From: Subject: Alternative inclusion of fibroblast growth factor receptor 2 exon IIIc in Dunning prostate tumors reveals unexpected epithelial mesenchymal plasticity -- Oltean et al. 103 (38): 14116 -- Proceedings of the National Academy of Sciences Date: Sun, 1 Oct 2006 10:36:48 +0200 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01C6E545.7FA17670" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.2962 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01C6E545.7FA17670 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.pnas.org/cgi/content/full/103/38/14116 Alternative inclusion of fibroblast growth factor = receptor 2 exon IIIc in Dunning prostate tumors reveals unexpected = epithelial mesenchymal plasticity -- Oltean et al. 103 (38): 14116 -- = Proceedings of the National Academy of Sciences
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Published online before print = September 8, 2006,=20 10.1073/pnas.0603090103
PNAS | = September=20 19, 2006 | vol. 103 | no. 38 | 14116-14121
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BIOLOGICAL SCIENCES / MEDICAL = SCIENCES
Alternative = inclusion of=20 fibroblast growth factor receptor 2 exon IIIc in Dunning prostate tumors = reveals=20 unexpected epithelial mesenchymal plasticity

Sebastian Oltean*,3D{dagger}=20, = Brian S.=20 Sorg3D{ddagger},3D=A7=20,=20 Todd Albrecht*,3D{dagger}=20,=B6,=20 Vivian I. Bonano*,3D{dagger}=20,||,=20 Robert M. Brazas*,3D{dagger}=20,**,=20 Mark W. Dewhirst3D{ddagger}=20, = and=20 Mariano A. Garcia-Blanco*,3D{dagger}=20,3D{dagger}=203D{dagger}=20,3D{ddagger}=203D{ddagger}=20=20

Departments of *Molecular Genetics and Microbiology, 3D{ddagger}=20Radiation = Oncology, and=20 3D{dagger}Medicine,=20 3D{dagger}Center for RNA Biology, and ||University = Program in=20 Genetics and Genomics, Duke University Medical Center, Durham, NC 27710=20

Edited by Joan A. Steitz, Yale University, New Haven, CT, and = approved July=20 26, 2006 (received for review April 17, 2006)


3D"   =20 Abstract
3D"Top
3D"Abstract
Results
Discussion
Methods
3D"Acknowledgements
References
 
I= n=20 epithelial cells, alternative splicing of fibroblast growth = factor=20 receptor 2 (FGFR2) transcripts leads to the expression of the = FGFR2(IIIb) isoform, whereas in mesenchymal cells, the same = process=20 results in the synthesis of FGFR2(IIIc). Expression of the=20 FGFR2(IIIc) isoform during prostate tumor progression = suggests a=20 disruption of the epithelial character of these tumors. To = visualize=20 the use of FGFR2 exon IIIc in prostate AT3 tumors in = syngeneic rats,=20 we constructed minigene constructs that report on alternative = splicing. Imaging these alternative splicing decisions = revealed=20 unexpected mesenchymal=96epithelial transitions in these = primary=20 tumors. These transitions were observed more frequently where = tumor=20 cells were in contact with stroma. Indeed, these transitions = were=20 frequently observed among lung micrometastases in the organ=20 parenchyma and immediately adjacent to blood vessels. Our = data=20 suggest an unforeseen relationship between epithelial = mesenchymal=20 plasticity and malignant fitness.

alternative splicing | mesenchymal=96epithelial = transitions |=20 tumor plasticity

Regulation of alternative splicing is essential for normal gene=20 expression (1), = and=20 alterations of this regulation are linked to disease (2), as = illustrated by the association between cancer and splicing = defects=20 (3=967). An = elegant=20 example of this is provided by the splicing of transcripts = encoding=20 fibroblast growth factor receptor 2 (FGFR2). The status of = FGFR2=20 alternative splicing depends on the interplay between several = cis-acting elements in the FGFR2 premRNA and transacting = factors,=20 some of which are cell-type-specific (8). In = mesenchymal cells, exon IIIb is silenced by the action of an = exonic=20 splicing silencer (9) and = two=20 flanking intronic splicing silencers (10=9612).=20 This silencing is mediated by Polypyrimidine tract-binding = protein=20 (PTB), hnRNP A1, and heretofore unknown factors. In = epithelial=20 cells, exon IIIb silencing is countered by several intronic=20 elements. The best characterized are the intronic activating=20 sequence 2, the intronic splicing activator and repressor = (ISAR,=20 also known as IAS3), and several GCAUG repeats (13=9618).=20 These elements have a dual function in epithelial cells, = because=20 they are also involved in silencing exon IIIc (14=9618).=20

FGFR2 splicing has been studied in tumors derived from the = R-3327=20 Dunning rat prostate tumor, which arose spontaneously from = the=20 dorsal lobe of the prostate in a Copenhagen rat (19). = Some=20 R-3327-derived tumors (DT or DT3) express FGFR2(IIIb), which = is=20 consistent with their epithelial phenotype (20), = whereas AT=20 tumors (e.g., AT3), which have lost epithelial markers and = display=20 many mesenchymal indicators (21), = express=20 FGFR2(IIIc) (20). = The=20 significance of these alternative decisions for tumor = behavior is=20 underscored by the fact that forced expression of FGFR2(IIIb) = suppresses tumor progression of AT3 tumors (22). = Most=20 importantly, however, the differential splicing of FGFR2 = transcripts=20 in these two cell types highlights broad differences in gene=20 expression programs. Arguably, monitoring alternative = splicing, which=20 has an unrivaled capacity to multiply coding diversity, can = provide=20 information that exquisitely discerns between unique cellular = states.

These considerations led us to conclude that the state of tumor=20 cells could be effectively reflected by the splicing status = of=20 FGFR2 transcripts. To observe this status in tumors in animals, = we=20 have developed reporters that can monitor alternative splicing=20 decisions in time and space. In this article, we visualized = the=20 alternative inclusion of FGFR2 exon IlIc in cells in culture = and in=20 tumors in animals. Studies of AT3 tumors revealed unexpected=20 plasticity of these tumors, which where previously thought to = be anaplastic (23). = Based on=20 these alternative splicing choices, we concluded that groups = of cells=20 within the primary tumors had transitioned toward an = epithelial=20 phenotype. This was noted to be associated with contact with = stroma.=20 Remarkably, many tumor cells that had invaded the lungs also=20 displayed this mesenchymal to epithelial transition (MET). = These data=20 force a reconsideration of the plasticity of this aggressive = tumor=20 and suggest a new relationship between epithelial mesenchymal = plasticity and malignant fitness.


