Resistance to tyrosine kinase inhibitors in clear cell renal cell carcinoma: From the patient's bed to molecular mechanisms

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1845, Issue 1, 2014, Pages 31-41

  Buczek, Magdalena ^a   Escudier, Bernard ^b   Bartnik, Ewa ^c   Szczylik, Cezary ^a   Czarnecka, Anna ^a  

^a MILITARY INSTITUTE OF MEDICINE   (Poland)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

Acquired and intrinsic resistance; Angiogenesis; Clear cell renal cell carcinoma; Drug resistance; Tyrosine kinase inhibitors

Indexed keywords

ANTINEOPLASTIC AGENT; PROTEIN TYROSINE KINASE INHIBITOR; SUNITINIB; VASCULOTROPIN;

APOPTOSIS; CLINICAL RESEARCH; DRUG MECHANISM; DRUG RESPONSE; HUMAN; IMMUNOMODULATION; INFLAMMATORY CELL; KIDNEY CARCINOMA; LYSOSOME; METASTASIS; NONHUMAN; PERICYTE; PRIORITY JOURNAL; REVIEW; TUMOR INVASION; TUMOR VASCULARIZATION; UPREGULATION;

ACQUIRED AND INTRINSIC RESISTANCE; ANGIOGENESIS; CLEAR CELL RENAL CELL CARCINOMA; DRUG RESISTANCE; TYROSINE KINASE INHIBITORS;

ANIMALS; APOPTOSIS; CARCINOMA, RENAL CELL; DRUG RESISTANCE, NEOPLASM; HUMANS; KIDNEY NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84890182925     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2013.10.001     Document Type: Review

References (131)

1. Escudier B., Eisen T., Stadler W.M., Szczylik C., Oudard S., Siebels M., Negrier S., Chevreau C., Solska E., Desai A.A., Rolland F., Demkow T., Hutson T.E., Gore M., Freeman S., Schwartz B., Shan M., Simantov R., Bukowski R.M. Sorafenib in advanced clear-cell renal-cell carcinoma. N. Engl. J. Med. 2007, 356:125-134.
2. Motzer R.J., Escudier B., Oudard S., Hutson T.E., Porta C., Bracarda S., Grunwald V., Thompson J.A., Figlin R.A., Hollaender N., Urbanowitz G., Berg W.J., Kay A., Lebwohl D., Ravaud A. Efficacy of everolimus in advanced renal cell carcinoma: a double-blind, randomised, placebo-controlled phase III trial. Lancet 2008, 372:449-456.
3. Motzer R.J., Hutson T.E., Tomczak P., Michaelson M.D., Bukowski R.M., Rixe O., Oudard S., Negrier S., Szczylik C., Kim S.T., Chen I., Bycott P.W., Baum C.M., Figlin R.A. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N. Engl. J. Med. 2007, 356:115-124.
4. Sternberg C.N., Davis I.D., Mardiak J., Szczylik C., Lee E., Wagstaff J., Barrios C.H., Salman P., Gladkov O.A., Kavina A., Zarba J.J., Chen M., McCann L., Pandite L., Roychowdhury D.F., Hawkins R.E. Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial. J. Clin. Oncol. 2010, 28:1061-1068.
5. Thomas G.V., Tran C., Mellinghoff I.K., Welsbie D.S., Chan E., Fueger B., Czernin J., Sawyers C.L. Hypoxia-inducible factor determines sensitivity to inhibitors of mTOR in kidney cancer. Nat. Med. 2006, 12:122-127.
6. Mills E.J., Rachlis B., O'Regan C., Thabane L., Perri D. Metastatic renal cell cancer treatments: an indirect comparison meta-analysis. BMC Cancer 2009, 9:34.
7. Ravaud A., Gross-Goupil M. Overcoming resistance to tyrosine kinase inhibitors in renal cell carcinoma. Cancer Treat. Rev. 2012, 38(8):996-1003.
8. Rini B.I., Atkins M.B. Resistance to targeted therapy in renal-cell carcinoma. Lancet Oncol. 2009, 10:992-1000.
9. Motzer R.J., Hutson T.E., Tomczak P., Michaelson M.D., Bukowski R.M., Oudard S., Negrier S., Szczylik C., Pili R., Bjarnason G.A., Garcia-del-Muro X., Sosman J.A., Solska E., Wilding G., Thompson J.A., Kim S.T., Chen I., Huang X., Figlin R.A. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 2009, 27:3584-3590.
10. Albiges L., Oudard S., Negrier S., Caty A., Gravis G., Joly F., Duclos B., Geoffrois L., Rolland F., Guillot A., Laguerre B., Legouffe E., Kohser F., Dietrich P.Y., Theodore C.A., Escudier B. Complete remission with tyrosine kinase inhibitors in renal cell carcinoma. J. Clin. Oncol. 2012, 30:482-487.
