Fibroblast Growth Factor Receptor-Dependent and -Independent Paracrine Signaling by Sunitinib-Resistant Renal Cell Carcinoma

REFERENCES

• Nickerson ML, Jaeger E, Shi Y, Durocher JA, Mahurkar S, Zaridze D, Matveev V, Janout V, Kollarova H, Bencko V, Navratilova M, Szeszenia-Dabrowska N, Mates D, Mukeria A, Holcatova I, Schmidt LS, Toro JR, Karami S, Hung R, Gerard GF, Linehan WM, Merino M, Zbar B, Boffetta P, Brennan P, Rothman N, Chow WH, Waldman FM, Moore LE. 2008. Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. Clin Cancer Res 14:4726–4734. http://dx.doi.org/10.1158/1078-0432.CCR-07-4921.
   PubMed Web of Science ®Google Scholar
• Linehan WM, Walther MM, Zbar B. 2003. The genetic basis of cancer of the kidney. J Urol 170:2163–2172. http://dx.doi.org/10.1097/01.ju.0000096060.92397.ed.
   PubMed Web of Science ®Google Scholar
• Duan DR, Pause A, Burgess WH, Aso T, Chen DY, Garrett KP, Conaway RC, Conaway JW, Linehan WM, Klausner RD. 1995. Inhibition of transcription elongation by the VHL tumor suppressor protein. Science 269:1402–1406. http://dx.doi.org/10.1126/science.7660122.
   PubMed Web of Science ®Google Scholar
• Kamura T, Sato S, Iwai K, Czyzyk-Krzeska M, Conaway RC, Conaway JW. 2000. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci U S A 97:10430–10435. http://dx.doi.org/10.1073/pnas.190332597.
   PubMed Web of Science ®Google Scholar
• Kibel A, Iliopoulos O, DeCaprio JA, Kaelin WG, Jr. 1995. Binding of the von Hippel-Lindau tumor suppressor protein to elongin B and C. Science 269:1444–1446. http://dx.doi.org/10.1126/science.7660130.
   PubMed Web of Science ®Google Scholar
• Kishida T, Stackhouse TM, Chen F, Lerman MI, Zbar B. 1995. Cellular proteins that bind the von Hippel-Lindau disease gene product: mapping of binding domains and the effect of missense mutations. Cancer Res 55:4544–4548.
   PubMed Web of Science ®Google Scholar
• Lonergan KM, Iliopoulos O, Ohh M, Kamura T, Conaway RC, Conaway JW, Kaelin WG, Jr. 1998. Regulation of hypoxia-inducible mRNAs by the von Hippel-Lindau tumor suppressor protein requires binding to complexes containing elongins B/C and Cul2. Mol Cell Biol 18:732–741. http://dx.doi.org/10.1128/MCB.18.2.732.
   PubMed Web of Science ®Google Scholar
• Pause A, Lee S, Worrell RA, Chen DY, Burgess WH, Linehan WM, Klausner RD. 1997. The von Hippel-Lindau tumor-suppressor gene product forms a stable complex with human CUL-2, a member of the Cdc53 family of proteins. Proc Natl Acad Sci U S A 94:2156–2161. http://dx.doi.org/10.1073/pnas.94.6.2156.
   PubMed Web of Science ®Google Scholar
• Kamura T, Koepp DM, Conrad MN, Skowyra D, Moreland RJ, Iliopoulos O, Lane WS, Kaelin WG, Jr, Elledge SJ, Conaway RC, Harper JW, Conaway JW. 1999. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 284:657–661. http://dx.doi.org/10.1126/science.284.5414.657.
   PubMed Web of Science ®Google Scholar
• Cockman ME, Masson N, Mole DR, Jaakkola P, Chang GW, Clifford SC, Maher ER, Pugh CW, Ratcliffe PJ, Maxwell PH. 2000. Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem 275:25733–25741. http://dx.doi.org/10.1074/jbc.M002740200.
   PubMed Web of Science ®Google Scholar
• Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271–275. http://dx.doi.org/10.1038/20459.
   PubMed Web of Science ®Google Scholar
• Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, Huang LE, Pavletich N, Chau V, Kaelin WG. 2000. Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat Cell Biol 2:423–427. http://dx.doi.org/10.1038/35017054.
   PubMed Web of Science ®Google Scholar
• Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E. 1998. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394:485–490. http://dx.doi.org/10.1038/28867.