3D"   =20 Results
3D"Top
3D"Abstract
3D"Results
Discussion
Methods
3D"Acknowledgements
References
 
<= STRONG>Imaging=20 Alternative Inclusion of FGFR2 Exon IlIc in Cell Culture. We = set out to=20 visualize the alternative inclusion of FGFR2 exon IlIc in = tumor cells=20 in culture. We used two well established Dunning cell lines, = DT3 and=20 AT3, and the imaging reporters described in Fig. = 1A.=20 The control pRint reporter encodes transcripts that contain = strong=20 splice sites expected to promote splicing efficiently in all = cell=20 types, and indeed Rint transcripts are efficiently spliced = and=20 express high levels of red fluorescent protein (RFP) in both = DT3 and=20 AT3 cells (Fig.=20 1 B and C; Fig. 6, which is published as supporting=20 information on the PNAS web site). RIIIcI2=20 transcripts, which include the elements necessary for = silencing=20 of exon IlIc in epithelial cells, were expected to include = exon=20 IIIc in a cell-type-specific fashion. Indeed, expression of=20 pRIIIcI2 in DT3 cells led to high levels of RFP, as=20 detected by epifluorescence microscopy (Fig. = 1C)=20 or FACS (Fig. 6), which is accompanied by efficient skipping = of exon=20 IIIc in pRIIIcI2 transcripts (Fig. = 1B).=20 Efficient inclusion of exon IIIc among pRIIIcI2=20 transcripts in AT3 cells disrupts the RFP ORF, leading to low = levels=20 of RFP (Figs.=20 1 B and C and 6A). We also tested = splicing=20 of R3D{Delta}, = transcripts,=20 which are identical to RIIIcI2 RNAs, except that = the=20 intronic activating sequence 2 and intronic splicing = activator and=20 repressor elements have been deleted (Fig. = 1A).=20 These two elements have no known function in mesenchymal = cells but=20 are required for efficient repression of exon IIIc in = epithelial=20 cells (15,=20 17). = As=20 expected, R3D{Delta},3D{Delta}=20 transcripts show a disruption of exon IIIc silencing in DT3 = cells and=20 express lower levels of RFP than observed with = RIIIcI2=20 RNAs (Fig.=20 1 B and C). It should be noted that, = whereas the=20 RT-PCR shown here can be used to compare between constructs = and cells=20 lines, the assay overestimates the levels of exon IIIc = skipping,=20 and therefore we calculate that the majority of R3D{Delta}=20,3D{Delta}=20 transcripts = included=20 this exon in DT3 cells (17). = As=20 expected, in AT3 cells, the R3D{Delta}=20,3D{Delta}=20 transcripts = include exon IIIc=20 as efficiently as do RIIIcI2 transcripts. These = results=20 indicated that the RFP constructs described above accurately = report=20 on the cell-type-specific use of FGFR2 exon IIIc in tissue=20 culture.



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  		Fig. 1. = Minigene=20 constructs, molecular analysis, and imaging of exon IIIc = inclusion=20 in DT3 and AT3 cells. (A) Schematic representation = (not to=20 scale) of the minigene reporters used to image alternative = splicing.=20 (B) RT-PCR analysis of the reporter in total RNA = extracts=20 from the different DT3 and AT3 cell lines was carried out as = described in Methods. RT-PCRs for pRint, = pRIIIcI2,=20 or pR3D{Delta},3D{Delta} transcripts resulted in the expected size = products (398 bp=20 for products that include IIIc and 250 bp for the products = that skip=20 this exon), and splice junctions were confirmed by = sequencing.=20 (C) Imaging FGFR2 exon IlIc inclusion in DT3 and AT3 = cells.=20 (Upper) Fluorescence imaging of DT3 and AT3 cells = stably=20 transfected with the pRint, pRIIIcI2, or pR,=20 minigenes. (Lower) Phase-contrast pictures of the = same fields=20 (images were acquired at x200=20 magnification). =

Visualizing=20 the Inclusion of Exon IIIc in AT3 Tumors. Because the=20 pRIIIcI2 reporter provided an accurate readout of = splicing=20 decisions in cells in culture, we asked whether it could be = used to=20 image these decisions in tumors in animals. AT3 cells = harboring=20 either pRint or pRIIIcI2 were injected s.c. into = the=20 flanks of syngeneic Copenhagen white 2331 male and female = rats.=20 AT3-Rint or -RIIIcI2 tumors were grown for 20=9630 = days,=20 harvested, and imaged whole in a fluorescence light box = before=20 freezing (see Methods). Rint tumors displayed high levels = of=20 fluorescence compared with na=EFve AT3 tumors (not shown).=20 AT3-RIIIcI2 tumors were expected to include exon IIIc = and=20 thus prevent synthesis of RFP and, indeed, the fluorescence=20 intensity of these tumors was much lower than that of Rint = tumors=20 and just slightly above background (not shown). These data=20 suggested that pRIIIcI2 could accurately report on = alternative splicing in tumors in living animals.

To confirm the conclusions reached by gross examination, we=20 inspected histological sections of AT3-Rint and = -RIIIcI2=20 tumors using epifluorescence microscopy. Three sections (15 = =B5m)=20 from different parts of at least three tumors were fixed in=20 paraformaldehyde and imaged as described below. Sections of = AT3=20 tumors appeared as homogenous sheets of malignant cells, as = has been=20 described by others (20). = Most, if=20 not all, of the cells in Rint tumors expressed high levels of = RFP,=20 whereas the great majority of cells in RIIIcI2 = tumors had=20 fluorescence that was indistinguishable from background auto=20 fluorescence in na=EFve AT3 tumors (Fig. = 2A).=20 The low level of RFP expression was due to efficient = inclusion of=20 exon IIIc in pRIIIcI2 reporter transcripts (Fig. = 2B),=20 which paralleled the inclusion of exon IlIc in endogenous = FGFR2=20 transcripts (data not shown). In AT3-RIIIcI2 tumors, a = few=20 cells expressing RFP at low levels were observed (Fig. = 2A=20 Right), and this was consistent with what had been = observed=20 in tissue culture, i.e., the AT3-RIIIcI2 population had = few cells expressing RFP above background, but at low levels=20 (see AT3-RIIIcI2 FACS in Fig. 6). All these data = indicated=20 that RIIIcI2 transcripts were reporting accurately = the=20 status of exon IlIc inclusion in tumors in vivo. =