11. National Comprehensive Cancer Network NCCN Clinical Practive Guidelines in Oncology Kidney Cancer 2012, (in, vol.).
12. Eisen T., Escudier B., Porta C., Patard J.J., Khoo V., Algaba F., Mulders P., Kataja V. Renal cell carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of Oncology vol. Suppl 7 2012, vii65-vii71.
13. Busch J., Seidel C., Weikert S., Wolff I., Kempkensteffen C., Weinkauf L., Hinz S., Magheli A., Miller K., Grunwald V. Intrinsic resistance to tyrosine kinase inhibitors is associated with poor clinical outcome in metastatic renal cell carcinoma. BMC cancer 2011, 11:295.
14. Park K., Lee J.L., Park I., Park S., Ahn Y., Ahn J.H., Ahn S., Song C., Hong J.H., Kim C.S., Ahn H. Comparative efficacy of vascular endothelial growth factor (VEGF) tyrosine kinase inhibitor (TKI) and mammalian target of rapamycin (mTOR) inhibitor as second-line therapy in patients with metastatic renal cell carcinoma after the failure of first-line VEGF TKI. Med. Oncol. 2012, 29(5):3291-3297.
15. Zhang L., Bhasin M., Schor-Bardach R., Wang X., Collins M.P., Panka D., Putheti P., Signoretti S., Alsop D.C., Libermann T., Atkins M.B., Mier J.W., Goldberg S.N., Bhatt R.S. Resistance of renal cell carcinoma to sorafenib is mediated by potentially reversible gene expression. PloS One 2011, 6:e19144.
16. Huang D., Ding Y., Zhou M., Rini B.I., Petillo D., Qian C.N., Kahnoski R., Futreal P.A., Furge K.A., Teh B.T. Interleukin-8 mediates resistance to antiangiogenic agent sunitinib in renal cell carcinoma. Cancer Res. 2010, 70:1063-1071.
17. Bergers G., Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 2008, 8:592-603.
18. Gorre M.E., Sawyers C.L. Molecular mechanisms of resistance to STI571 in chronic myeloid leukemia. Curr. Opin. Hematol. 2002, 9:303-307.
19. O'Connor R., Clynes M., Dowling P., O'Donovan N., O'Driscoll L. Drug resistance in cancer - searching for mechanisms, markers and therapeutic agents. Expert. Opin. Drug. Metab. Toxicol. 2007, 3:805-817.
20. Gottesman M.M., Fojo T., Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2002, 2:48-58.
21. Gotink K.J., Broxterman H.J., Labots M., de Haas R.R., Dekker H., Honeywell R.J., Rudek M.A., Beerepoot L.V., Musters R.J., Jansen G., Griffioen A.W., Assaraf Y.G., Pili R., Peters G.J., Verheul H.M. Lysosomal sequestration of sunitinib: a novel mechanism of drug resistance. Clin. Cancer Res. 2011, 17:7337-7346.
22. Bhatt R.S., Atkins M.B. Translational research studies in renal cancer: mechanisms and management of resistance to anti-VEGF therapy in renal cell carcinoma. InforMEDical 2012.
23. Casanovas O., Hicklin D.J., Bergers G., Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005, 8:299-309.
24. Batchelor T.T., Sorensen A.G., di Tomaso E., Zhang W.T., Duda D.G., Cohen K.S., Kozak K.R., Cahill D.P., Chen P.J., Zhu M., Ancukiewicz M., Mrugala M.M., Plotkin S., Drappatz J., Louis D.N., Ivy P., Scadden D.T., Benner T., Loeffler J.S., Wen P.Y., Jain R.K. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007, 11:83-95.
25. Mizukami Y., Jo W.S., Duerr E.M., Gala M., Li J., Zhang X., Zimmer M.A., Iliopoulos O., Zukerberg L.R., Kohgo Y., Lynch M.P., Rueda B.R., Chung D.C. Induction of interleukin-8 preserves the angiogenic response in HIF-1alpha-deficient colon cancer cells. Nat. Med. 2005, 11:992-997.
26. Teh B.T., Huang D., Ding Y., Zhou M., Rini B.I., Petillo D., Qian C., Kahnoski R.J., Futreal P., Furge K.A. The mechanism of action and resistance of sunitinib in RCC. ASCO Annual Meeting 2010 2010.
27. Fischer C., Jonckx B., Mazzone M., Zacchigna S., Loges S., Pattarini L., Chorianopoulos E., Liesenborghs L., Koch M., De Mol M., Autiero M., Wyns S., Plaisance S., Moons L., van Rooijen N., Giacca M., Stassen J.M., Dewerchin M., Collen D., Carmeliet P. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 2007, 131:463-475.
