Predictive and prognostic biomarkers of targeted agents and modern immunotherapy in renal cell carcinoma

ESMO Open

Volumn 1, Issue 3, 2016, Pages

  Rodriguez Vida, Alejo ^a   Strijbos, Michiel ^b   Hutson, Thomas ^c  

^a HOSPITAL DEL MAR   (Spain)

^b Department of Medical Oncology ^*  (Belgium)

^c BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Biomarker; Immunotherapy; Programmed cell death 1; Renal cell carcinoma; Tyrosine kinase inhibitor

Indexed keywords

EID: 85013757590     PISSN: None     EISSN: 20597029     Source Type: Journal    
DOI: 10.1136/esmoopen-2015-000013     Document Type: Review

References (77)

1. Sternberg CN, Davis ID, Mardiak J, et al. Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial. J Clin Oncol 2010;28:1061-8.
2. Motzer RJ, Hutson TE, Tomczak P, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007;356:115-24.
3. Hudes G, Carducci M, Tomczak P, et al. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 2007;356:2271-81.
4. Rini BI, Escudier B, Tomczak P, et al. Comparative effectiveness of axitinib versus sorafenib in advanced renal cell carcinoma (AXIS): A randomised phase 3 trial. Lancet 2011;378:1931-9.
5. Motzer RJ, Escudier B, Oudard S, et al. Efficacy of everolimus in advanced renal cell carcinoma: A double-blind, randomised, placebo-controlled phase III trial. Lancet 2008;372:449-56.
6. Kaelin WG. The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. Clin Cancer Res 2007;13(2 Pt 2):680s-4s.
7. Kim BY, Kim H, Cho EJ, et al. Nur77 upregulates HIF-alpha by inhibiting pVHL-mediated degradation. Exp Mol Med 2008;40:71-83.
8. Xu K, Liu P, Wei W. mTOR signaling in tumorigenesis. Biochim Biophys Acta 2014;1846:638-54.
9. Hoeben A, Landuyt B, Highley MS, et al. Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 2004;56:549-80.
10. Yang Y, Cong H, Han C, et al. 12-Deoxyphorbol 13-palmitate inhibits the expression of VEGF and HIF-1 in MCF-7 cells by blocking the PI3K/Akt/mTOR signaling pathway. Oncol Rep 2015;34:1755-60.
11. Rini BI, Halabi S, Rosenberg JE, et al. 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 2010;28:2137-43.
12. Ljungberg B, Bensalah K, Canfield S, et al. EAU guidelines on renal cell carcinoma: 2014 update. Eur Urol 2015;67:913-24.
13. National Comprehensive Cancer Network Clinical Practice Guidelines in Oncology (NCCN Guidelines®). Kidney Cancer (Version 2. 2016). http://www. nccn. org/professionals/physician-gls/ pdf/kidney. pdf (accessed 5 Dec 2015).
14. Heng DY, Xie W, Regan MM, et al. Prognostic factors for overall survival in patients with metastatic renal cell carcinoma treated with vascular endothelial growth factor-targeted agents: results from a large, multicenter study. J Clin Oncol 2009;27:5794-9.
15. Motzer RJ, Mazumdar M, Bacik J, et al. Survival and prognostic stratification of 670 patients with advanced renal cell carcinoma. J Clin Oncol 1999;17:2530-40.
16. Heng DY, Xie W, Regan MM, et al. External validation and comparison with other models of the International Metastatic Renal-Cell Carcinoma Database Consortium prognostic model: A population-based study. Lancet Oncol 2013;14:141-8.
17. Bono P, Elfving H, Utriainen T, et al. Hypertension and clinical benefit of bevacizumab in the treatment of advanced renal cell carcinoma. Ann Oncol 2009;20:393-4.
18. Rini BI, Cohen DP, Lu DR, et al. Hypertension as a biomarker of efficacy in patients with metastatic renal cell carcinoma treated with sunitinib. J Natl Cancer Inst 2011;103:763-73.
19. Gunnarsson O, Pfanzelter NR, Cohen RB, et al. Evaluating the safety and efficacy of axitinib in the treatment of advanced renal cell carcinoma. Cancer Manag Res 2015;7:65-73.