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  		Fig. 2. Imaging = alternative use of exon IlIc in AT3 tumors using fluorescent = reporters. (A) Fluorescence imaging of AT3 tumor = sections=20 either untransfected (background) or stably transfected with = the=20 pRint and pRIIIcI2 constructs (all images were = acquired=20 at x200 magnification). = (B)=20 RT-PCR analysis of the reporter was carried out as described = in=20 Methods. RT-PCRs for RFP transcripts resulted in the = expected=20 size products, and splice junctions were confirmed by = sequencing.=20 Analysis of four different regions (denoted 1, 2, 3, or 4) = for each=20 type of tumor is shown. =

Imaging=20 Alternative Splicing Revealed Surprising Plasticity of AT3 = Tumors. As=20 described above, we noted very low expression of RFP in=20 AT3-RIIIcI2 tumors. Extensive surveys of = histological=20 sections from RIIIcI2 tumors, however, revealed = the=20 existence of "clusters" of red fluorescence (Fig. = 3A).=20 These RFP+ cells must be skipping exon IlIc very efficiently. = We=20 examined 14 RIIIcI2 tumors (nine in males and five = in=20 females), and 12 contained at least one RFP+ cluster (85% = frequency; Table=20 1, which is published as supporting=20 information on the PNAS web site). There was no = significant=20 difference between males and females in the frequency of = these=20 clusters (Table 1). Within each tumor, the number of RFP+ = clusters=20 was low, as indicated by the fact that the clusters were = found in=20 3D{approx}34%=20 of the sections surveyed (Table 1). These results indicated=20 that, whereas RFP expression was occurring in a small number = of=20 cells in each tumor, it was observed in the majority of=20 AT3-RIIIcI2 tumors.



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  		Fig. 3. MET in = tumors.=20 (A) Fluorescence and phase-contrast images of a = section of an=20 AT3-RIIIcI2 tumor close to the tumor capsule. = Images were=20 acquired at x200 = magnification.=20 (B) (Upper) Fluorescence images of sections of = AT3-Rint, -RIIIcI2, and -R3D{Delta}=20,3D{Delta}=20 = tumors.=20 (Lower) Phase-contrast pictures of the same fields. = Images=20 were acquired at x400=20 magnification. (C) E-cadherin counterstaining = confirms MET.=20 Example of a section from AT3-RIIIcI2 tumors = shows that=20 the red fluorescent cells also stained positive for = E-cadherin.=20 Images were acquired at x400=20 magnification. =

One=20 possibility for this splicing choice between different cells = in the=20 tumors could be differences in the reporters (e.g., acquired=20 mutations around exon IlIc). The nonrandom location of these=20 "clusters" (see below) suggested that this explanation was=20 improbable. A more likely possibility was that inclusion of = exon IIIc=20 was due to differences in transacting factors secondary to=20 either genetic alterations or phenotypic transitions in = response=20 to environmental signals. Indeed, efficient silencing of exon = IlIc and concomitant RFP expression would be the expected = result=20 of a phenotypic transformation toward a more epithelium-like=20 state, as in MET (24=9626). = To examine=20 this idea, we tested AT3-R3D{Delta}=20,3D{Delta}=20 tumors, which = harbor plasmid=20 pR3D{Delta}, (Fig. = 1B).=20 A systematic examination of four =96R3D{Delta}=20,3D{Delta}=20 tumors failed to = detect any=20 clusters of RFP expression (Fig. = 3B=20 Right and Table 1), strongly suggesting that the clusters = observed in RIIIcI2 tumors depended on epithelial = specific=20 cis elements and thus on transacting factors found in = epithelial=20 cells.

To test the possibility that the RFP+ clusters were indeed the=20 result of an epithelial transition, we interrogated these=20 RFP-producing clusters for the expression of E-cadherin, a = cell=20 adhesion molecule that is poorly expressed in mesenchymal = cells but=20 highly expressed in epithelial cells (24). = Of 18 RFP+=20 clusters from different tumors and different animals (see = Table 1),=20 14 stained positive for E-cadherin, confirming our prediction = that=20 the majority of these cells were undergoing MET (Fig. = 3C).=20 To further test the idea that RFP+ cells were transitioning = to an=20 epithelial state, we tested for the expression of zonula = occludens=20 protein-1 (ZO-1), which increases and/or redistributes in the = cell=20 during MET, and for vimentin, which decreases during MET (27, = 28).=20 RFP+ cells were also ZO-1+ but had poor staining for = vimentin,=20 and this contrasted with the bulk of the RIIIcI2 tumors = that stained negative for ZO-1 and positive for vimentin = (Fig.=20 7, which is published as supporting=20 information on the PNAS web site). It must be noted that = the=20 subcellular localizations of E-cadherin and ZO-1 are not = those=20 observed in normal epithelial tissues, suggesting that these = RFP+ AT3=20 cells had transitioned toward, but had not completely arrived = to, an=20 epithelial state (29). = The=20 staining with vimentin suggested that RFP clusters usually = arose=20 within larger areas of the tumors that had lost vimentin = staining=20 (Fig. 7). These data indicate that the skipping of exon IlIc, = which=20 led to RFP expression, was, in the majority of cases, due to = MET.=20 Therefore, we conclude that RFP expression in = RIIIcI2=20 tumors revealed epithelial plasticity of AT3 tumors.

