Metastatic clear cell renal cell carcinoma: A review of current therapies and novel immunotherapies

Critical Reviews in Oncology/Hematology

Volumn 96, Issue 3, 2015, Pages 527-533

  Thomas, Jacob S ^a   Kabbinavar, Fairooz ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Carcinoma; Dendritic cells; Immunotherapy; Programmed cell death 1 receptor; Renal cell

Indexed keywords

ADENOVIRUS VECTOR; ALANINE AMINOTRANSFERASE; ALPHA INTERFERON; AMYLASE; AXITINIB; BEVACIZUMAB; BMS 936559; CARBONATE DEHYDRATASE IX; DOVITINIB; DURVALUMAB; EVEROLIMUS; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IPILIMUMAB; NIVOLUMAB; PAZOPANIB; PLACEBO; PROGRAMMED DEATH 1 RECEPTOR; ROCAPULDENCEL T; SORAFENIB; SUNITINIB; TEMSIROLIMUS; TRIACYLGLYCEROL LIPASE; ANTINEOPLASTIC AGENT;

ALOPECIA; ANOREXIA; ASTHENIA; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; COLITIS; CYTOPENIA; DENDRITIC CELL; DIABETES MELLITUS; DIARRHEA; DISEASE FREE SURVIVAL; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; DYSPNEA; EYE INFLAMMATION; FATIGUE; FLU LIKE SYNDROME; HAIR COLOR; HAND FOOT SYNDROME; HEPATITIS; HUMAN; HYPERGLYCEMIA; HYPERLIPIDEMIA; HYPERTENSION; HYPERTRIGLYCERIDEMIA; HYPONATREMIA; HYPOTHYROIDISM; KIDNEY METASTASIS; LEUKOPENIA; MOLECULAR BIOLOGY; MOLECULARLY TARGETED THERAPY; MULTICENTER STUDY (TOPIC); MYASTHENIA GRAVIS; NAUSEA; OVERALL SURVIVAL; PAIN; PERIPHERAL EDEMA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PNEUMONIA; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEINURIA; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RASH; REVIEW; SARCOIDOSIS; STOMATITIS; SWEAT; THYROIDITIS; TREATMENT DURATION; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR VOLUME; UNSPECIFIED SIDE EFFECT; VIRAL GENE THERAPY; VITILIGO; VOMITING; ANIMAL; CARCINOMA, RENAL CELL; IMMUNOLOGY; IMMUNOTHERAPY; KIDNEY NEOPLASMS; MULTIMODALITY CANCER THERAPY; PATHOLOGY; PROGNOSIS; SECONDARY;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, RENAL CELL; COMBINED MODALITY THERAPY; HUMANS; IMMUNOTHERAPY; KIDNEY NEOPLASMS; PROGNOSIS;

EID: 84983097821     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2015.07.009     Document Type: Review

References (69)