28. Autiero M., Luttun A., Tjwa M., Carmeliet P. Placental growth factor and its receptor, vascular endothelial growth factor receptor-1: novel targets for stimulation of ischemic tissue revascularization and inhibition of angiogenic and inflammatory disorders. J. Thromb. Haemost. 2003, 1:1356-1370.
29. Luttun A., Tjwa M., Carmeliet P. Placental growth factor (PlGF) and its receptor Flt-1 (VEGFR-1): novel therapeutic targets for angiogenic disorders. Ann. N. Y. Acad. Sci. 2002, 979:80-93.
30. Xu L., Jain R.K. Down-regulation of placenta growth factor by promoter hypermethylation in human lung and colon carcinoma. Mol. Cancer Res. 2007, 5:873-880.
31. Bullock A.J., Zhang L., O'Neill A.M., Percy A., Sukhatme V., Mier J.W., Atkins M.B., Bhatt R.S. Plasma angiopoietin-2 (ANG2) as an angiogenic biomarker in renal cell carcinoma (RCC). ASCO Annual Meeting, 2010 2010.
32. Tamaskar I., Dhillon J., Pili R. Resistance to angiogenesis inhibitors in renal cell carcinoma. Clin. Adv. Hematol. Oncol. 2011, 9:101-110.
33. Huang H., Lai J.Y., Do J., Liu D., Li L., Del Rosario J., Doppalapudi V.R., Pirie-Shepherd S., Levin N., Bradshaw C., Woodnutt G., Lappe R., Bhat A. Specifically targeting angiopoietin-2 inhibits angiogenesis, Tie2-expressing monocyte infiltration, and tumor growth. Clin. Cancer Res. 2011, 17:1001-1011.
34. Cuvillier O., Ader I., Bouquerel P., Brizuela L., Malavaud B., Mazerolles C., Rischmann P. Activation of sphingosine kinase-1 in cancer: implications for therapeutic targeting. Curr. Mol. Pharmacol. 2010, 3:53-65.
35. Bhatt R.S., Zhang L., Bullock A., et al. Sphingosine-1-phosphate (S1P) as a novel target in renal cancer (RCC). Proceedings of the 101st annual meeting of the American association for, cancer research 2010.
36. Bender C., Ullrich A. PRKX, TTBK2 and RSK4 expression causes sunitinib resistance in kidney carcinoma- and melanoma-cell lines. Int. J. Cancer 2012, 131:E45-E55.
37. Zhu S., Wurdak H., Wang Y., Galkin A., Tao H., Li J., Lyssiotis C.A., Yan F., Tu B.P., Miraglia L., Walker J., Sun F., Orth A., Schultz P.G., Wu X. A genomic screen identifies TYRO3 as a MITF regulator in melanoma. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17025-17030.
38. Argani P., Antonescu C.R., Illei P.B., Lui M.Y., Timmons C.F., Newbury R., Reuter V.E., Garvin A.J., Perez-Atayde A.R., Fletcher J.A., Beckwith J.B., Bridge J.A., Ladanyi M. Primary renal neoplasms with the ASPL-TFE3 gene fusion of alveolar soft part sarcoma: a distinctive tumor entity previously included among renal cell carcinomas of children and adolescents. Am. J. Pathol. 2001, 159:179-192.
39. Davis I.J., Hsi B.L., Arroyo J.D., Vargas S.O., Yeh Y.A., Motyckova G., Valencia P., Perez-Atayde A.R., Argani P., Ladanyi M., Fletcher J.A., Fisher D.E. Cloning of an alpha-TFEB fusion in renal tumors harboring the t(6;11)(p21;q13) chromosome translocation. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6051-6056.
40. Kuiper D.R., Hoekstra H.J., Veth R.P., Wobbes T. The management of clear cell sarcoma. Eur. J. Surg. Oncol. 2003, 29:568-570.
41. Thakur A., Rahman K.W., Wu J., Bollig A., Biliran H., Lin X., Nassar H., Grignon D.J., Sarkar F.H., Liao J.D. Aberrant expression of X-linked genes RbAp46, Rsk4, and Cldn2 in breast cancer. Mol. Cancer Res. 2007, 5:171-181.
42. Bonni A., Brunet A., West A.E., Datta S.R., Takasu M.A., Greenberg M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 1999, 286:1358-1362.
43. De Cesare D., Jacquot S., Hanauer A., Sassone-Corsi P. Rsk-2 activity is necessary for epidermal growth factor-induced phosphorylation of CREB protein and transcription of c-fos gene. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:12202-12207.
44. Ginty D.D., Bonni A., Greenberg M.E. Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 1994, 77:713-725.
45. Arao T., Matsumoto K., Furuta K., Kudo K., Kaneda H., Nagai T., Sakai K., Fujita Y., Tamura D., Aomatsu K., Koizumi F., Nishio K. Acquired drug resistance to vascular endothelial growth factor receptor 2 tyrosine kinase inhibitor in human vascular endothelial cells. Anticancer Res. 2011, 31:2787-2796.