MET Clusters Are Frequently Found Near Stroma. = Examination=20 of the histological sections indicated that the location of = the RFP+=20 clusters was not random. The majority of cases of the RFP+ = clusters=20 occurred in the vicinity of structures that appeared to be = stroma=20 [e.g., the tumor capsule (Fig.=20 3A)]. We confirmed this suggestion by = counterstaining=20 histological sections with Masson=92s Trichrome, which=20 differentially stains stromal components and has been used to = identify stroma in human prostate tumors (30). = In a=20 survey of tumor sections, we noted that 14 of 16 RFP+ = clusters were=20 found in close association with stromal structures containing = collagen, which was stained blue by Masson=92s Trichrome (Fig. 4 = and Table=20 1). These observations indicated that RFP+ cells (i.e., cells = that=20 would silence exon IIIc) predominantly occurred near = stroma.=20



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  		Fig. 4. MET = predominates=20 in stromal regions rich in collagen fibers. Masson=92s = Trichrome=20 staining confirms that RFP+ cells are situated in stromal = regions.=20 Examples are shown from three regions of three different=20 AT3-RIIIcI2 tumors (Left, image obtained = with=20 epifluorescence microscopy; Center, phase-contrast = picture of=20 the same field; Right, bright field of the same = region=20 located after Masson=92s Trichrome staining. All images were = acquired=20 at x200 magnification). = In the=20 Masson=92s Trichrome images, collagen is stained in blue, = nuclei in=20 black, and cytoplasm of cells in red. =

Alternative=20 Splicing Reporters Visualized MET in Lung Metastases. The = imaging=20 reporters described here permitted a comprehensive survey of = AT3 lung=20 metastases in 13 lungs from animals bearing = AT3-RIIIcI2=20 tumors. This survey revealed the presence of RFP+ = disseminated tumor=20 cells, which we refer to as micrometastases, in 12 of these = lungs (Fig. = 5A=20 and Table 1). As in the primary tumors, we observed = expression of=20 E-cadherin in the overwhelming majority (Table 1) of RFP+ = cells in=20 AT3-RIIIcI2 lung metastases (Fig. = 5B).=20 RFP+ micrometastasis in lungs coincided also with expression = of ZO-1=20 (not shown). Although we found these RFP+ cells distributed=20 throughout the lung parenchyma, we noted a propensity of = these cells=20 to surround blood vessels (Fig. = 5).=20 These data suggested that cells actively involved in lung = metastases=20 had undergone a transition to a more epithelium-like state. =



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  		Fig. 5. MET in = lung=20 metastasis. (A) Fluorescence and phase-contrast = images of a=20 lung section from animals harboring AT3-RIIIcI2 = tumors=20 (x200 magnification). = Fluorescent=20 cells are situated around a blood vessel (confirmed by=20 hematoxylin/eosin staining; data not shown). (B) = Example of a=20 section from lungs of an animal bearing an = AT3-RIIIcI2=20 tumor shows that the great majority of red fluorescent = metastatic=20 cells also stained positive for E-cadherin. Images were = acquired at=20 x200 magnification. =

In = lung=20 sections, we also observed large metastatic nodules (Fig. = 8A,=20 which is published as supporting=20 information on the PNAS web site). Although in the lung = tissue in=20 the immediate vicinity of nodules we were able to detect RFP+ = micrometastases (Fig. 8B, "lung"), analysis of the = central=20 parts of the nodule failed to detect RFP expression (Fig. = 8B,=20 "nodule"). Interestingly, RFP+ metastatic cells could be = observed at=20 the interface of the lung tissue with the nodule (Fig. = 8B,=20 "interface"). These data suggested that, in primary tumors = and large=20 nodules, where most tumor cells are in contact with each = other, there=20 are few RFP+ tumor cells. On the other hand, RFP+ tumor cells = were=20 frequently observed in contact with lung parenchyma and other = stromal=20 components, which were confirmed as such by Masson=92s = Trichrome=20 staining (not shown). All of these observations from primary = tumors=20 suggest that a population of metastatic AT3 cells undergo MET = upon=20 seeding in the lung stroma.


3D"   =20 Discussion
3D"Top
3D"Abstract
Results
3D"Discussion
Methods
3D"Acknowledgements
References
 
T= he=20 original goal of the study was to design and construct reporters = of=20 an alternative splicing decision in tumors in vivo. We = showed=20 here, by macroscopic and microscopic imaging, that this = objective=20 was achieved. In this and related work, which describes the=20 effective use of reporters to image splicing decisions in = normal=20 tissues in transgenic mice (V.I.B., S.O., R.M.B., and = M.A.G.-B.,=20 unpublished work), we describe tools and methods that will be = generally useful to those wanting to examine alternative = splicing=20 in vivo. In addition to this technical goal, we = anticipated=20 at the outset that monitoring alternative splicing would = provide=20 a sensitive measure of altered tumor cell states or = responses.=20 The design of the RIIIcI2 reporters was such that even=20 weak silencing of exon IIIc would result in the reporter = protein=20 expressed well above background. Indeed, the existence of AT3 = tumor cells that silenced FGFR2 exon IIIc led to the = discovery=20 of unexpected plasticity among AT3 cells in primary tumors = and=20 metastases. Here we will discuss what we know and what we = hypothesize=20 about this plasticity.

What Are These RFP+ Cells? Alternative silencing of = FGFR2=20 exon IIIc suggested that groups of AT3 cells (RFP+ clusters) = were in=20 transition to an epithelium-like state. This suggestion was = supported=20 by coexpression of well characterized markers of MET. These=20 transitions were observed in a small minority of the cells in = each=20 AT3 tumor, but clusters were found in 12 of 14 tumors (85% of = tumors). Our=20 data support the conclusion that RFP+ clusters in AT3=20 RIIIcI2 tumors are the result of epithelial = plasticity.=20 The opposite type of plasticity, EMT, has been proposed to = occur at=20 the leading edge of colorectal carcinomas (31) = and is=20 considered by some a required step in invasion and metastasis = (24, = 29, = 32, = 33). = Transition=20 to a mesenchymal-like state has also been noted in primary = pancreatic=20 carcinomas (34).=20 Less is known about sarcomas; however, phenotypic plasticity=20 has been noted in experimental fibrosarcomas induced by Rous=20 sarcoma virus oncogene (v-src) in athymic mice (35) = and in=20 biopsies of Ewing sarcomas in humans (36). = We predict=20 that careful examination of sarcomas will reveal plasticity = due to=20 MET as observed in the AT3 tumors.