   PubMed Web of Science ®Google Scholar
• Ferrara N, Hillan KJ, Gerber HP, Novotny W. 2004. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov 3:391–400. http://dx.doi.org/10.1038/nrd1381.
   PubMed Web of Science ®Google Scholar
• Escudier B, Bellmunt J, Negrier S, Bajetta E, Melichar B, Bracarda S, Ravaud A, Golding S, Jethwa S, Sneller V. 2010. Phase III trial of bevacizumab plus interferon alfa-2a in patients with metastatic renal cell carcinoma (AVOREN): final analysis of overall survival. J Clin Oncol 28:2144–2150. http://dx.doi.org/10.1200/JCO.2009.26.7849.
   PubMed Web of Science ®Google Scholar
• Rini BI, Halabi S, Rosenberg JE, Stadler WM, Vaena DA, Archer L, Atkins JN, Picus J, Czaykowski P, Dutcher J, Small EJ. 2010. Phase III trial of bevacizumab plus interferon alfa versus interferon alfa monotherapy in patients with metastatic renal cell carcinoma: final results of CALGB 90206. J Clin Oncol 28:2137–2143. http://dx.doi.org/10.1200/JCO.2009.26.5561.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Oudard S, Negrier S, Szczylik C, Pili R, Bjarnason GA, Garcia-del-Muro X, Sosman JA, Solska E, Wilding G, Thompson JA, Kim ST, Chen I, Huang X, Figlin RA. 2009. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J Clin Oncol 27:3584–3590. http://dx.doi.org/10.1200/JCO.2008.20.1293.
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Rixe O, Oudard S, Negrier S, Szczylik C, Kim ST, Chen I, Bycott PW, Baum CM, Figlin RA. 2007. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 356:115–124. http://dx.doi.org/10.1056/NEJMoa065044.
   PubMed Web of Science ®Google Scholar
• Engelman JA, Janne PA. 2008. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 14:2895–2899. http://dx.doi.org/10.1158/1078-0432.CCR-07-2248.
   PubMed Web of Science ®Google Scholar
• Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, Kosaka T, Holmes AJ, Rogers AM, Cappuzzo F, Mok T, Lee C, Johnson BE, Cantley LC, Janne PA. 2007. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316:1039–1043. http://dx.doi.org/10.1126/science.1141478.
   PubMed Web of Science ®Google Scholar
• Ogino A, Kitao H, Hirano S, Uchida A, Ishiai M, Kozuki T, Takigawa N, Takata M, Kiura K, Tanimoto M. 2007. Emergence of epidermal growth factor receptor T790M mutation during chronic exposure to gefitinib in a non small cell lung cancer cell line. Cancer Res 67:7807–7814. http://dx.doi.org/10.1158/0008-5472.CAN-07-0681.
   PubMed Web of Science ®Google Scholar
• Yamasaki F, Johansen MJ, Zhang D, Krishnamurthy S, Felix E, Bartholomeusz C, Aguilar RJ, Kurisu K, Mills GB, Hortobagyi GN, Ueno NT. 2007. Acquired resistance to erlotinib in A-431 epidermoid cancer cells requires down-regulation of MMAC1/PTEN and up-regulation of phosphorylated Akt. Cancer Res 67:5779–5788. http://dx.doi.org/10.1158/0008-5472.CAN-06-3020.
   PubMed Web of Science ®Google Scholar
• Welti JC, Gourlaouen M, Powles T, Kudahetti SC, Wilson P, Berney DM, Reynolds AR. 2011. Fibroblast growth factor 2 regulates endothelial cell sensitivity to sunitinib. Oncogene 30:1183–1193. http://dx.doi.org/10.1038/onc.2010.503.
   PubMed Web of Science ®Google Scholar
• Casanovas O, Hicklin DJ, Bergers G, Hanahan D. 2005. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 8:299–309. http://dx.doi.org/10.1016/j.ccr.2005.09.005.
   PubMed Web of Science ®Google Scholar
• Sivanand S, Pena-Llopis S, Zhao H, Kucejova B, Spence P, Pavia-Jimenez A, Yamasaki T, McBride DJ, Gillen J, Wolff NC, Morlock L, Lotan Y, Raj GV, Sagalowsky A, Margulis V, Cadeddu JA, Ross MT, Bentley DR, Kabbani W, Xie XJ, Kapur P, Williams NS, Brugarolas J. 2012. A validated tumorgraft model reveals activity of dovitinib against renal cell carcinoma. Sci Transl Med 4:137ra175.