1. Alessandrini A., De Haseth S., Fray M., et al. Dendritic cell maturation occurs through the inhibition of GSK-3β. Cell Immunol. 2011, 270(2):114-125.
2. Alvarez A. A phase II study of pazopanib (P) in patients (Pts) with localized renal cell carcinoma (RCC) to enable partial nephrectomy (PN). ASCO Meeting Abstr. 2014, 32(15S):LBA4522.
3. Amato R.J. Chemotherapy for renal cell carcinoma. Semin. Oncol. 2000, 27(2):177-186.
4. Amin A., Plimack E.R., Infante J.R., Ernstoff M.S. 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, Vol 32(5s):5010. abstr.
5. Amin A. Long-term survival in unfavorable-risk mRCC patients treated with a combination of autologous immunotherapy (AGS-003) plus sunitinib. ASCO Meeting Abstr. 2014, 32(15S):4524.
6. Attig S., Hennenlotter J., Pawelec G., et al. Simultaneous infiltration of polyfunctional effector and suppressor T cells into renal cell carcinomas. Cancer Res. 2009, 69(21):8412-8419.
7. Birkhäuser F.D., Koya R.C., Neufeld C., et al. Dendritic cell-based immunotherapy in prevention and treatment of renal cell carcinoma: efficacy, safety, and activity of Ad-GM·CAIX in immunocompetent mouse models. J. Immunother. 2013, 36(2):102-111.
8. Bjornsti M.A., Houghton P.J., The T.O.R. pathway: a target for cancer therapy. Nat. Rev. Cancer 2004, 4(5):335-348.
9. Bleumer I., Tiemessen D.M., Oosterwijk-Wakka J.C., et al. Preliminary analysis of patients with progressive renal cell carcinoma vaccinated with CA9-peptide-pulsed mature dendritic cells. J. Immunother. 2007, 30(1):116-122.
10. Brahmer J.R., Tykodi S.S., Chow L.Q., et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 2012, 366(26):2455-2465.
11. Callahan M. A phase 1 study to evaluate the safety and tolerability of MEDI4736, an anti?PD-L1 antibody, in combination with tremelimumab in patients with advanced solid tumors. ASCO Meeting Abstr. 2014, 32(15S):TPS3120.
12. Chen D.S., Irving B.A., Hodi F.S. Molecular pathways: next-generation immunotherapy-inhibiting programmed death-ligand 1 and programmed death-1. Clin. Cancer Res. 2012, 18(24):6580-6587.
13. Chiche J., Ilc K., Laferrière J., et al. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. 2009, 69(1):358-368.
14. DeBenedette M.A., Calderhead D.M., Tcherepanova I.Y., Nicolette C.A., Healey D.G. Potency of mature CD40L RNA electroporated dendritic cells correlates with IL-12 secretion by tracking multifunctional CD8(+)/CD28(+) cytotoxic T-cell responses in vitro. J. Immunother. 2011, 34(1):45-57.
15. Escudier B., Eisen T., Stadler W.M., et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N. Engl. J. Med. 2007, 356(2):125-134.
16. Escudier B., Pluzanska A., Koralewski P., et al. Bevacizumab plus interferon alfa-2a for treatment of metastatic renal cell carcinoma: a randomised, double-blind phase III trial. Lancet 2007, 370(9605):2103-2111.
17. Escudier B., Szczylik C., Hutson T.E., et al. Randomized phase II trial of first-line treatment with sorafenib versus interferon Alfa-2a in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 2009, 27(8):1280-1289.
18. Escudier B., Porta C., Bono P., et al. Randomized, controlled, double-blind, cross-over trial assessing treatment preference for pazopanib versus sunitinib in patients with metastatic renal cell carcinoma: PISCES Study. J. Clin. Oncol. 2014, 32(14):1412-1418.
19. Figlin R.A., Amin A., Dudek A., et al. Phase II. study combining personalized dendritic cell (DC)-based therapy, AGS-003, with sunitinib in metastatic renal cell carcinoma (mRCC). ASCO Meeting Abstracts 2012, vol. 30.
20. Figlin R.A., 2014. ADAPT. An ongoing international phase III randomized trial of autologous dendritic cell immunotherapy (AGS-003) plus standard treatment in advanced renal cell carcinoma (RCC). 32, 2014 (suppl 4; abstr 449^).
21. Finke J.H., Rini B., Ireland J., et al. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin. Cancer Res. 2008, 14(20):6674-6682.