What Is the Origin of MET in AT3 Tumors? An answer = to this=20 question is suggested by the nonrandom spatial distribution = of the=20 AT3 cells undergoing MET (RFP+ cells). These clusters of RFP=20 expression predominate near stroma, many near the tumor = capsule. We=20 observed a similar phenomenon among lung micrometastases = where many=20 RFP+ AT3 cells were seen in direct contact with the lung = parenchyma=20 or decorating blood vessels. This was in contrast to large = metastatic=20 nodules, which had very few, if any, RFP+ cells. There are = two=20 general explanations for the nonrandom distribution of RFP+ = cells=20 near stroma: recruitment or induction. Recruitment would = suggest that=20 a preexisting population of cells undergoing MET is attracted = to or=20 preferentially survives near stroma. There is no evidence for = the=20 existence of RFP+ cells among the AT3-RIIIcI2 cell = population in culture 1 day before implantation (compare the=20 distribution of RFP expression of AT3-RIIIcI2 and = Rint in=20 Fig. 6), and thus we do not favor this idea. Induction, which = is the=20 explanation we prefer, implies that the transition to an=20 epithelium-like state is a phenotypic response to signals = from the=20 microenvironment. A similar explanation has been offered to = explain=20 MET in the central areas of metastases of colorectal cancers = in=20 animal models (31). = Stromal=20 signals are likely growth factors, and indeed a switch in = FGFR2=20 isoforms was observed in rat bladder carcinoma NBT-II cells = in=20 culture during growth-factor-induced EMT (37).=20

What Are the Implications of MET in Terms of Tumor = Progression and=20 Metastasis? Although distinct roles for EMT in tumor = progression and=20 metastasis have been proposed (24, = 25, = 38=9640), = the=20 function of MET in malignancy is not clear. MET could be seen = as a=20 process of redifferentiation and perhaps a desired outcome. = Our data=20 suggest otherwise. The appearance of RFP+ lung metastases in=20 animals harboring AT3-RIIIcI2 tumors indicated = that the=20 potential to undergo MET was compatible with the capacity to = invade=20 and form metastases. Indeed, the numbers of these RFP+=20 micrometastases suggest they represent frequent events, = especially=20 when compared with the frequency of RFP+ clusters in primary = tumors.=20 We propose that what makes AT3 tumors highly aggressive is = not their=20 mesenchymal character per se but rather their capacity = to=20 undergo phenotypic transitions. We summarize this idea by = analogy to=20 a potential energy diagram, where the likelihood to = transition from=20 one cell state to another is determined by the equivalent of = an=20 activation energy barrier. For instance, a normal polarized=20 epithelial cell is much less likely to reach a mesenchymal = state=20 than a transformed cell. We suggest that AT3 cells probably=20 inhabit a metastable state, and the great majority of AT3 = cells=20 in a tumor can be induced to undergo MET. We further propose=20 that the increased capacity to transition is related to = malignant=20 fitness (41). = Finally,=20 we believe this idea can explain the rarity and = aggressiveness of=20 tumors of mixed carcinoid and sarcomatoid histology. We = propose that=20 in sarcomatoid carcinomas, the epithelioid and fibroblastoid = cells,=20 which can arise from the same clone (42), = inhabit=20 different phenotypic states very near an unstable transition = state.=20 The instability of these phenotypes suggests these states = would be=20 relatively uncommon, and indeed a survey of prostate = sarcomatoid=20 carcinomas so confirms (43). = The=20 ability to readily transition between epithelial and = mesenchymal=20 phenotypes makes these tumors fit to conquer the many hurdles = to=20 establish a successful metastasis. Thus, for both carcinomas = and=20 sarcomas, we postulate that phenotypic versatility leads to=20 increased malignant fitness.


3D"   =20 Methods
3D"Top
3D"Abstract
Results
Discussion
3D"Methods
3D"Acknowledgements
References
 
<= STRONG>Plasmids.=20 Plasmids encoding the RFP were constructed on the backbone of = the=20 pcDNA6/V5-HisA vector (Invitrogen, Carlsbad, CA), which has = an=20 ampicillin cassette for selection in Escherichia coli = and a=20 blasticidin resistance gene for generation of stable transfectants = in=20 mammalian cell cultures. The RFP we have used is a DsRed = dimer=20 variant (44)=20 kindly provided by Roger Tsien. The plasmid pRint has the = intron from=20 plasmid pI12 (11) = inserted at=20 position 369 of the RFP ORF (see Fig. = 1B).=20 The plasmid pRIIIcI2 is derived from pRint by = subcloning=20 the rat FGFR2 exon IIIc and flanking intronic sequences, = including=20 the regulatory sequences the intronic activating sequence 2 = (IAS2)=20 and intronic splicing activator and repressor (ISAR), into = the middle=20 of the pRint intron. pR3D{Delta},3D{Delta} is identical to pRIIIcI2, except that = the IAS2=20 and ISAR sequences have been deleted as described for = pI12IIIc-3D{Delta}=20 in ref. 17. = The=20 complete sequence of the plasmids will be provided upon = request.=20

Cell Culture and Transfections. DT and AT3 rat = prostate=20 tumor cells were kindly provided to our laboratory by Wallace = McKeehan. We refer to the DT cells as DT3 cells. Cells were=20 transfected by using lipofectamine (Invitrogen), and stable=20 transfectants were selected by using 15 =B5g/ml blasticidin.=20 Fluorescent cells were analyzed by fluorescence cytometry at = the Duke=20 University Cytometry facility, and this analysis revealed = that=20 initial blasticidin resistant populations were relatively=20 homogeneous. Nonetheless, we used preparative FACS to exclude = low-intensity fluorescence cells in the case of AT3-Rint, = DT3-Rint,=20 and DT3-RIIIcI2 and high-intensity fluorescence = cells for=20 AT3-RIIIcI2 and -R3D{Delta}=203D{Delta}, which were = present=20 in very small numbers. Cell populations with high levels of = RFP=20 expression (AT3-Rint, DT3-Rint, and DT3-RIIIcI2) contain = a=20 small number of cells with background levels of fluorescence = (see=20 Fig. 6) that probably represent cells where the reporter is = disrupted=20 or lost. Variability of RFP expression among cells in the = transfected=20 populations could be deduced from FACS of AT3-Rint cell = populations=20 (see Fig. 6). FACS profiles indicated that = AT3-RIIIcI2 and=20 AT3-R3D{Delta} = cells have stable=20 low levels of RFP expression over several months (not shown). = The=20 FACS analysis of AT3 cells that is shown in Fig. 6 was = performed 1=20 day before implantation of tumor cells in animals. =

Animals and Tumor Cell Implantation. For the studies = involving fluorescent reporters, AT3 cells were trypsinized,=20 resuspended in PBS to a final concentration of = 107/ml, and=20 kept on ice. Cells (1=962 x = 106) were=20 injected s.c. in one flank of Copenhagen 2331 rats (Harlan = Labs,=20 Indianapolis, IN; 75=9690 g, 2 mo of age). Animals were = continuously=20 monitored for tumor growth. All animal procedures were = performed=20 according to the Duke University Institutional and Animal = Care and=20 Use guidelines.