46. Deprimo S.E., Bello C.L., Smeraglia J., Shalinsky D.R., Freddo J., Baum C.M., Rini B.I., Michaelson D., Motzer R.J., Spinella D.G. Soluble protein biomarkers of pharmacodynamic activity of the multi-targeted kinase inhibitor SU11248 in patients with metastatic renal cell cancer. Proceedings in American Association of Cancer Research 2005.
47. Deprimo S.E., Bello C.L., Smeraglia J., Baum C.M., Spinella D., Rini B.I., Michaelson M.D., Motzer R.J. Circulating protein biomarkers of pharmacodynamic activity of sunitinib in patients with metastatic renal cell carcinoma: modulation of VEGF and VEGF-related proteins. J. Transl. Med. 2007, 5:32.
48. Leroy X., Aubert S., Zini L., Franquet H., Kervoaze G., Villers A., Delehedde M., Copin M.C., Lassalle P. Vascular endocan (ESM-1) is markedly overexpressed in clear cell renal cell carcinoma. Histopathology 2010, 56:180-187.
49. Xu L., Duda D.G., di Tomaso E., Ancukiewicz M., Chung D.C., Lauwers G.Y., Samuel R., Shellito P., Czito B.G., Lin P.C., Poleski M., Bentley R., Clark J.W., Willett C.G., Jain R.K. Direct evidence that bevacizumab, an anti-VEGF antibody, up-regulates SDF1alpha, CXCR4, CXCL6, and neuropilin 1 in tumors from patients with rectal cancer. Cancer Res. 2009, 69:7905-7910.
50. Jain R.K., Booth M.F. What brings pericytes to tumor vessels?. J. Clin. Invest. 2003, 112:1134-1136.
51. Kamba T., McDonald D.M. Mechanisms of adverse effects of anti-VEGF therapy for cancer. Br. J. Cancer 2007, 96:1788-1795.
52. Mancuso M.R., Davis R., Norberg S.M., O'Brien S., Sennino B., Nakahara T., Yao V.J., Inai T., Brooks P., Freimark B., Shalinsky D.R., Hu-Lowe D.D., McDonald D.M. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J. Clin. Invest. 2006, 116:2610-2621.
53. Benjamin L.E., Hemo I., Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1998, 125:1591-1598.
54. Hirschi K.K., D'Amore P.A. Control of angiogenesis by the pericyte: molecular mechanisms and significance. EXS 1997, 79:419-428.
55. Orlidge A., D'Amore P.A. Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J. Cell Biol. 1987, 105:1455-1462.
56. Xian X., Hakansson J., Stahlberg A., Lindblom P., Betsholtz C., Gerhardt H., Semb H. Pericytes limit tumor cell metastasis. J. Clin. Invest. 2006, 116:642-651.
57. Pollard J.W. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 2004, 4:71-78.
58. Hattori K., Heissig B., Wu Y., Dias S., Tejada R., Ferris B., Hicklin D.J., Zhu Z., Bohlen P., Witte L., Hendrikx J., Hackett N.R., Crystal R.G., Moore M.A., Werb Z., Lyden D., Rafii S. Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone-marrow microenvironment. Nat. Med. 2002, 8:841-849.
59. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., Zhu Z., Hicklin D., Wu Y., Port J.L., Altorki N., Port E.R., Ruggero D., Shmelkov S.V., Jensen K.K., Rafii S., Lyden D. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
60. De Palma M., Venneri M.A., Galli R., Sergi Sergi L., Politi L.S., Sampaolesi M., Naldini L. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005, 8:211-226.
61. Bunt S.K., Sinha P., Clements V.K., Leips J., Ostrand-Rosenberg S. Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 2006, 176:284-290.
62. Yang L., DeBusk L.M., Fukuda K., Fingleton B., Green-Jarvis B., Shyr Y., Matrisian L.M., Carbone D.P., Lin P.C. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004, 6:409-421.
63. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z., Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13:206-220.
64. Grunewald M., Avraham I., Dor Y., Bachar-Lustig E., Itin A., Jung S., Chimenti S., Landsman L., Abramovitch R., Keshet E. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 2006, 124:175-189.
65. Finke J., Ko J., Rini B., Rayman P., Ireland J., Cohen P. MDSC as a mechanism of tumor escape from sunitinib mediated anti-angiogenic therapy. Int. Immunopharmacol. 2011, 11:856-861.
66. Xin H., Zhang C., Herrmann A., Du Y., Figlin R., Yu H. Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res. 2009, 69:2506-2513.
67. Ceradini D.J., Kulkarni A.R., Callaghan M.J., Tepper O.M., Bastidas N., Kleinman M.E., Capla J.M., Galiano R.D., Levine J.P., Gurtner G.C. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 2004, 10:858-864.