22. Fisher R.I., Rosenberg S.A., Fyfe G. Long-term survival update for high-dose recombinant interleukin-2 in patients with renal cell carcinoma. Cancer J. Sci. Am. 2000, 6(Suppl 1):S55-S57.
23. Fisher R. A-PREDICT. A phase II study of axitinib in patients with metastatic renal cell cancer unsuitable for nephrectomy (CRUKE/11/061). ASCO Meeting Abstr. 2014, 32(15S):TPS4597.
24. Fosså S.D. Interferon in metastatic renal cell carcinoma. Semin. Oncol. 2000, 27(2):187-193.
25. Gore M.E., Hariharan S., Porta C., et al. Sunitinib in metastatic renal cell carcinoma patients with brain metastases. Cancer 2011, 117(3):501-509.
26. Griffiths R.W., Elkord E., Gilham D.E., et al. Frequency of regulatory T cells in renal cell carcinoma patients and investigation of correlation with survival. Cancer Immunol. Immunother. 2007, 56(11):1743-1753.
27. Hammers H. Phase I study of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma (mRCC). ASCO Meeting Abstr. 2014, 32(15S):4504.
28. Harris A.L. Hypoxia - a key regulatory factor in tumour growth. Nat. Rev. Cancer 2002, 2(1):38-47.
29. Hudes G., Carducci M., Tomczak P., et al. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N. Engl. J. Med. 2007, 356(22):2271-2281.
30. Hutson T.E., Lesovoy V., Al-Shukri S., et al. Axitinib versus sorafenib as first-line therapy in patients with metastatic renal-cell carcinoma: a randomised open-label phase 3 trial. Lancet Oncol. 2013, 14(13):1287-1294.
31. Hutson T.E., Escudier B., Esteban E., et al. Randomized phase III trial of temsirolimus versus sorafenib as second-line therapy after sunitinib in patients with metastatic renal cell carcinoma. J Clin Oncol. 2014, 32(8):760-767.
32. Ivanov S., Liao S.Y., Ivanova A., et al. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am. J. Pathol. 2001, 158(3):905-919.
33. Janikashvili N., Larmonier N., Katsanis E. Personalized dendritic cell-based tumor immunotherapy. Immunotherapy 2010, 2(1):57-68.
34. Kabbinavar, F.F., Nazy, Z., Belldegrun, Arie S., Wong, Steven G., Bot A., 2014. A phase I, open label, dose escalation and cohort expansion study to evaluate the safety and immune response to autologous dendritic cells (DC) transduced with AdGMCA9 (DC-AdGMCAIX) in patients with mRCC. Vol 32. J. Clin. Oncol. Abst 490.
35. Karumanchi S.A., Merchan J., Sukhatme V.P. Renal cancer: molecular mechanisms and newer therapeutic options. Curr. Opin. Nephrol. Hypertens. 2002, 11(1):37-42.
36. King S.C., Pollack L., Li J., King J.B., Master V.A. Continued rise in incidence of renal cell, carcinoma especially in young and high-grade disease-US 2001-2010. J. Urol. 2014.
37. Latif F., Tory K., Gnarra J., et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993, 260(5112):1317-1320.
38. Leibovich B.C., Sheinin Y., Lohse C.M., et al. Carbonic anhydrase IX is not an independent predictor of outcome for patients with clear cell renal cell carcinoma. J. Clin. Oncol. 2007, 25(30):4757-4764.
39. Leung S.K., Ohh M. Playing Tag with HIF: the VHL Story. J. Biomed. Biotechnol. 2002, 2(3):131-135.
40. Liotta F., Gacci M., Frosali F., et al. Frequency of regulatory T cells in peripheral blood and in tumour-infiltrating lymphocytes correlates with poor prognosis in renal cell carcinoma. BJU Int. 2011, 107(9):1500-1506.
41. Lipson E.J., Sharfman W.H., Drake C.G., et al. Durable cancer regression off-treatment and effective reinduction therapy with an anti-PD-1 antibody. Clin. Cancer Res. 2013, 19(2):462-468.
42. Ljungberg B., Campbell S.C., Choi H.Y., et al. The epidemiology of renal cell carcinoma. Eur. Urol. 2011, 60(4):615-621.
43. Lokich J. Spontaneous regression of metastatic renal cancer. Case report and literature review. Am. J. Clin. Oncol. 1997, 20(4):416-418.
44. Maher E.R., Neumann H.P., Richard S. von Hippel-Lindau disease: a clinical and scientific review. Eur. J. Hum. Genet. 2011, 19(6):617-623.
45. McDermott D.F., Cheng S.C., Signoretti S., et al. The high-dose aldesleukin "select" trial: a trial to prospectively validate predictive models of response treatment in patients with metastatic renal cell carcinoma. Clin. Cancer Res. 2014.