20. Rixe O, Dutcher J, Motzer R, et al. Diastolic blood pressure (dBP) and pharmacokinetics (PK) as predictors of axitinib efficacy in metastatic renal cell cancer (mRCC). J Clin Oncol 2009;25(Suppl). (Abstract 5045).
21. Nosov DA, Esteves B, Lipatov ON, et al. Antitumor activity and safety of tivozanib (AV-951) in a phase II randomized discontinuation trial in patients with renal cell carcinoma. J Clin Oncol 2012;30:1678-85.
22. Nearchou A, Valachis A, Lind P, et al. Acquired hypothyroidism as a predictive marker of outcome in patients with metastatic renal cellcarcinoma treated with tyrosine kinase inhibitors: A literature-based meta-analysis. Clin Genitourin Cancer 2015;13:280-6.
23. Donskov F, Michaelson MD, Puzanov I, et al. Sunitinib-associated hypertension and neutropenia as efficacy biomarkers in metastatic renal cell carcinoma patients. Br J Cancer 2015;113:1571-80.
24. Escudier B, Eisen T, Stadler WM, et al. Sorafenib for treatment of renal cell carcinoma: final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial. J Clin Oncol 2009;27:3312-18.
25. Zurita AJ, Jonasch E, Wang X, et al. A cytokine and angiogenic factor (CAF) analysis in plasma for selection of sorafenib therapy in patients with metastatic renal cell carcinoma. Ann Oncol 2012;23:46-52.
26. Tran HT, Liu Y, Zurita AJ, et al. 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 2012;13:827-37.
27. Lambrechts D, Claes B, Delmar P, et al. VEGF pathway genetic variants as biomarkers of treatment outcome with bevacizumab: An analysis of data from the AViTA and AVOREN randomised trials. Lancet Oncol 2012;13:724-33.
28. Xu CF, Bing NX, Ball HA, et al. Pazopanib efficacy in renal cell carcinoma: evidence for predictive genetic markers in angiogenesis-related and exposure-related genes. J Clin Oncol 2011;29:2557-64.
29. Kim JJ, Vaziri SA, Rini BI, et al. Association of VEGF and VEGFR2 single nucleotide polymorphisms with hypertension and clinical outcome in metastatic clear cell renal cell carcinoma patients treated with sunitinib. Cancer 2012;118:1946-54.
30. Motzer RJ, Hutson TE, Hudes GR, et al. Investigation of novel circulating proteins, germ line single-nucleotide polymorphisms, and molecular tumor markers as potential efficacy biomarkers of first-line sunitinib therapy for advanced renal cell carcinoma. Cancer Chemother Pharmacol 2014;74:739-50.
31. Escudier B, Rini BI, Motzer RJ, et al. Genotype correlations with blood pressure and efficacy from a randomized phase III trial of second-line axitinib versus sorafenib in metastatic renal cell carcinoma. Clin Genitourin Cancer 2015;13:328-37. e3.
32. Choueiri TK, Vaziri SA, Jaeger E, et al. von Hippel-Lindau gene status and response to vascular endothelial growth factor targeted therapy for metastatic clear cell renal cell carcinoma. J Urol 2008;180:860-5; discussion 5-6.
33. Choueiri TK, Fay AP, Gagnon R, et al. The role of aberrant VHL/HIF pathway elements in predicting clinical outcome to pazopanib therapy in patients with metastatic clear-cell renal cell carcinoma. Clin Cancer Res 2013;19:5218-26.
34. Peña C, Lathia C, Shan M, et al. Biomarkers predicting outcome in patients with advanced renal cell carcinoma: results from sorafenib phase III Treatment Approaches in Renal Cancer Global Evaluation Trial. Clin Cancer Res 2010;16:4853-63.
35. Schwarzenbach H, Hoon DS, Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer 2011;11:426-37.
36. Feng G, Ye X, Fang F, et al. Quantification of plasma cell-free DNA in predicting therapeutic efficacy of sorafenib on metastatic clear cell renal cell carcinoma. Dis Markers 2013;34:105-11.
37. Semenza GL. HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations. J Clin Invest 2013;123:3664-71.