68. Petit I., Jin D., Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol. 2007, 28:299-307.
69. Aghi M., Cohen K.S., Klein R.J., Scadden D.T., Chiocca E.A. Tumor stromal-derived factor-1 recruits vascular progenitors to mitotic neovasculature, where microenvironment influences their differentiated phenotypes. Cancer Res. 2006, 66:9054-9064.
70. Farace F., Gross-Goupil M., Tournay E., Taylor M., Vimond N., Jacques N., Billiot F., Mauguen A., Hill C., Escudier B. Levels of circulating CD45(dim)CD34(+)VEGFR2(+) progenitor cells correlate with outcome in metastatic renal cell carcinoma patients treated with tyrosine kinase inhibitors. Br. J. Cancer 2011, 104:1144-1150.
71. Shaked Y., Ciarrocchi A., Franco M., Lee C.R., Man S., Cheung A.M., Hicklin D.J., Chaplin D., Foster F.S., Benezra R., Kerbel R.S. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 2006, 313:1785-1787.
72. Blouw B., Song H., Tihan T., Bosze J., Ferrara N., Gerber H.P., Johnson R.S., Bergers G. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell 2003, 4:133-146.
73. Rubenstein J.L., Kim J., Ozawa T., Zhang M., Westphal M., Deen D.F., Shuman M.A. Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia 2000, 2:306-314.
74. Hammers H.J., Verheul H.M., Salumbides B., Sharma R., Rudek M., Jaspers J., Shah P., Ellis L., Shen L., Paesante S., Dykema K., Furge K., Teh B.T., Netto G., Pili R. Reversible epithelial to mesenchymal transition and acquired resistance to sunitinib in patients with renal cell carcinoma: evidence from a xenograft study. Mol. Cancer Ther. 2010, 9:1525-1535.
75. Fu C., Gerber S., Van Den Berg S., Steenwinkel F., Kant H., Moriarty W., Keizman D., Marchionni L., Carducci M., Netto G., Kachhap S., Hammers H. Abstract 1913: epithelial mesenchymal transition: a mechanism of resistance to VEGF pathway inhibition in genitourinary cancers. Cancer Research 2012, vol. 72.
76. Sarkadi B., Homolya L., Szakacs G., Varadi A. Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol. Rev. 2006, 86:1179-1236.
77. Brendel C., Scharenberg C., Dohse M., Robey R.W., Bates S.E., Shukla S., Ambudkar S.V., Wang Y., Wennemuth G., Burchert A., Boudriot U., Neubauer A. Imatinib mesylate and nilotinib (AMN107) exhibit high-affinity interaction with ABCG2 on primitive hematopoietic stem cells. Leukemia 2007, 21:1267-1275.
78. Brozik A., Hegedus C., Erdei Z., Hegedus T., Ozvegy-Laczka C., Szakacs G., Sarkadi B. Tyrosine kinase inhibitors as modulators of ATP binding cassette multidrug transporters: substrates, chemosensitizers or inducers of acquired multidrug resistance?. Expert. Opin. Drug Metab. Toxicol. 2011, 7:623-642.
79. Burger H., van Tol H., Brok M., Wiemer E.A., de Bruijn E.A., Guetens G., de Boeck G., Sparreboom A., Verweij J., Nooter K. Chronic imatinib mesylate exposure leads to reduced intracellular drug accumulation by induction of the ABCG2 (BCRP) and ABCB1 (MDR1) drug transport pumps. Cancer Biol. Ther. 2005, 4:747-752.
80. Leggas M., Panetta J.C., Zhuang Y., Schuetz J.D., Johnston B., Bai F., Sorrentino B., Zhou S., Houghton P.J., Stewart C.F. Gefitinib modulates the function of multiple ATP-binding cassette transporters in vivo. Cancer Res. 2006, 66:4802-4807.
81. Shi Z., Peng X.X., Kim I.W., Shukla S., Si Q.S., Robey R.W., Bates S.E., Shen T., Ashby C.R., Fu L.W., Ambudkar S.V., Chen Z.S. Erlotinib (Tarceva, OSI-774) antagonizes ATP-binding cassette subfamily B member 1 and ATP-binding cassette subfamily G member 2-mediated drug resistance. Cancer Res. 2007, 67:11012-11020.
82. Shukla S., Robey R.W., Bates S.E., Ambudkar S.V. Sunitinib (Sutent, SU11248), a small-molecule receptor tyrosine kinase inhibitor, blocks function of the ATP-binding cassette (ABC) transporters P-glycoprotein (ABCB1) and ABCG2. Drug Metab. Dispos. 2009, 37:359-365.
83. Dai C.L., Liang Y.J., Wang Y.S., Tiwari A.K., Yan Y.Y., Wang F., Chen Z.S., Tong X.Z., Fu L.W. Sensitization of ABCG2-overexpressing cells to conventional chemotherapeutic agent by sunitinib was associated with inhibiting the function of ABCG2. Cancer Lett. 2009, 279:74-83.