Histological Sections. Preparation and=20 imaging.  Excised tumors and lungs were washed in PBS = at room=20 temperature. Tumors were dissected in eight smaller sections = to=20 provide a thorough survey of the tumor. Depending on the size = of the=20 lungs, they were frozen either together or separate. The = tumor=20 sections and the lungs were placed in cryomolds, embedded in=20 optimal-cutting-temperature tissue sectioning medium (Sakura = Finetek,=20 Torrance, CA), snap-frozen in liquid nitrogen, and stored at = =9680=B0C.=20 Slides for fluorescence imaging were prepared as follows: the = tissue=20 was incubated for 15 min at =9620=B0C to equilibrate the = temperature=20 and then sectioned with a microtome. The sections (15 =B5m) = were=20 placed on glass slides, fixed in 4% (wt/vol) paraformaldehyde = for 5=20 min at room temperature, and rinsed in PBS at room temperature. = The=20 slides were mounted with gel/mount media (Biomeda, Foster = City, CA).=20 The sections were analyzed by using an Olympus (Melville, NY) = IX 71=20 epifluorescence microscope, and images were acquired by using = an=20 Olympus DP70 digital camera. Image processing was done with = DP=20 controller software (Olympus). Masson=92s Trichrome staining = was=20 performed by using a commercially available kit (DBS, = Pleasanton,=20 CA). After taking the fluorescent and phase-contrast images = of=20 particular regions, the section was stained with the = Masson=92s=20 Trichrome kit, and the same regions were identified by = comparison to=20 the phase contrast and imaged as described above.

Immunofluorescence staining.  Sections = were=20 fixed in 4% paraformaldehyde for 1 h before blocking and = incubation=20 with antibody. The E-cadherin (BD Biosciences, Franklin = Lakes, NJ),=20 ZO-1 (Biogenesis), and vimentin (Invitrogen) antibodies were=20 previously labeled with Zenon Alexa Fluor 488 (Molecular = Probes,=20 Eugene, OR), according to the manufacturer=92s = specifications. The=20 sections were analyzed by epifluorescence microscopy as = described=20 above.

Molecular analysis.  After macroscopic = imaging, the tumors were snap-frozen and stored at =9680=B0C. = The tissue=20 was ground to a powder in liquid nitrogen using a mortar and = pestle,=20 and RNA was extracted by using TRIzol as recommended by the=20 manufacturer (Invitrogen). RT-PCR for RFP transcripts was = performed=20 by using primers on the R and FP exons (Fig.=20 1B).


3D"   =20 Acknowledgements
3D"Top
3D"Abstract
Results
Discussion
Methods
3D"Acknowledgements
References
 
W= e thank=20 Dr. Roger Tsien (University of California, San Diego, CA) for = the=20 gift of the dimer dsRED (RFP) and Dr. Wallace McKeehan (Texas = A&M=20 University System Health Science Center, Houston, TX) for the = gift of=20 the DT3 and AT3 cells. We thank members of the M.A.G.-B. = laboratory=20 for helpful discussions. M.A.G.-B. acknowledges support from = National=20 Cancer Institute Grant R33 CA97502.


3D"   =20 Footnotes
 

Abbreviations: FGFR2, fibroblast growth factor receptor 2; MET, = mesenchymal=20 to epithelial transition; RFP, red fluorescent protein.

3D{ddagger}=203D{ddagger}=20To whom = correspondence=20 should be addressed. E-mail: garci001{at}mc.duke.edu

Freely available online through the = PNAS open=20 access option.

3D=A7=20Present = address:=20 Department of Biomedical Engineering, University of Florida, = 130 BME=20 Building, P.O. Box 116131, Gainesville, FL 32611-6131. = 3DBack

=B6Present address: = Cryolife, Inc.,=20 Kennesaw, GA 30144. 3DBack

**Present address: Mirus Corporation, = Madison,=20 WI 53719. 3DBack

Author contributions: S.O., B.S.S., = R.M.B.,=20 M.W.D., and M.A.G.-B. designed research; S.O., B.S.S., T.A., = and=20 V.I.B. performed research; T.A. contributed new = reagents/analytic=20 tools; S.O., B.S.S., V.I.B., R.M.B., M.W.D., and M.A.G.-B. = analyzed=20 data; and S.O., V.I.B., and M.A.G.-B. wrote the paper. =

Conflict of interest statement: = M.A.G.-B. is a=20 founder and consultant for Intronn, Inc., which owns and is=20 commercializing the use of transsplicing reactions in gene=20 therapy.

This paper was submitted directly = (Track II) to=20 the PNAS office.

=A9 2006 by The = National Academy=20 of Sciences of the USA


3D"   =20 References
3D"Top
3D"Abstract
Results
Discussion
Methods
3D"Acknowledgements
3D"References
&nb= sp;