   Google Scholar
• Kucejova B, Pena-Llopis S, Yamasaki T, Sivanand S, Tran TA, Alexander S, Wolff NC, Lotan Y, Xie XJ, Kabbani W, Kapur P, Brugarolas J. 2011. Interplay between pVHL and mTORC1 pathways in clear-cell renal cell carcinoma. Mol Cancer Res 9:1255–1265. http://dx.doi.org/10.1158/1541-7786.MCR-11-0302.
   PubMed Web of Science ®Google Scholar
• Vega-Rubin-de-Celis S, Abdallah Z, Kinch L, Grishin NV, Brugarolas J, Zhang X. 2010. Structural analysis and functional implications of the negative mTORC1 regulator REDD1. Biochemistry 49:2491–2501. http://dx.doi.org/10.1021/bi902135e.
   PubMedGoogle Scholar
• Peña-Llopis S, Brugarolas J. 2013. Simultaneous isolation of high-quality DNA, RNA, miRNA and proteins from tissues for genomic applications. Nat Protoc 8:2240–2255. http://dx.doi.org/10.1038/nprot.2013.141.
   PubMedGoogle Scholar
• Leong HS, Steinmetz NF, Ablack A, Destito G, Zijlstra A, Stuhlmann H, Manchester M, Lewis JD. 2010. Intravital imaging of embryonic and tumor neovasculature using viral nanoparticles. Nat Protoc 5:1406–1417. http://dx.doi.org/10.1038/nprot.2010.103.
   PubMed Web of Science ®Google Scholar
• Leong HS, Chambers AF, Lewis JD. 2012. Assessing cancer cell migration and metastatic growth in vivo in the chick embryo using fluorescence intravital imaging. Methods Mol Biol 872:1–14. http://dx.doi.org/10.1007/978-1-61779-797-2_1.
   PubMedGoogle Scholar
• Cho CF, Ablack A, Leong HS, Zijlstra A, Lewis J. 21 June 2011. Evaluation of nanoparticle uptake in tumors in real time using intravital imaging. J Vis Exp http://dx.doi.org/10.3791/2808.
   Google Scholar
• Sun L, Liang C, Shirazian S, Zhou Y, Miller T, Cui J, Fukuda JY, Chu JY, Nematalla A, Wang XY, Chen H, Sistla A, Luu TC, Tang F, Wei J, Tang C. 2003. Discovery of 5-5-fluoro-2-oxo-1,2-dihydroindol-(3Z)-ylidenemethyl-2,4-dimethyl-1H-p yrrole-3-carboxylic acid (2-diethylaminoethyl)amide, a novel tyrosine kinase inhibitor targeting vascular endothelial and platelet-derived growth factor receptor tyrosine kinase. J Med Chem 46:1116–1119. http://dx.doi.org/10.1021/jm0204183.
   PubMed Web of Science ®Google Scholar
• Faivre S, Demetri G, Sargent W, Raymond E. 2007. Molecular basis for sunitinib efficacy and future clinical development. Nat Rev Drug Discov 6:734–745. http://dx.doi.org/10.1038/nrd2380.
   PubMed Web of Science ®Google Scholar
• Greenman C, Stephens P, Smith R, Dalgliesh GL, Hunter C, Bignell G, Davies H, Teague J, Butler A, Stevens C, Edkins S, O'Meara S, Vastrik I, Schmidt EE, Avis T, Barthorpe S, Bhamra G, Buck G, Choudhury B, Clements J, Cole J, Dicks E, Forbes S, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jenkinson A, Jones D, Menzies A, Mironenko T, Perry J, Raine K, Richardson D, Shepherd R, Small A, Tofts C, Varian J, Webb T, West S, Widaa S, Yates A, Cahill DP, Louis DN, Goldstraw P, Nicholson AG, Brasseur F, Looijenga L, Weber BL, et al.. 2007. Patterns of somatic mutation in human cancer genomes. Nature 446:153–158. http://dx.doi.org/10.1038/nature05610.
   PubMed Web of Science ®Google Scholar
• Bender C, Ullrich A. 28 February 2012. PRKX, TTBK2 and RSK4 expression causes sunitinib resistance in kidney carcinoma- and melanoma-cell lines. Int J Cancer http://dx.doi.org/10.1002/ijc.26486.