84. Kawahara H., Noguchi K., Katayama K., Mitsuhashi J., Sugimoto Y. Pharmacological interaction with sunitinib is abolished by a germ-line mutation (1291T>C) of BCRP/ABCG2 gene. Cancer Sci. 2010, 101:1493-1500.
85. Singhal S.S., Sehrawat A., Sahu M., Singhal P., Vatsyayan R., Rao Lelsani P.C., Yadav S., Awasthi S. Rlip76 transports sunitinib and sorafenib and mediates drug resistance in kidney cancer. Int. J. Cancer 2010, 126:1327-1338.
86. Ostrand-Rosenberg S., Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 2009, 182:4499-4506.
87. Shojaei F., Wu X., Malik A.K., Zhong C., Baldwin M.E., Schanz S., Fuh G., Gerber H.P., Ferrara N. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat. Biotechnol. 2007, 25:911-920.
88. Gabrilovich D. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat. Rev. Immunol. 2004, 4:941-952.
89. Gabrilovich D.I., Chen H.L., Girgis K.R., Cunningham H.T., Meny G.M., Nadaf S., Kavanaugh D., Carbone D.P. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 1996, 2:1096-1103.
90. Marigo I., Dolcetti L., Serafini P., Zanovello P., Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev. 2008, 222:162-179.
91. Talmadge J.E. Pathways mediating the expansion and immunosuppressive activity of myeloid-derived suppressor cells and their relevance to cancer therapy. Clin. Cancer Res. 2007, 13:5243-5248.
92. Kujawski M., Kortylewski M., Lee H., Herrmann A., Kay H., Yu H. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J. Clin. Invest. 2008, 118:3367-3377.
93. Ko J.S., Zea A.H., Rini B.I., Ireland J.L., Elson P., Cohen P., Golshayan A., Rayman P.A., Wood L., Garcia J., Dreicer R., Bukowski R., Finke J.H. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin. Cancer Res. 2009, 15:2148-2157.
94. Nishioka Y., Aono Y., Sone S. Role of tyrosine kinase inhibitors in tumor immunology. Immunotherapy 2011, 3:107-116.
95. Topalian S.L., Brahmer J.R., Hodi F.S., McDermott D.F., Smith D.C., Gettinger S.N., Taube J.M., Drake C.G., Pardoll D.M., Antonia S., Spigel D.R., Atkins M.B., Lawrence D.P., McDonald D., Jure-Kunkel M., Korman A., Kollia G., Topalian S.L., Brahmer J.R., Hodi F.S., McDermott D.F., Smith D.C., Gettinger S.N., Taube J.M., Drake C.G., Pardoll D.M., Antonia S., Spigel D.R., Atkins M.B., Lawrence D.P., McDonald D., Jure-Kunkel M., Korman A., Kollia G. Anti-PD-1 (BMS-936558, MDX-1106) in patients with advanced solid tumors: clinical activity, safety, and a potential biomarker for response. ASCO Annual Meeting 2012 2012.
96. Avigan D. PD-1 Alone or With Dendritic Cell/Renal Cell Carcinoma Fusion Cell Vaccine [ClinicalTrials.gov Identifier: NCT01441765]. Beth Israel Deaconess Medical Center Dana-Farber Cancer Institute 2012.
97. Kren L., Valkovsky I., Dolezel J., Capak I., Pacik D., Poprach A., Lakomy R., Redova M., Fabian P., Krenova Z., Slaby O. HLA-G and HLA-E specific mRNAs connote opposite prognostic significance in renal cell carcinoma. Diagn. Pathol. 2012, 7:58.
98. Amiot L., Ferrone S., Grosse-Wilde H., Seliger B. Biology of HLA-G in cancer: a candidate molecule for therapeutic intervention?. Cell. Mol. Life Sci. 2011, 68:417-431.
99. Rajandram R., Bennett N.C., Morais C., Johnson D.W., Gobe G.C. Renal cell carcinoma: resistance to therapy, role of apoptosis, and the prognostic and therapeutic target potential of TRAF proteins. Med. Hypotheses 2012, 78:330-336.
100. Ruddle N.H. Workshop summary: roles of the TNF family in normal development and cancer. Adv. Exp. Med. Biol. 2011, 691:3-4.
101. Voelkel-Johnson C. TRAIL-mediated signaling in prostate, bladder and renal cancer. Nat. Rev. Urol. 2011, 8:417-427.
102. Yang E.S., Woo S.M., Choi K.S., Kwon T.K. Acrolein sensitizes human renal cancer Caki cells to TRAIL-induced apoptosis via ROS-mediated up-regulation of death receptor-5 (DR5) and down-regulation of Bcl-2. Exp. Cell Res. 2011, 317:2592-2601.