38. Agarwala SS, Case S. Everolimus (RAD001) in the treatment of advanced renal cell carcinoma: A review. Oncologist 2010;15:236-45.
39. Hudson CC, Liu M, Chiang GG, et al. Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol Cell Biol 2002;22:7004-14.
40. White DA, Camus P, Endo M, et al. Noninfectious pneumonitis after everolimus therapy for advanced renal cell carcinoma. Am J Respir Crit Care Med 2010;182:396-403.
41. Dabydeen DA, Jagannathan JP, Ramaiya N, et al. Pneumonitis associated with mTOR inhibitors therapy in patients with metastatic renal cell carcinoma: incidence, radiographic findings and correlation with clinical outcome. Eur J Cancer 2012;48:1519-24.
42. Atkinson BJ, Cauley DH, Ng C, et al. Mammalian target of rapamycin (mTOR) inhibitor-associated non-infectious pneumonitis in patients with renal cell cancer: predictors, management, and outcomes. BJU Int 2014;113:376-82.
43. Lee CK, Marschner IC, Simes RJ, et al. Increase in cholesterol predicts survival advantage in renal cell carcinoma patients treated with temsirolimus. Clin Cancer Res 2012;18:3188-96.
44. Armstrong AJ, George DJ, Halabi S. Serum lactate dehydrogenase predicts for overall survival benefit in patients with metastatic renal cell carcinoma treated with inhibition of mammalian target of rapamycin. J Clin Oncol 2012;30:3402-7.
45. Disis ML. Immunologic biomarkers as correlates of clinical response to cancer immunotherapy. Cancer Immunol Immunother 2011;60:433-42.
46. Montero AJ, Diaz-Montero CM, Millikan RE, et al. Cytokines and angiogenic factors in patients with metastatic renal cell carcinoma treated with interferon-alpha: Association of pretreatment serum levels with survival. Ann Oncol 2009;20:1682-7.
47. McDermott DF, Ghebremichael MS, Signoretti S, et al. The high-dose aldesleukin (HD IL-2) "SELECT" trial in patients with metastatic renal cell carcinoma (mRCC). J Clin Oncol 2010;28:15s, (suppl; abstr 4514).
48. Motzer RJ, Bacik J, Murphy BA, et al. Interferon-alfa as a comparative treatment for clinical trials of new therapies against advanced renal cell carcinoma. J Clin Oncol 2002;20: 289-96.
49. Négrier S, Escudier B, Gomez F, et al. Prognostic factors of survival and rapid progression in 782 patients with metastatic renal carcinomas treated by cytokines: A report from the Groupe Français d'Immunothérapie. Ann Oncol 2002;13:1460-8.
50. Mekhail TM, Abou-Jawde RM, Boumerhi G, et al. Validation and extension of the Memorial Sloan-Kettering prognostic factors model for survival in patients with previously untreated metastatic renal cell carcinoma. J Clin Oncol 2005;23:832-41.
51. Patil S, Figlin RA, Hutson TE, et al. Prognostic factors for progression-free and overall survival with sunitinib targeted therapy and with cytokine as first-line therapy in patients with metastatic renal cell carcinoma. Ann Oncol 2011;22:295-300.
52. Atzpodien J, Royston P, Wandert T, et al. DGCIN-German Cooperative Renal Carcinoma Chemo-Immunotherapy Trials Group. Metastatic renal carcinoma comprehensive prognostic system. Br J Cancer 2003;88:348-53.
53. Thompson RH, Dong H, Kwon ED. Implications of B7-H1 expression in clear cell carcinoma of the kidney for prognostication and therapy. Clin Cancer Res 2007;13(2 Pt 2):709s-15s.
54. Jilaveanu LB, Shuch B, Zito CR, et al. PD-L1 expression in clear cell renal cell carcinoma: An analysis of nephrectomy and sites of metastases. J Cancer 2014;5:166-72.
55. Callea M, Albiges L, Gupta M, et al. Differential expression of PD-L1 between primary and metastatic sites in clear cell Renal Cell Carcinoma. Cancer Immunol Res 2015;3:1158-64.
56. Thompson RH, Kuntz SM, Leibovich BC, et al. Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res 2006;66:3381-5.