   Google Scholar
• Gotink KJ, Broxterman HJ, Labots M, de Haas RR, Dekker H, Honeywell RJ, Rudek MA, Beerepoot LV, Musters RJ, Jansen G, Griffioen AW, Assaraf YG, Pili R, Peters GJ, Verheul HM. 2011. Lysosomal sequestration of sunitinib: a novel mechanism of drug resistance. Clin Cancer Res 17:7337–7346. http://dx.doi.org/10.1158/1078-0432.CCR-11-1667.
   PubMed Web of Science ®Google Scholar
• Huang D, Ding Y, Li Y, Luo WM, Zhang ZF, Snider J, Vandenbeldt K, Qian CN, Teh BT. 2010. Sunitinib acts primarily on tumor endothelium rather than tumor cells to inhibit the growth of renal cell carcinoma. Cancer Res 70:1053–1062. http://dx.doi.org/10.1158/0008-5472.CAN-09-3722.
   PubMed Web of Science ®Google Scholar
• Faivre S, Delbaldo C, Vera K, Robert C, Lozahic S, Lassau N, Bello C, Deprimo S, Brega N, Massimini G, Armand JP, Scigalla P, Raymond E. 2006. Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer. J Clin Oncol 24:25–35. http://dx.doi.org/10.1200/JCO.2005.02.2194.
   PubMed Web of Science ®Google Scholar
• Atkins MB, Hidalgo M, Stadler WM, Logan TF, Dutcher JP, Hudes GR, Park Y, Liou SH, Marshall B, Boni JP, Dukart G, Sherman ML. 2004. Randomized phase II study of multiple dose levels of CCI-779, a novel mammalian target of rapamycin kinase inhibitor, in patients with advanced refractory renal cell carcinoma. J Clin Oncol 22:909–918. http://dx.doi.org/10.1200/JCO.2004.08.185.
   PubMed Web of Science ®Google Scholar
• Beroukhim R, Brunet JP, Di Napoli A, Mertz KD, Seeley A, Pires MM, Linhart D, Worrell RA, Moch H, Rubin MA, Sellers WR, Meyerson M, Linehan WM, Kaelin WG, Jr, Signoretti S. 2009. Patterns of gene expression and copy-number alterations in von Hippel-Lindau disease-associated and sporadic clear cell carcinoma of the kidney. Cancer Res 69:4674–4681. http://dx.doi.org/10.1158/0008-5472.CAN-09-0146.
   PubMed Web of Science ®Google Scholar
• Kaelin WG. 2012. Molecular biology of clear cell renal cell carcinoma, p 283–303. In Figlin RA, Rathmell WK, Rini BI (ed), Renal cell carcinoma: translational biology, personalized medicine, and novel therapeutic targets. Springer, New York, NY.
   Google Scholar
• Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. 1998. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. J Biol Chem 273:30336–30343.
   PubMed Web of Science ®Google Scholar
• Gospodarowicz D, Moran J, Braun D, Birdwell C. 1976. Clonal growth of bovine vascular endothelial cells: fibroblast growth factor as a survival agent. Proc Natl Acad Sci U S A 73:4120–4124. http://dx.doi.org/10.1073/pnas.73.11.4120.
   PubMed Web of Science ®Google Scholar
• Cenni E, Perut F, Granchi D, Avnet S, Amato I, Brandi ML, Giunti A, Baldini N. 2007. Inhibition of angiogenesis via FGF-2 blockage in primitive and bone metastatic renal cell carcinoma. Anticancer Res 27:315–319.
   PubMed Web of Science ®Google Scholar
• Nakagawa M, Emoto A, Hanada T, Nasu N, Nomura Y. 1997. Tubulogenesis by microvascular endothelial cells is mediated by vascular endothelial growth factor (VEGF) in renal cell carcinoma. Br J Urol 79:681–687. http://dx.doi.org/10.1046/j.1464-410X.1997.00140.x.
   PubMedGoogle Scholar
• Shi W, Siemann DW. 2002. Inhibition of renal cell carcinoma angiogenesis and growth by antisense oligonucleotides targeting vascular endothelial growth factor. Br J Cancer 87:119–126. http://dx.doi.org/10.1038/sj.bjc.6600416.
