and anti-SCF (1:100 dilution), respectively, All of the = primary=20 antibodies were purchased from Dako Corp. (Carpinteria, CA) except for = the=20 anti-SCF antibody, which was bought from Chemicon. Visualization of = antibody=20 binding was performed by a FITC-conjugated second antibody (1:500 = dilution;=20 Molecular Probes, Eugene, OR) or by the second antibody tagged with HRP = (1:1000=20 dilution; Dako) following reaction to DAB (Molecular Probes) or AEC = (Sigma).

In situ hybridization

The DIG-labeled probe hybridized to nucleotides 848=E2=80=93895 of = the mouse=20 SCF mRNA sequence (NM_013598 in GenBank) was obtained from = GeneDetect=20 company (Aucklank, New Zealand). After they were deparaffinized, mouse = sections=20 were permeabilized with target retrieval solution (Dako) and hybridized = with=20 sense or antisense DIG-labeled probe at 37=C2=B0C for 18 hr. After = stringent washing,=20 the hybridized signals were detected by tyramide signal amplification = system and=20 visualized with DAB (Dako).

Statistical analysis

Student's t test was used to determine statistical significance in=20 comparisons. Survival curves were plotted with Kaplan-Meier method and = compared=20 using log-rank test. p < 0.05 was considered significance. Survival = trends of=20 grade IV glioma patients (n =3D 64) were analyzed relative to SCF = mRNA=20 levels. The actin normalized SCF levels ranging from 0.64- to = 10.76-fold=20 were determined by real-time PCR; levels less than 1.8 were grouped as = low SCF,=20 and those greater than 1.8 were classified as high SCF. In the figures, = columns=20 and bars show the mean and SEM, respectively.


Acknowledgments

The authors would like to thank Cindy Harris, Molecular Diagnosis = Section,=20 Department of Pathology, Institute of Neurological Disorders and Stroke, = for=20 technical support in immunohistochemical staining; Nagle and Deborah = Kauffman,=20 Sequencing Facility, Institute of Neurological Disorders and Stroke, for = DNA=20 sequencing; and Dr. Carolyn Smith, Light Imaging Facility, Institute of=20 Neurological Disorders and Stroke, for confocal microscope analysis. = J.M. was a=20 2004 HHMI-NIH Research Scholar.


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Supplemental data

Document S1. Two supplemental figures and two supplemental = tables.  = (419 K)
= mmc1.pdf    3D"Help
Acrobat PDF file 1.=20

Accession numbers

The microarray data have been submitted to the Gene Expression = Omnibus=20 (GEO) public database at NCBI, and the accession number is GSE4290.=20