57. Kang MJ, Kim KM, Bae JS, et al. Tumor-infiltrating PD1-positive lymphocytes and FoxP3-positive regulatory T cells predict distant metastatic relapse and survival of clear cell renal cell carcinoma. Transl Oncol 2013;6:282-9.
58. Choueiri TK, Figueroa DJ, Fay AP, et al. Correlation of PD-L1 tumor expression and treatment outcomes in patients with renal cell carcinoma receiving sunitinib or pazopanib: results from COMPARZ, a randomized controlled trial. Clin Cancer Res 2015;21:1071-7.
59. Brahmer JR, Drake CG, Wollner I, et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol 2010;28:3167-75.
60. Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
61. Taube JM, Klein A, Brahmer JR, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014;20:5064-74.
62. Choueiri TK, Fishman MN, Escudier BJ, et al. Immunomodulatory activity of nivolumab in previously treated and untreated metastatic renal cell carcinoma (mRCC): biomarker-based results from a randomized clinical trial. J Clin Oncol 2014;32:5s, (suppl; abstr 5012).
63. Choueiri TK, Fishman MN, Escudier B, et al. Immunomodulatory activity of nivolumab in metastatic renal cell carcinoma (mRCC): Association of biomarkers with clinical outcomes. J Clin Oncol 2015;33 (suppl; abstr 4500).
64. Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab for metastatic renal cell carcinoma: results of a randomized phase II trial. J Clin Oncol 2015;33:1430-7.
65. Plimack ER, Hammers HJ, Rini BI, et al. Updated survival results from a randomized, dose-ranging phase II study of nivolumab (NIVO) in metastatic renal cell carcinoma (mRCC). J Clin Oncol 2015;33 (suppl; abstr 4553).
66. Motzer RJ, Escudier B, McDermott DF, et al. CheckMate 025 Investigators. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med 2015;373:1803-13.
67. Hammers H, Plimack ER, Infante JR, et al. Phase I study of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma (mRCC). Ann Oncol 2014;25 (suppl; abstr 1050O).
68. Amin A, Plimack ER, Infante JR, et al. Nivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with sunitinib or pazopanib in patients ( pts) with metastatic renal cell carcinoma (mRCC). J Clin Oncol 2014;32:5s (suppl; abstr 5010).
69. McDermott DF, Sznol M, Sosman JA, et al. Immune correlates and long term follow up of a phase Ia study of MPDL3280A, an engineered PD-L1 antibody, in patients with metastatic renal cell carcinoma (mRCC). Ann Oncol 2014;25(Suppl; abstr 809O).
70. Powderly JD, Koeppen H, Hodi FS, et al. Biomarkers and associations with the clinical activity of PD-L1 blockade in a MPDL3280A study. J Clin Oncol 2013;31 (Suppl; abstr 3001).
71. Callea M, Genega EM, Gupta M, et al. PD-L1 expression in primary clear cell renal cell carcinomas (ccRCCs) and their metastases. J Clin Oncol 2014;32:5s (Suppl 4; abstr 467).
72. Gajewski TF, Fuertes M, Spaapen R, et al. Molecular profiling to identify relevant immune resistance mechanisms in the tumor microenvironment. Curr Opin Immunol 2011;23: 286-92.
73. Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab for metastatic renal cell carcinoma (mRCC): results of a randomized, dose-ranging phase II trial. J Clin Oncol 2015;33:1430-7.
74. Beck KE, Blansfield JA, Tran KQ, et al. Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 2006;24:2283-9.
75. Yang JC, Hughes M, Kammula U, et al. Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J Immunother 2007;30:825-30.
76. Attia P, Phan GQ, Maker AV, et al. Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic T-lymphocyte antigen-4. J Clin Oncol 2005;23:6043-53.
77. Childs R, Chernoff A, Contentin N, et al. Regression of metastatic renal-cell carcinoma after nonmyeloablative allogeneic peripheralblood stem-cell transplantation. N Engl J Med 2000;343:750-8.