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http://www.pnas.org/javascript/ajax/xmlhttprequest.js /*=0A= =0A= Cross-Browser XMLHttpRequest v1.2=0A= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=0A= =0A= Emulate Gecko 'XMLHttpRequest()' functionality in IE and Opera. Opera = requires=0A= the Sun Java Runtime Environment .=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. 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_0000_01C6E545.7FA17670 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.pnas.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 if (name =3D=3D "margin-right") {=0A= e.style.marginRight =3D value;=0A= }=0A= else if (name =3D=3D "margin-top") {=0A= e.style.marginTop =3D value;=0A= }=0A= else if (name =3D=3D "min-height") {=0A= e.style.minHeight =3D value;=0A= }=0A= else if (name =3D=3D "overflow") {=0A= e.style.overflow =3D value;=0A= }=0A= else if (name =3D=3D "overflow-x") {=0A= e.style.overflowX =3D value;=0A= }=0A= else if (name =3D=3D "overflow-y") {=0A= e.style.overflowY =3D value;=0A= }=0A= else if (name =3D=3D "padding") {=0A= e.style.padding =3D value;=0A= }=0A= else if (name =3D=3D "padding-bottom") {=0A= e.style.paddingBottom =3D value;=0A= }=0A= else if (name =3D=3D "padding-left") {=0A= e.style.paddingLeft =3D value;=0A= }=0A= else if (name =3D=3D "padding-right") {=0A= e.style.paddingRight =3D value;=0A= }=0A= else if (name =3D=3D "padding-top") {=0A= e.style.paddingTop =3D value;=0A= }=0A= else if (name =3D=3D "page-break-after") {=0A= e.style.pageBreakAfter =3D value;=0A= }=0A= else if (name =3D=3D "page-break-before") {=0A= e.style.pageBreakBefore =3D value;=0A= }=0A= else if (name =3D=3D "pixelBottom") {=0A= e.style.pixelBottom =3D value;=0A= }=0A= else if (name =3D=3D "pixelHeight") {=0A= e.style.pixelHeight =3D value;=0A= }=0A= else if (name =3D=3D "pixelLeft") {=0A= e.style.pixelLeft =3D value;=0A= }=0A= else if (name =3D=3D "pixelRight") {=0A= e.style.pixelRight =3D value;=0A= }=0A= else if (name =3D=3D "pixelTop") {=0A= e.style.pixelTop =3D value;=0A= }=0A= else if (name =3D=3D "pixelWidth") {=0A= e.style.pixelWidth =3D value;=0A= }=0A= else if (name =3D=3D "posBottom") {=0A= e.style.posBottom =3D value;=0A= }=0A= else if (name =3D=3D "posHeight") {=0A= e.style.posHeight =3D value;=0A= }=0A= else if (name =3D=3D "position") {=0A= e.style.position =3D value;=0A= }=0A= else if (name =3D=3D "posLeft") {=0A= e.style.posLeft =3D value;=0A= }=0A= else if (name =3D=3D "posRight") {=0A= e.style.posRight =3D value;=0A= }=0A= else if (name =3D=3D "posTop") {=0A= e.style.posTop =3D value;=0A= }=0A= else if (name =3D=3D "posWidth") {=0A= e.style.posWidth =3D value;=0A= }=0A= else if (name =3D=3D "right") {=0A= e.style.right =3D value;=0A= }=0A= else if (name =3D=3D "ruby-align") {=0A= e.style.rubyAlign =3D value;=0A= }=0A= else if (name =3D=3D "ruby-overhang") {=0A= e.style.rubyOverhang =3D value;=0A= }=0A= else if (name =3D=3D "ruby-position") {=0A= e.style.rubyPosition =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-3dlight-color") {=0A= e.style.scrollbar3dLightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-arrow-color") {=0A= e.style.scrollbarArrowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-base-color") {=0A= e.style.scrollbarBaseColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-darkshadow-color") {=0A= e.style.scrollbarDarkShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-face-color") {=0A= e.style.scrollbarFaceColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-highlight-color") {=0A= e.style.scrollbarHighlightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-shadow-color") {=0A= e.style.scrollbarShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-track-color") {=0A= e.style.scrollbarTrackColor =3D value;=0A= }=0A= else if (name =3D=3D "float") {=0A= e.style.styleFloat =3D value;=0A= }=0A= else if (name =3D=3D "table-layout") {=0A= e.style.tableLayout =3D value;=0A= }=0A= else if (name =3D=3D "text-align") {=0A= e.style.textAlign =3D value;=0A= }=0A= else if (name =3D=3D "text-align-last") {=0A= e.style.textAlignLast =3D value;=0A= }=0A= else if (name =3D=3D "text-autospace") {=0A= e.style.textAutospace =3D value;=0A= }=0A= else if (name =3D=3D "text-decoration") {=0A= e.style.textDecoration =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationBlink") {=0A= e.style.textDecorationBlink =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationLineThrough") {=0A= e.style.textDecorationLineThrough =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationNone") {=0A= e.style.textDecorationNone =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationOverline") {=0A= e.style.textDecorationOverline =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationUnderline") {=0A= e.style.textDecorationUnderline =3D value;=0A= }=0A= else if (name =3D=3D "text-indent") {=0A= e.style.textIndent =3D value;=0A= }=0A= else if (name =3D=3D "text-justify") {=0A= e.style.textJustify =3D value;=0A= }=0A= else if (name =3D=3D "text-kashida-space") {=0A= e.style.textKashidaSpace =3D value;=0A= }=0A= else if (name =3D=3D "text-overflow") {=0A= e.style.textOverflow =3D value;=0A= }=0A= else if (name =3D=3D "text-transform") {=0A= e.style.textTransform =3D value;=0A= }=0A= else if (name =3D=3D "text-underline-position") {=0A= e.style.textUnderlinePosition =3D value;=0A= }=0A= else if (name =3D=3D "top") {=0A= e.style.top =3D value;=0A= }=0A= else if (name =3D=3D "unicode-bidi") {=0A= e.style.unicodeBidi =3D value;=0A= }=0A= else if (name =3D=3D "vertical-align") {=0A= e.style.verticalAlign =3D value;=0A= }=0A= else if (name =3D=3D "visibility") {=0A= e.style.visibility =3D value;=0A= }=0A= else if (name =3D=3D "white-space") {=0A= e.style.whiteSpace =3D value;=0A= }=0A= else if (name =3D=3D "width") {=0A= e.style.width =3D value;=0A= }=0A= else if (name =3D=3D "word-break") {=0A= e.style.wordBreak =3D value;=0A= }=0A= else if (name =3D=3D "word-spacing") {=0A= e.style.wordSpacing =3D value;=0A= }=0A= else if (name =3D=3D "word-wrap") {=0A= e.style.wordWrap =3D value;=0A= }=0A= else if (name =3D=3D "writing-mode") {=0A= e.style.writingMode =3D value;=0A= }=0A= else if (name =3D=3D "z-index") {=0A= e.style.zIndex =3D value;=0A= }=0A= else if (name =3D=3D "zoom") {=0A= e.style.zoom =3D value;=0A= }=0A= }=0A= catch (e) {=0A= /* ignore error on attempt to set e.style.[property] */=0A= }=0A= }=0A= }=0A= }=0A= ------=_NextPart_000_0000_01C6E545.7FA17670 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.pnas.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. For now we have to disable=0A= * the callback until we can track down a proper fix=0A= * (or everybody sanely upgrades to version 6 or 7!).=0A= */=0A= if (navigator) {=0A= var appname =3D navigator.appName;=0A= if (appname =3D=3D "Microsoft Internet Explorer") {=0A= var userAgent =3D navigator["userAgent"];=0A= var s =3D "MSIE ";=0A= var n =3D -1; =0A= if ((n =3D userAgent.indexOf(s)) !=3D -1) {=0A= var v =3D parseFloat(userAgent.substring(n+s.length));=0A= if (v < 6) {=0A= return;=0A= }=0A= }=0A= }=0A= }=0A= =0A= /*=0A= * Acquire table row element to update, initiate callback=0A= * to update table with Entrez Links.=0A= */=0A= var tr =3D document.getElementById('entrez_callback_'+pmid);=0A= if (!tr) {=0A= return;=0A= }=0A= var req =3D new XMLHttpRequest();=0A= if (!req) {=0A= return;=0A= }=0A= req.onreadystatechange =3D function() {=0A= if (req.readyState =3D=3D 4 && (req.status =3D=3D 200 || req.status = =3D=3D 304)) {=0A= var src =3D req.responseXML.documentElement;=0A= var dst =3D document.createDocumentFragment();=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], dst);=0A= }=0A= var tbl =3D tr.parentNode;=0A= tbl.replaceChild(dst, tr);=0A= }=0A= }=0A= req.open('GET', callback_url, true);=0A= req.send(null);=0A= }=0A= ------=_NextPart_000_0000_01C6E545.7FA17670 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.google-analytics.com/urchin.js //-- Google Analytics Urchin Module=0A= //-- Copyright 2005 Google, All Rights Reserved.=0A= =0A= //-- Urchin On Demand Settings ONLY=0A= var _uacct=3D""; // set up the Urchin Account=0A= var _userv=3D1; // service mode (0=3Dlocal,1=3Dremote,2=3Dboth)=0A= =0A= //-- UTM User Settings=0A= var _ufsc=3D1; // set client info flag (1=3Don|0=3Doff)=0A= var _udn=3D"auto"; // (auto|none|domain) set the domain name for cookies=0A= var _uhash=3D"on"; // (on|off) unique domain hash for cookies=0A= var _utimeout=3D"1800"; // set the inactive session timeout in seconds=0A= var _ugifpath=3D"/__utm.gif"; // set the web path to the __utm.gif file=0A= var _utsp=3D"|"; // transaction field separator=0A= var _uflash=3D1; // set flash version detect option (1=3Don|0=3Doff)=0A= var _utitle=3D1; // set the document title detect option = (1=3Don|0=3Doff)=0A= var _ulink=3D0; // enable linker functionality (1=3Don|0=3Doff)=0A= var _uanchor=3D0; // enable use of anchors for campaign = (1=3Don|0=3Doff)=0A= =0A= //-- UTM Campaign Tracking Settings=0A= var _uctm=3D1; // set campaign tracking module (1=3Don|0=3Doff)=0A= var _ucto=3D"15768000"; // set timeout in seconds (6 month default)=0A= var _uccn=3D"utm_campaign"; // name=0A= var _ucmd=3D"utm_medium"; // medium (cpc|cpm|link|email|organic)=0A= var _ucsr=3D"utm_source"; // source=0A= var _uctr=3D"utm_term"; // term/keyword=0A= var _ucct=3D"utm_content"; // content=0A= var _ucid=3D"utm_id"; // id number=0A= var _ucno=3D"utm_nooverride"; // don't override=0A= =0A= //-- Auto/Organic Sources and Keywords=0A= var _uOsr=3Dnew Array();=0A= var _uOkw=3Dnew Array();=0A= _uOsr[0]=3D"google"; 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path=3D"+_utcp+"; = expires=3DSun, 18 Jan 2038 00:00:00 GMT;"+_udo;=0A= var s=3D"&utmt=3Dvar&utmn=3D"+r;=0A= if (_userv=3D=3D0 || _userv=3D=3D2) {=0A= var i=3Dnew Image(1,1);=0A= i.src=3D_ugifpath+"?"+"utmwv=3D"+_uwv+s;=0A= i.onload=3Dfunction() { _uVoid(); }=0A= }=0A= if (_userv=3D=3D1 || _userv=3D=3D2) {=0A= var i2=3Dnew Image(1,1);=0A= = i2.src=3D_ugifpath2+"?"+"utmwv=3D"+_uwv+s+"&utmac=3D"+_uacct+"&utmcc=3D"+= _uGCS();=0A= i2.onload=3Dfunction() { _uVoid(); }=0A= }=0A= }=0A= function _uGCS() {=0A= var t,c=3D"",dc=3D_ubd.cookie;=0A= if ((t=3D_uGC(dc,"__utma=3D"+_udh,";"))!=3D"-") = c+=3D_uES("__utma=3D"+t+";+");=0A= if ((t=3D_uGC(dc,"__utmb=3D"+_udh,";"))!=3D"-") = c+=3D_uES("__utmb=3D"+t+";+");=0A= if ((t=3D_uGC(dc,"__utmc=3D"+_udh,";"))!=3D"-") = c+=3D_uES("__utmc=3D"+t+";+");=0A= if ((t=3D_uGC(dc,"__utmz=3D"+_udh,";"))!=3D"-") = c+=3D_uES("__utmz=3D"+t+";+");=0A= if ((t=3D_uGC(dc,"__utmv=3D"+_udh,";"))!=3D"-") = c+=3D_uES("__utmv=3D"+t+";");=0A= if (c.charAt(c.length-1)=3D=3D"+") c=3Dc.substring(0,c.length-1);=0A= return c;=0A= }=0A= function _uGC(l,n,s) {=0A= if (!l || l=3D=3D"" || !n || n=3D=3D"" || !s || s=3D=3D"") return "-";=0A= var i,i2,i3,c=3D"-";=0A= i=3Dl.indexOf(n);=0A= i3=3Dn.indexOf("=3D")+1;=0A= if (i > -1) {=0A= i2=3Dl.indexOf(s,i); 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