Ph: 301 402 6383; Fax: 301 480 2246



Volume=20 9, Issue 4, April 2006, Pages 287-300
 
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white; BACKGROUND-COLOR: #777777; TEXT-DECORATION: none } A.linkopen:active { COLOR: white; BACKGROUND-COLOR: #777777; TEXT-DECORATION: none } SPAN.linkopen { COLOR: white; BACKGROUND-COLOR: #777777; TEXT-DECORATION: none } .linknoborder IMG { BORDER-RIGHT: medium none; BORDER-TOP: medium none; BORDER-LEFT: medium = none; BORDER-BOTTOM: medium none } .linkdisabled { COLOR: #999999 } INPUT.xpstyle { BORDER-RIGHT: #666666 1px solid; BORDER-TOP: #666666 1px solid; = BORDER-LEFT: #666666 1px solid; BORDER-BOTTOM: #666666 1px solid } INPUT.qsinput { FONT-FAMILY: arial, verdana, helvetica, sans-serif; HEIGHT: 1.6em } TABLE.sdMainNav { BACKGROUND-POSITION: left top; MARGIN-TOP: 0.2em; FONT-SIZE: 1em; = WIDTH: 100%; BORDER-BOTTOM: black 0.1em solid; BACKGROUND-REPEAT: = repeat-x; HEIGHT: 2em } TD.sdMainNav { BACKGROUND-POSITION: left top; BACKGROUND-REPEAT: repeat-x } .sci_dirNav { BACKGROUND-COLOR: #6c9d31 } .sci_dirNavActive { =09 } .blueNav { BACKGROUND-COLOR: #0000aa } .blueNavActive { COLOR: #0000aa; BACKGROUND-COLOR: #bad3f3 } .redNav { BACKGROUND-COLOR: #990000 } .redNavActive { COLOR: #990000; BACKGROUND-COLOR: #f7cece } .greyNav { BACKGROUND-COLOR: #7f7f7f } .greyNavActive { COLOR: #7f7f7f; BACKGROUND-COLOR: #e6e6e6 } .greenNav { BACKGROUND-COLOR: #007703 } .greenNavActive { COLOR: #007703; BACKGROUND-COLOR: #c2edc0 } .orangeNav { BACKGROUND-COLOR: #cc5200 } .orangeNavActive { COLOR: #cc5200; BACKGROUND-COLOR: #ffdfca } TABLE.sdMainNav A:hover { TEXT-DECORATION: none } TABLE.sdMainNavCenter TD { FONT-SIZE: 1em; BORDER-LEFT: white 0.01em solid; HEIGHT: 1.82em } TABLE.sdMainNavCenter TBODY { FONT-SIZE: 1em } TD { FONT-SIZE: 1em } TR { FONT-SIZE: 1em } DIV { FONT-SIZE: 1em } TABLE.sdMainNavCenter { BORDER-RIGHT: white 0.01em solid; HEIGHT: 1.82em } TABLE.sdMainNav A { FONT-WEIGHT: normal; PADDING-BOTTOM: 0.33em; VERTICAL-ALIGN: middle; = COLOR: white; PADDING-TOP: 0.19em; HEIGHT: 1.82em; TEXT-DECORATION: none } TABLE.sdMainNav A:link { FONT-WEIGHT: normal; PADDING-BOTTOM: 0.33em; VERTICAL-ALIGN: middle; = COLOR: white; PADDING-TOP: 0.19em; HEIGHT: 1.82em; TEXT-DECORATION: none } TABLE.sdMainNav A:visited { FONT-WEIGHT: normal; PADDING-BOTTOM: 0.33em; VERTICAL-ALIGN: middle; = COLOR: white; PADDING-TOP: 0.19em; HEIGHT: 1.82em; TEXT-DECORATION: none } DIV.sdMainNavPadding { PADDING-RIGHT: 1em; PADDING-LEFT: 1em } .alphaDivider { DISPLAY: inline; WIDTH: 0px; POSITION: relative; HEIGHT: 0px } .alphaSelect { LEFT: 0px; POSITION: absolute; TOP: -11px; HEIGHT: 14px; = BACKGROUND-COLOR: #777777 } .libBannerText { FONT-SIZE: smaller; FONT-FAMILY: Verdana, Arial, Helvetica, sans-serif } .sci_dirBtn { BACKGROUND-COLOR: #7aa544 } .sci_dirBtnHov { COLOR: #ffffff; BACKGROUND-COLOR: #1d6b2f } .blueBtn { BACKGROUND-COLOR: #0000aa } .blueBtnHov { COLOR: #0000aa; BACKGROUND-COLOR: #bad3f3 } .greenBtn { BACKGROUND-COLOR: #007703 } .greenBtnHov { COLOR: #007703; BACKGROUND-COLOR: #c2edc0 } .greyBtn { BACKGROUND-COLOR: #7f7f7f } .greyBtnHov { COLOR: #7f7f7f; BACKGROUND-COLOR: #e6e6e6 } .redBtn { BACKGROUND-COLOR: #990000 } .redBtnHov { COLOR: #990000; BACKGROUND-COLOR: #f7cece } .orangeBtn { BACKGROUND-COLOR: #cc5200 } .orangeBtnHov { COLOR: #cc5200; BACKGROUND-COLOR: #ffdfca } INPUT.btn { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 1px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 1px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 0px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; OVERFLOW: visible; BORDER-LEFT: #666666 1px solid; WIDTH: auto; = CURSOR: pointer; COLOR: #ffffff; PADDING-TOP: 