103. Brooks A.D., Jacobsen K.M., Li W., Shanker A., Sayers T.J. Bortezomib sensitizes human renal cell carcinomas to TRAIL apoptosis through increased activation of caspase-8 in the death-inducing signaling complex. Mol. Cancer Res. 2010, 8:729-738.
104. Gobe G., Rubin M., Williams G., Sawczuk I., Buttyan R. Apoptosis and expression of Bcl-2, Bcl-XL, and Bax in renal cell carcinomas. Cancer Invest. 2002, 20:324-332.
105. Ramp U., Dejosez M., Mahotka C., Czarnotta B., Kalinski T., Wenzel M., Lorenz I., Muller M., Krammer P., Gabbert H.E., Gerharz C.D. Deficient activation of CD95 (APO-1/Fas)-mediated apoptosis: a potential factor of multidrug resistance in human renal cell carcinoma. Br. J. Cancer 2000, 82:1851-1859.
106. Owen-Schaub L.B., Zhang W., Cusack J.C., Angelo L.S., Santee S.M., Fujiwara T., Roth J.A., Deisseroth A.B., Zhang W.W., Kruzel E., et al. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol. Cell. Biol. 1995, 15:3032-3040.
107. Tsao C.C., Corn P.G. MDM-2 antagonists induce p53-dependent cell cycle arrest but not cell death in renal cancer cell lines. Cancer Biol. Ther. 2011, 10:1315-1325.
108. Cash T.P., Gruber J.J., Hartman T.R., Henske E.P., Simon M.C. Loss of the Birt-Hogg-Dube tumor suppressor results in apoptotic resistance due to aberrant TGFbeta-mediated transcription. Oncogene 2011, 30:2534-2546.
109. Gerlinger M., Rowan A.J., Horswell S., Larkin J., Endesfelder D., Gronroos E., Martinez P., Matthews N., Stewart A., Tarpey P., Varela I., Phillimore B., Begum S., McDonald N.Q., Butler A., Jones D., Raine K., Latimer C., Santos C.R., Nohadani M., Eklund A.C., Spencer-Dene B., Clark G., Pickering L., Stamp G., Gore M., Szallasi Z., Downward J., Futreal P.A., Swanton C. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 2012, 366:883-892.
110. Kaelin W.G. The von Hippel-Lindau tumor suppressor gene and kidney cancer. Clin. Cancer Res. 2004, 10:6290S-6295S.
111. Pili R., Lodge M., Verheul H., Mashtare T., Wahl R.L., Martin J.E., Espinoza-Delgado I., Liu G., Carducci M.A. Combination of the histone deacetylase inhibitor vorinostat with bevacizumab in pretreated patients with renal cell carcinoma: safety, efficacy, and pharmacodynamic results. ASCO 2010 Genitourinary Cancers Symposium 2010.
112. Qian D.Z., Wang X., Kachhap S.K., Kato Y., Wei Y., Zhang L., Atadja P., Pili R. The histone deacetylase inhibitor NVP-LAQ824 inhibits angiogenesis and has a greater antitumor effect in combination with the vascular endothelial growth factor receptor tyrosine kinase inhibitor PTK787/ZK222584. Cancer Res. 2004, 64:6626-6634.
113. Wang X.F., Qian D.Z., Ren M., Kato Y., Wei Y., Zhang L., Fansler Z., Clark D., Nakanishi O., Pili R. Epigenetic modulation of retinoic acid receptor beta2 by the histone deacetylase inhibitor MS-275 in human renal cell carcinoma. Clin. Cancer Res. 2005, 11:3535-3542.
114. Duignan I.J., Corcoran E., Pennello A., Plym M.J., Amatulli M., Claros N., Iacolina M., Youssoufian H., Witte L., Samakoglu S., Schwartz J., Surguladze D., Tonra J.R. Pleiotropic stromal effects of vascular endothelial growth factor receptor 2 antibody therapy in renal cell carcinoma models. Neoplasia 2011, 13:49-59.
115. Rini B.I., Szczylik C., Tannir N.M., Koralewski P., Tomczak P., Deptala A., Kracht K., Sun Y., Puhlmann M., Escudier B. AMG 386 in combination with sorafenib in patients (pts) with metastatic renal cell cancer (mRCC): a randomized, double-blind, placebo-controlled, phase II study, in: American Society of Clinical Oncology (ASCO) vol. J. Clin. Oncol. 2011, 29(Suppl. 7; abstr 309). (2011).
116. Zhong H., Bowen J.P. Recent advances in small molecule inhibitors of VEGFR and EGFR signaling pathways. Curr. Top. Med. Chem. 2011, 11:1571-1590.
117. Voce P., D'Agostino M., Moretti S., Sponziello M., Rhoden K., Calcinaro F., Tamburrano G., Tallini G., Puxeddu E., Filetti S., Russo D., Durante C. Sunitinib inhibits tumor vascularity and growth but does not affect Akt and ERK phosphorylation in xenograft tumors. Oncol. Rep. 2011, 26:1075-1080.