   PubMed Web of Science ®Google Scholar
• Gnarra JR, Tory K, Weng Y, Schmidt L, Wei MH, Li H, Latif F, Liu S, Chen F, Duh FM, Lubensky I, Duan DR, Florence C, Pozzatti R, Walther MM, Bander NH, Grossman HB, Brauch H, Pomer S, Brooks JD, Isaacs WB, Lerman MI, Zbar B, Linehan WM. 1994. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat Genet 7:85–90. http://dx.doi.org/10.1038/ng0594-85.
   PubMed Web of Science ®Google Scholar
• Iliopoulos O, Kibel A, Gray S, Kaelin WG, Jr. 1995. Tumour suppression by the human von Hippel-Lindau gene product. Nat Med 1:822–826. http://dx.doi.org/10.1038/nm0895-822.
   PubMed Web of Science ®Google Scholar
• Potapova O, Laird AD, Nannini MA, Barone A, Li G, Moss KG, Cherrington JM, Mendel DB. 2006. Contribution of individual targets to the antitumor efficacy of the multitargeted receptor tyrosine kinase inhibitor SU11248. Mol Cancer Ther 5:1280–1289. http://dx.doi.org/10.1158/1535-7163.MCT-03-0156.
   PubMed Web of Science ®Google Scholar
• Ribatti D, Nico B, Vacca A, Presta M. 2006. The gelatin sponge-chorioallantoic membrane assay. Nat Protoc 1:85–91. http://dx.doi.org/10.1038/nprot.2006.13.
   PubMed Web of Science ®Google Scholar
• Ribatti D, Nico B, Vacca A, Roncali L, Burri PH, Djonov V. 2001. Chorioallantoic membrane capillary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo. Anat Rec 264:317–324. http://dx.doi.org/10.1002/ar.10021.
   PubMedGoogle Scholar
• Ausprunk DH, Knighton DR, Folkman J. 1975. Vascularization of normal and neoplastic tissues grafted to the chick chorioallantois. Role of host and preexisting graft blood vessels. Am J Pathol 79:597–618.
   PubMed Web of Science ®Google Scholar
• Ribatti D. 2008. The chick embryo chorioallantoic membrane in the study of tumor angiogenesis. Rom J Morphol Embryol 49:131–135.
   PubMed Web of Science ®Google Scholar
• Pan CC, Chen PC, Ho DM. 2004. The diagnostic utility of MOC31, BerEP4, RCC marker and CD10 in the classification of renal cell carcinoma and renal oncocytoma: an immunohistochemical analysis of 328 cases. Histopathology 45:452–459. http://dx.doi.org/10.1111/j.1365-2559.2004.01962.x.
   PubMed Web of Science ®Google Scholar
• Shen SS, Truong LD, Scarpelli M, Lopez-Beltran A. 2012. Role of immunohistochemistry in diagnosing renal neoplasms: when is it really useful? Arch Pathol Lab Med 136:410–417. http://dx.doi.org/10.5858/arpa.2011-0472-RA.
   PubMedGoogle Scholar
• Bikfalvi A, Klein S, Pintucci G, Rifkin DB. 1997. Biological roles of fibroblast growth factor-2. Endocr Rev 18:26–45.
   PubMed Web of Science ®Google Scholar
• Chow LQ, Eckhardt SG. 2007. Sunitinib: from rational design to clinical efficacy. J Clin Oncol 25:884–896. http://dx.doi.org/10.1200/JCO.2006.06.3602.
   PubMed Web of Science ®Google Scholar
• Mendel DB, Laird AD, Xin X, Louie SG, Christensen JG, Li G, Schreck RE, Abrams TJ, Ngai TJ, Lee LB, Murray LJ, Carver J, Chan E, Moss KG, Haznedar JO, Sukbuntherng J, Blake RA, Sun L, Tang C, Miller T, Shirazian S, McMahon G, Cherrington JM. 2003. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 9:327–337.
   PubMed Web of Science ®Google Scholar
• Basilico C, Moscatelli D. 1992. The FGF family of growth factors and oncogenes. Adv Cancer Res 59:115–165. http://dx.doi.org/10.1016/S0065-230X(08)60305-X.
   PubMed Web of Science ®Google Scholar
• Turner N, Grose R. 2010. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10:116–129. http://dx.doi.org/10.1038/nrc2780.