0px; BORDER-BOTTOM: = #666666 1px solid; TEXT-DECORATION: none } INPUT.btnhov { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 1px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 1px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 0px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; OVERFLOW: visible; BORDER-LEFT: #666666 1px solid; WIDTH: auto; = CURSOR: pointer; PADDING-TOP: 0px; BORDER-BOTTOM: #666666 1px solid; = TEXT-DECORATION: none } A.articleBtn { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 12px; = PADDING-BOTTOM: 1px; MARGIN: 0px; BORDER-LEFT: medium none; CURSOR: = pointer; COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.articleBtn:hover { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 12px; = PADDING-BOTTOM: 1px; MARGIN: 0px; BORDER-LEFT: medium none; CURSOR: = pointer; COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.articleBtnActive { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.articleBtnActive:hover { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.articleBtn:hover { BACKGROUND-COLOR: #7aa544 } A.btn { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 5px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 5px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 1px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; BORDER-LEFT: #666666 1px solid; COLOR: #ffffff; PADDING-TOP: = 1px; BORDER-BOTTOM: #666666 1px solid; FONT-FAMILY: arial, verdana, = helvetica, sans-serif; HEIGHT: 1.17em; TEXT-DECORATION: none } A.btn:hover { BORDER-RIGHT: #666666 1px solid; PADDING-RIGHT: 5px; BORDER-TOP: = #666666 1px solid; PADDING-LEFT: 5px; FONT-WEIGHT: bold; FONT-SIZE: = 12px; PADDING-BOTTOM: 1px; MARGIN: 0px 1px 0px 0px; VERTICAL-ALIGN: = middle; BORDER-LEFT: #666666 1px solid; COLOR: #ffffff; PADDING-TOP: = 1px; BORDER-BOTTOM: #666666 1px solid; FONT-FAMILY: arial, verdana, = helvetica, sans-serif; HEIGHT: 1.17em; TEXT-DECORATION: none } A.sci_dirBtn { BACKGROUND-COLOR: #7aa544 } A.sci_dirBtn:hover { COLOR: #ffffff; BACKGROUND-COLOR: #1d6b2f } A.blueBtn { BACKGROUND-COLOR: #0000aa } A.blueBtn:hover { COLOR: #0000aa; BACKGROUND-COLOR: #bad3f3 } A.greenBtn { BACKGROUND-COLOR: #007703 } A.greenBtn:hover { COLOR: #007703; BACKGROUND-COLOR: #c2edc0 } A.greyBtn { BACKGROUND-COLOR: #7f7f7f } A.greyBtn:hover { COLOR: #7f7f7f; BACKGROUND-COLOR: #e6e6e6 } A.redBtn { BACKGROUND-COLOR: #990000 } A.redBtn:hover { COLOR: #990000; BACKGROUND-COLOR: #f7cece } A.orangeBtn { BACKGROUND-COLOR: #cc5200 } A.orangeBtn:hover { COLOR: #cc5200; BACKGROUND-COLOR: #ffdfca } A.noul:hover { TEXT-DECORATION: none } .tableFmBg { PADDING-RIGHT: 0px; BORDER-TOP: #8cc919 2px solid; PADDING-LEFT: 0px; = PADDING-BOTTOM: 0px; MARGIN: 0px; PADDING-TOP: 0px; BORDER-BOTTOM: = #8cc919 2px solid; BACKGROUND-COLOR: #efefef } .sci_dirBorder { BORDER-TOP: #8cc919 2px solid; BORDER-BOTTOM: #8cc919 2px solid } .blueBorder { BORDER-TOP: #0000aa 2px solid; BORDER-BOTTOM: #0000aa 2px solid } .greenBorder { BORDER-TOP: #007703 2px solid; BORDER-BOTTOM: #007703 2px solid } .greyBorder { BORDER-TOP: #7f7f7f 2px solid; BORDER-BOTTOM: #7f7f7f 2px solid } .redBorder { BORDER-TOP: #990000 2px solid; BORDER-BOTTOM: #990000 2px solid } .orangeBorder { BORDER-TOP: #cc5200 2px solid; BORDER-BOTTOM: #cc5200 2px solid } .sci_dirBorderBtm { BORDER-BOTTOM: #8cc919 2px solid } .blueBorderBtm { BORDER-BOTTOM: #0000aa 2px solid } .greenBorderBtm { BORDER-BOTTOM: #007703 2px solid } .greyBorderBtm { BORDER-BOTTOM: #7f7f7f 2px solid } .redBorderBtm { BORDER-BOTTOM: #990000 2px solid } .orangeBorderBtm { BORDER-BOTTOM: #cc5200 2px solid } .tableFmBgGray { FONT-SIZE: 1em; FONT-FAMILY: arial, helvetica, sans-serif; = BACKGROUND-COLOR: #efefef } .tableFmBgGrayNoCell { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-SIZE: 1em; PADDING-BOTTOM: = 5px; MARGIN: 5px; PADDING-TOP: 5px; FONT-FAMILY: arial, helvetica, = sans-serif; BACKGROUND-COLOR: #efefef } .tableFmBgPad { MARGIN-TOP: 5px; MARGIN-BOTTOM: 5px; PADDING-BOTTOM: 5px; PADDING-TOP: = 5px; BACKGROUND-COLOR: #efefef } .tableFmCell { PADDING-LEFT: 10px; FONT-WEIGHT: bold; PADDING-BOTTOM: 3px; = MARGIN-LEFT: 10px; VERTICAL-ALIGN: top; PADDING-TOP: 3px; TEXT-ALIGN: = right } .tableFmCellTop { FONT-WEIGHT: bold; VERTICAL-ALIGN: top; PADDING-TOP: 0px; TEXT-ALIGN: = right } .tableFmCellAbove { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-WEIGHT: bold; = PADDING-BOTTOM: 5px; PADDING-TOP: 5px; TEXT-ALIGN: left } .tableFmCellL { PADDING-LEFT: 10px; FONT-WEIGHT: bold; PADDING-BOTTOM: 3px; = MARGIN-LEFT: 10px; VERTICAL-ALIGN: top; PADDING-TOP: 3px; TEXT-ALIGN: = left } .tableFmDivider { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; WIDTH: 100%; PADDING-TOP: 0px; HEIGHT: 2px; BACKGROUND-COLOR: = #ffffff } .redtableFmDivider { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; WIDTH: 100%; PADDING-TOP: 0px; HEIGHT: 2px; BACKGROUND-COLOR: = #990000 } .SDtxtLarger { FONT-WEIGHT: bold; FONT-SIZE: larger; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtSmall { FONT-SIZE: xx-small; COLOR: #000000; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtSmallBold { FONT-WEIGHT: bold; FONT-SIZE: 0.9em } .SDtxtNote { FONT-SIZE: 1em; COLOR: #000000; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtNoteSmall { FONT-SIZE: 10px; COLOR: #000000; FONT-FAMILY: arial, helvetica, = sans-serif } .SDtxtPgTitleBlack { FONT-WEIGHT: bold; FONT-SIZE: 150%; COLOR: #000000; FONT-FAMILY: arial, = helvetica, sans-serif } A.errMsg { COLOR: #ff0000; TEXT-DECORATION: none } A.errMsg:hover { TEXT-DECORATION: underline } .boldText { FONT-WEIGHT: bold } .sci_dirColor { COLOR: #7aa544 } .blueColor { COLOR: #0000aa } .greenColor { COLOR: #007703 } .greyColor { COLOR: #7f7f7f } .redColor { COLOR: #990000 } .orangeColor { COLOR: #cc5200 } .tablePlainWhite { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; = PADDING-TOP: 0px; BACKGROUND-COLOR: #ffffff } .inputBox { BORDER-RIGHT: #666666 1px solid; BORDER-TOP: #666666 1px solid; = FONT-SIZE: 1em; VERTICAL-ALIGN: top; BORDER-LEFT: #666666 1px solid; = BORDER-BOTTOM: #666666 1px solid; BACKGROUND-COLOR: #ffffff } A.tabActive { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = TEXT-DECORATION: none } A.tabActive:hover { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = TEXT-DECORATION: none } A.tab { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.tab:hover { BORDER-RIGHT: medium none; PADDING-RIGHT: 20px; BORDER-TOP: medium = none; PADDING-LEFT: 20px; FONT-WEIGHT: bold; FONT-SIZE: 1em; = PADDING-BOTTOM: 1px; MARGIN: 0px 2px 0px 0px; BORDER-LEFT: medium none; = COLOR: #ffffff; PADDING-TOP: 1px; BORDER-BOTTOM: medium none; = BACKGROUND-COLOR: #999999; TEXT-DECORATION: none } A.sci_dirTabActive { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.sci_dirTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #7aa544; TEXT-DECORATION: none } A.sci_dirTab:hover { BACKGROUND-COLOR: #7aa544 } A.blueTabActive { CURSOR: default; BACKGROUND-COLOR: #0000aa; TEXT-DECORATION: none } A.blueTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #0000aa; TEXT-DECORATION: none } A.blueTab:hover { BACKGROUND-COLOR: #0000aa } A.greenTabActive { CURSOR: default; BACKGROUND-COLOR: #007703; TEXT-DECORATION: none } A.greenTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #007703; TEXT-DECORATION: none } A.greenTab:hover { BACKGROUND-COLOR: #007703 } A.greyTabActive { CURSOR: default; BACKGROUND-COLOR: #7f7f7f; TEXT-DECORATION: none } A.greyTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #7f7f7f; TEXT-DECORATION: none } A.greyTab:hover { BACKGROUND-COLOR: #7f7f7f } A.redTabActive { CURSOR: default; BACKGROUND-COLOR: #990000; TEXT-DECORATION: none } A.redTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #990000; TEXT-DECORATION: none } A.redTab:hover { BACKGROUND-COLOR: #990000 } A.orangeTabActive { CURSOR: default; BACKGROUND-COLOR: #cc5200; TEXT-DECORATION: none } A.orangeTabActive:hover { CURSOR: default; BACKGROUND-COLOR: #cc5200; TEXT-DECORATION: none } A.orangeTab:hover { BACKGROUND-COLOR: #cc5200 } .textBoxMultipleRow { FONT-SIZE: 1em; FONT-FAMILY: Arial, Helvetica, sans-serif; = BACKGROUND-COLOR: #ffffff } A.nextPrev { FONT-SIZE: 1em; MARGIN: 0px 10px; WIDTH: 1%; COLOR: #ffffff; = TEXT-DECORATION: none } A.nextPrev:hover { FONT-SIZE: 1em; MARGIN: 0px 10px; WIDTH: 1%; COLOR: #ffffff; = TEXT-DECORATION: underline } INPUT.nextPrev { BORDER-RIGHT: medium none; PADDING-RIGHT: 1px; BORDER-TOP: medium none; = PADDING-LEFT: 1px; FONT-SIZE: 1em; PADDING-BOTTOM: 0px; MARGIN: 0px 5px; = VERTICAL-ALIGN: middle; OVERFLOW: visible; BORDER-LEFT: medium none; = WIDTH: auto; COLOR: #0000ee; PADDING-TOP: 0px; BORDER-BOTTOM: medium = none; BACKGROUND-COLOR: transparent; TEXT-DECORATION: none } INPUT.nextPrevHov { BORDER-RIGHT: medium none; PADDING-RIGHT: 1px; BORDER-TOP: medium none; = PADDING-LEFT: 1px; FONT-SIZE: 1em; PADDING-BOTTOM: 0px; MARGIN: 0px 5px; = VERTICAL-ALIGN: middle; OVERFLOW: visible; BORDER-LEFT: medium none; = WIDTH: auto; COLOR: #0000ee; PADDING-TOP: 0px; BORDER-BOTTOM: medium = none; BACKGROUND-COLOR: transparent; TEXT-DECORATION: underline } .smCaps { FONT-VARIANT: small-caps } .nowrap { WHITE-SPACE: nowrap } SPAN.hit { FONT-WEIGHT: bold; COLOR: #ff0000 } SPAN.bf { FONT-WEIGHT: bold } SPAN.it { FONT-STYLE: italic } SPAN.monospace { FONT-FAMILY: courier } SPAN.sans-serif { FONT-FAMILY: sans-serif } SPAN.underline { TEXT-DECORATION: underline } SPAN.pit { FONT-SIZE: 0.9em; COLOR: #737373; FONT-FAMILY: arial, verdana, = helvetica, sans-serif } .charImg { BORDER-RIGHT: medium none; BORDER-TOP: medium none; VERTICAL-ALIGN: = baseline; BORDER-LEFT: medium none; BORDER-BOTTOM: medium none } SPAN.cross-out { TEXT-DECORATION: line-through } .refersTable { FONT-SIZE: 1em; LINE-HEIGHT: 16px; FONT-FAMILY: arial, helvetica, = sans-serif; BACKGROUND-COLOR: #efefef } .refersLeftColumn { PADDING-LEFT: 5px; FONT-WEIGHT: bold; VERTICAL-ALIGN: top; WIDTH: 55px; = TEXT-ALIGN: right } .refersDivider { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; WIDTH: 100%; PADDING-TOP: 0px; HEIGHT: 2px; BACKGROUND-COLOR: = #ffffff } .articleTitle { FONT-WEIGHT: bold; FONT-SIZE: 18px; FONT-FAMILY: Arial, Helvetica, = sans-serif } .h1 { FONT-WEIGHT: bold; FONT-SIZE: 2em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h2 { FONT-WEIGHT: bold; FONT-SIZE: 1.3em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h3 { FONT-WEIGHT: bold; FONT-SIZE: 1.2em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h4 { FONT-WEIGHT: bold; FONT-SIZE: 1.1em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .h5 { FONT-WEIGHT: bold; FONT-SIZE: 1em; FONT-FAMILY: = arial,verdana,helvetica,sans-serif } .ImageScroller { OVERFLOW: auto; WIDTH: 435px } .ImageScrollerPurchHist { OVERFLOW: auto; WIDTH: 455px } .ImageScrollerPurchCurr { OVERFLOW: auto; WIDTH: 415px } ------=_NextPart_000_000C_01C8586F.1D2DBCD0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://ad.doubleclick.net/adj/scidir.rbi/;dcopt=ist;abr=!webtv;categ=cancres;acct=d51dc24a2b132512122a31f7d7dda950;sz=728x90;ptile=1;ord=218513? document.write('\n
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