118. Makhov P.B., Golovine K., Kutikov A., Teper E., Canter D.J., Simhan J., Uzzo R.G., Kolenko V.M. Modulation of Akt/mTOR signaling overcomes sunitinib resistance in renal and prostate cancer cells. Mol. Cancer Ther. 2012, 11:1510-1517.
119. Negrier S., Gravis G., Perol D., Chevreau C., Delva R., Bay J.O., Blanc E., Ferlay C., Geoffrois L., Rolland F., Legouffe E., Sevin E., Laguerre B., Escudier B. Temsirolimus and bevacizumab, or sunitinib, or interferon alfa and bevacizumab for patients with advanced renal cell carcinoma (TORAVA): a randomised phase 2 trial. Lancet Oncol. 2011, 12:673-680.
120. Rini B.I., Garcia J.A., Cooney M.M., Elson P., Tyler A., Beatty K., Bokar J., Ivy P., Chen H.X., Dowlati A., Dreicer R. Toxicity of sunitinib plus bevacizumab in renal cell carcinoma. J. Clin. Oncol. 2010, 28:e284-e285. (author reply e286-287)0.
121. Gotink K.J., Broxterman H.J., de Haas R.R., Rovithi M.R., Pili R., Verheul H.M.W. Cross-resistance and sensitivity of sunitinib resistant tumor cells. Cancer Research 2012, vol. 72.
122. Yuasa T., Fujii Y., Takahasji S., Fukui I., Yonese J. Molecular targeted therapies for patients with metastatic renal cell cancer. Transl. Med. 2012, S2(003).
123. Serova M., Santos C.D., Tijeras-Raballand A., Riveiro M.E., de Gramont A., Faivre S., Raymond E. Antitumor effects of everolimus, sorafenib, and axitinib in human renal cells carcinoma xenografts resistant to first line treatment by sunitinib. Cancer Research 2012, vol. 72.
124. Serova M., Tijeras-Raballand A., Riveiro M.E., de Gramont A., Faivre S., Raymond E. Comparative analysis of 3 rapalogues, everolimus, temsirolimus and sirolimus, in hepatocarcinoma and renal cancer models resistant to VEGFR inhibitors. Cancer Research 2012, vol. 72.
125. Bhasin M., Gu X., Kung A., Libermann T.A. Identification of new drugs for treatment of renal cell cancer using genomics and the Connectivity Map Database in: Proceedings: Association of Cancer Research 103rd Annual Meeting 2012. Cancer Res. 2012, vol. 72.
126. An Z., Jiang P., Wang X., Moossa A.R., Hoffman R.M. Development of a high metastatic orthotopic model of human renal cell carcinoma in nude mice: benefits of fragment implantation compared to cell-suspension injection. Clin. Exp. Metastasis 1999, 17:265-270.
127. Karam J.A., Zhang X.Y., Tamboli P., Margulis V., Wang H., Abel E.J., Culp S.H., Wood C.G. Development and characterization of clinically relevant tumor models from patients with renal cell carcinoma. Eur. Urol. 2011, 59:619-628.
128. Murphy E.A., Shields D.J., Stoletov K., Dneprovskaia E., McElroy M., Greenberg J.I., Lindquist J., Acevedo L.M., Anand S., Majeti B.K., Tsigelny I., Saldanha A., Walsh B., Hoffman R.M., Bouvet M., Klemke R.L., Vogt P.K., Arnold L., Wrasidlo W., Cheresh D.A. Disruption of angiogenesis and tumor growth with an orally active drug that stabilizes the inactive state of PDGFRbeta/B-RAF. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4299-4304.
129. Fiebig H.H., Maier A., Burger A.M. Clonogenic assay with established human tumour xenografts: correlation of in vitro to in vivo activity as a basis for anticancer drug discovery. Eur. J. Cancer 2004, 40:802-820.
130. Marangoni E., Vincent-Salomon A., Auger N., Degeorges A., Assayag F., de Cremoux P., de Plater L., Guyader C., De Pinieux G., Judde J.G., Rebucci M., Tran-Perennou C., Sastre-Garau X., Sigal-Zafrani B., Delattre O., Dieras V., Poupon M.F. A new model of patient tumor-derived breast cancer xenografts for preclinical assays. Clin. Cancer Res. 2007, 13:3989-3998.
131. Nemati F., Daniel C., Arvelo F., Legrier M.E., Froget B., Livartowski A., Assayag F., Bourgeois Y., Poupon M.F., Decaudin D. Clinical relevance of human cancer xenografts as a tool for preclinical assessment: example of in-vivo evaluation of topotecan-based chemotherapy in a panel of human small-cell lung cancer xenografts. Anticancer Drugs 2010, 21:25-32.