   PubMed Web of Science ®Google Scholar
• Hadari YR, Gotoh N, Kouhara H, Lax I, Schlessinger J. 2001. Critical role for the docking-protein FRS2 alpha in FGF receptor-mediated signal transduction pathways. Proc Natl Acad Sci U S A 98:8578–8583. http://dx.doi.org/10.1073/pnas.161259898.
   PubMedGoogle Scholar
• Lax I, Wong A, Lamothe B, Lee A, Frost A, Hawes J, Schlessinger J. 2002. The docking protein FRS2alpha controls a MAP kinase-mediated negative feedback mechanism for signaling by FGF receptors. Mol Cell 10:709–719. http://dx.doi.org/10.1016/S1097-2765(02)00689-5.
   PubMedGoogle Scholar
• Motzer RJ, Porta C, Vogelzang NJ, Sternberg CN, Szczylik C, Zolnierek J, Kollmannsberger C, Rha SY, Bjarnason GA, Melichar B, De Giorgi U, Grunwald V, Davis ID, Lee JL, Esteban E, Urbanowitz G, Cai C, Squires M, Marker M, Shi MM, Escudier B. 2014. Dovitinib versus sorafenib for third-line targeted treatment of patients with metastatic renal cell carcinoma: an open-label, randomised phase 3 trial. Lancet Oncol 15:286–296.
   PubMed Web of Science ®Google Scholar
• Rini BI, Michaelson MD, Rosenberg JE, Bukowski RM, Sosman JA, Stadler WM, Hutson TE, Margolin K, Harmon CS, DePrimo SE, Kim ST, Chen I, George DJ. 2008. Antitumor activity and biomarker analysis of sunitinib in patients with bevacizumab-refractory metastatic renal cell carcinoma. J Clin Oncol 26:3743–3748. http://dx.doi.org/10.1200/JCO.2007.15.5416.
   PubMed Web of Science ®Google Scholar
• Tran HT, Liu Y, Zurita AJ, Lin Y, Baker-Neblett KL, Martin AM, Figlin RA, Hutson TE, Sternberg CN, Amado RG, Pandite LN, Heymach JV. 2 July 2012. Prognostic or predictive plasma cytokines and angiogenic factors for patients treated with pazopanib for metastatic renal-cell cancer: a retrospective analysis of phase 2 and phase 3 trials. Lancet Oncol http://dx.doi.org/10.1016/S1470-2045(12)70241-3.
   Google Scholar
• Paule B, Bastien L, Deslandes E, Cussenot O, Podgorniak MP, Allory Y, Naimi B, Porcher R, de La Taille A, Menashi S, Calvo F, Mourah S. 2010. Soluble isoforms of vascular endothelial growth factor are predictors of response to sunitinib in metastatic renal cell carcinomas. PLoS One 5:e10715. http://dx.doi.org/10.1371/journal.pone.0010715.
   PubMed Web of Science ®Google Scholar
• Bhargava M, Joseph A, Knesel J, Halaban R, Li Y, Pang S, Goldberg I, Setter E, Donovan MA, Zarnegar R, Michalopoulos GA, Nakamura T, Faletto D, Rosen EM. 1992. Scatter factor and hepatocyte growth factor: activities, properties, and mechanism. Cell Growth Differ 3:11–20.
   PubMedGoogle Scholar
• Rong S, Bodescot M, Blair D, Dunn J, Nakamura T, Mizuno K, Park M, Chan A, Aaronson S, Vande Woude GF. 1992. Tumorigenicity of the met proto-oncogene and the gene for hepatocyte growth factor. Mol Cell Biol 12:5152–5158. http://dx.doi.org/10.1128/MCB.12.11.5152.
   PubMed Web of Science ®Google Scholar
• Zhang YW, Su Y, Lanning N, Gustafson M, Shinomiya N, Zhao P, Cao B, Tsarfaty G, Wang LM, Hay R, Vande Woude GF. 2005. Enhanced growth of human met-expressing xenografts in a new strain of immunocompromised mice transgenic for human hepatocyte growth factor/scatter factor. Oncogene 24:101–106. http://dx.doi.org/10.1038/sj.onc.1208181.
   PubMedGoogle Scholar
• Shojaei F, Wu X, Malik AK, Zhong C, Baldwin ME, Schanz S, Fuh G, Gerber HP, Ferrara N. 2007. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+ Gr1+ myeloid cells. Nat Biotechnol 25:911–920. http://dx.doi.org/10.1038/nbt1323.
   PubMed Web of Science ®Google Scholar