46. Motzer R.J., Rini B.I., Bukowski R.M., et al. Sunitinib in patients with metastatic renal cell carcinoma. JAMA 2006, 295(21):2516-2524.
47. Motzer R.J., Hutson T.E., Tomczak P., et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N. Engl. J. Med. 2007, 356(2):115-124.
48. Motzer R.J., 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(9637):449-456.
49. Motzer R.J., Hutson T.E., Tomczak P., et al. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 2009, 27(22):3584-3590.
50. Motzer R.J., Escudier B., Oudard S., et al. Phase 3 trial of everolimus for metastatic renal cell carcinoma: final results and analysis of prognostic factors. Cancer 2010, 116(18):4256-4265.
51. Motzer R.J., Hutson T.E., Cella D., et al. Pazopanib versus sunitinib in metastatic renal-cell carcinoma. N. Engl. J. Med. 2013, 369(8):722-731.
52. Motzer R.J., Escudier B., Tomczak P., et al. Axitinib versus sorafenib as second-line treatment for advanced renal cell carcinoma: overall survival analysis and updated results from a randomised phase 3 trial. Lancet Oncol. 2013, 14(6):552-562.
53. Motzer R.J., Barrios C.H., Kim T.M., et al. Phase II. randomized trial comparing sequential first-line everolimus and second-line sunitinib versus first-line sunitinib and second-line everolimus in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 2014, 32(25):2765-2772.
54. Motzer R.J., Porta C., Vogelzang N.J., et al. Dovitinib versus sorafenib for third-line targeted treatment of patients with metastatic renal cell carcinoma: an open-label, randomised phase 3 trial. Lancet Oncol. 2014, 15(3):286-296.
55. Patard J.J., Fergelot P., Karakiewicz P.I., et al. Low CAIX expression and absence of VHL gene mutation are associated with tumor aggressiveness and poor survival of clear cell renal cell carcinoma. Int. J. Cancer 2008, 123(2):395-400.
56. Ribas A. Tumor immunotherapy directed at PD-1. N. Engl. J. Med. 2012, 366(26):2517-2519.
57. Rini B.I., Halabi S., Rosenberg J.E., 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(13):2137-2143.
58. Rini B.I., 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(9807):1931-1939.
59. Rosenberg S.A., Yang J.C., Topalian S.L., et al. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin 2. JAMA 1994, 271(12):907-913.
60. Sabado R.L., Bhardwaj N. Directing dendritic cell immunotherapy towards successful cancer treatment. Immunotherapy 2010, 2(1):37-56.
61. Schendel D.J., Gansbacher B., Oberneder R., et al. Tumor-specific lysis of human renal cell carcinomas by tumor-infiltrating lymphocytes. I. HLA-A2-restricted recognition of autologous and allogeneic tumor lines. J. Immunol. 1993, 151(8):4209-4220.
62. Siegel R., Ma J., Zou Z., Jemal A. Cancer statistics, 2014. CA Cancer J. Clin. 2014, 64(1):9-29.
63. Sternberg C.N., Davis I.D., 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(6):1061-1068.
64. Sternberg C.N., Hawkins R.E., Wagstaff J., et al. A randomised, double-blind phase III study of pazopanib in patients with advanced and/or metastatic renal cell carcinoma: final overall survival results and safety update. Eur. J. Cancer 2013, 49(6):1287-1296.
65. Thompson R.H., Kuntz S.M., Leibovich B.C., et al. Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res. 2006, 66(7):3381-3385.
66. Topalian S.L., Hodi F.S., Brahmer J.R., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 2012, 366(26):2443-2454.
67. Uemura H., Fujimoto K., Tanaka M., et al. A phase I trial of vaccination of CA9-derived peptides for HLA-A24-positive patients with cytokine-refractory metastatic renal cell carcinoma. Clin. Cancer Res. 2006, 12(6):1768-1775.
68. Yagoda A., Petrylak D., Thompson S. Cytotoxic chemotherapy for advanced renal cell carcinoma. Urol. Clin. North Am. 1993, 20(2):303-321.
69. Yang J.C., Haworth L., Sherry R.M., et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N. Engl. J. Med. 2003, 349(5):427-434.