Checkpoint modulation - A new way to direct the immune system against renal cell carcinoma

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 5, 2015, Pages 1201-1208

  Bedke, Jens ^a,b   Kruck, Stephan ^a   Gakis, Georgios ^a   Stenzl, Arnulf ^a,b   Goebell, Peter J ^c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Checkpoint inhibition; Immunotherapy; IMP321; Ipilimumab; Nivolumab; Renal cell carcinoma; Tremelimumab; Tyrosine kinase inhibitor

Indexed keywords

AMP 224; AVELUMAB; B7 ANTIGEN; BMS 936559; CD28 ANTIGEN; CD86 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DACARBAZINE; DURVALUMAB; GLYCOPROTEIN GP 100; IMP 321; INTERLEUKIN 2; IPILIMUMAB; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MPDL 3280A; NIVOLUMAB; PAZOPANIB; PEMBROLIZUMAB; PIDILIZUMAB; PROGRAMMED DEATH 1 RECEPTOR; SUNITINIB; TICILIMUMAB; UNCLASSIFIED DRUG; CTLA4 PROTEIN, HUMAN; IMMUNOLOGIC FACTOR; PDCD1 PROTEIN, HUMAN;

ADRENAL METASTASIS; ARTICLE; ASEPTIC MENINGITIS; CELL CYCLE CHECKPOINT; DRUG RESPONSE; HLA SYSTEM; HUMAN; IMMUNE SYSTEM; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSURVEILLANCE; KIDNEY CARCINOMA; METASTATIC MELANOMA; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); T LYMPHOCYTE ACTIVATION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; METABOLISM; PROCEDURES;

CARCINOMA, RENAL CELL; CTLA-4 ANTIGEN; HUMANS; IMMUNE SYSTEM; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; PROGRAMMED CELL DEATH 1 RECEPTOR;

EID: 84942430442     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1016657     Document Type: Article

References (59)

1. Yang JC, Sherry RM, Steinberg SM, Topalian SL, Schwartzentruber DJ, Hwu P, Seipp CA, Rogers-Freezer L, Morton KE, White DE, et al. Randomized study of high-dose and low-dose interleukin-2 in patients with metastatic renal cancer. J Clin Oncol 2003; 21(16):3127-32; PMID:12915604; http://dx. doi.org/10.1200/JCO.2003.02.122
2. Ljungberg B, Cowan NC, Hanbury DC, Hora M, Kuczyk MA, Merseburger AS, Patard JJ, Mulders PF, Sinescu IC; European Association of Urology Guideline Group. EAU guidelines on renal cell carcinoma: the 2010 update. Eur Urol 2010; 58(3):398-406; PMID:20633979; http://dx.doi.org/10.1016/j. eururo.2010.06.032
3. Flanigan RC, Mickisch G, Sylvester R, Tangen C, Van Poppel H, Crawford ED. Cytoreductive nephrectomy in patients with metastatic renal cancer: a combined analysis. J Urol 2004; 171(3):1071-6; PMID:14767273; http://dx.doi.org/10.1097/01. ju.0000110610.61545.ae
4. Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Oudard S, Negrier S, Szczylik C, Pili R, Bjarnason GA, 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):3584-90; PMID:19487381; http://dx.doi.org/10.1200/JCO.2008.20.1293
5. Motzer RJ, Hutson TE, McCann L, Deen K, Choueiri TK. Overall survival in renal-cell carcinoma with pazopanib versus sunitinib. N Engl J Med 2014; 370 (18):1769-70; PMID:24785224; http://dx.doi.org/ 10.1056/NEJMc1400731
6. Rini BI, Escudier B, Tomczak P, Kaprin A, Szczylik C, Hutson TE, Michaelson MD, Gorbunova VA, Gore ME, Rusakov IG, et al. Comparative effectiveness of axitinib versus sorafenib in advanced renal cell carcinoma (AXIS): a randomised phase 3 trial. Lancet 2011; 378(9807):1931-9; PMID:22056247; http://dx.doi. org/10.1016/S0140-6736(11)61613-9
7. Kruck S, Bedke J, Kuczyk MA, Merseburger AS. Second-line systemic therapy for the treatment of metastatic renal cell cancer. Exp Rev Antican Ther 2012; 12 (6):777-85; PMID:22716494; http://dx.doi.org/ 10.1586/era.12.43
8. van der Vliet HJ, Koon HB, Yue SC, Uzunparmak B, Seery V, Gavin MA, Rudensky AY, Atkins MB, Balk SP, Exley MA. Effects of the administration of highdose interleukin-2 on immunoregulatory cell subsets in patients with advanced melanoma and renal cell cancer. Clin Cancer Res 2007; 13(7):2100-08; PMID:17404092; http://dx.doi.org/10.1158/1078-0432.CCR-06-1662
9. Ahmadzadeh M, Rosenberg SA. IL-2 administration increases CD4C CD25(hi) Foxp3C regulatory T cells in cancer patients. Blood 2006; 107(6):2409-14; PMID:16304057; http://dx.doi.org/10.1182/blood-2005-06-2399
10. Bedke J, Stenzl A. Immunotherapeutic strategies for the treatment of renal cell carcinoma: where are we now? Exp Rev Antican Ther 2013; 13(12):1399-408; PMID:24215158; http://dx.doi.org/10.1586/ 14737140.2013.856761
11. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Sciencel 1991; 254(5038):1643-7; PMID:1840703; http://dx.doi. org/10.1126/science.1840703
12. Amin A, Dudek A, Logan T, Lance RS, Holzbeierlein JM, Master VA, Kumar Pal S, Knox JJ, Karsh LI, Plessinger D, et al. Prolonged survival with personalized immunotherapy (AGS-003) in combination with sunitinib in unfavorable risk metastatic RCC (mRCC). J Clin Oncol 2013; 31((suppl 6); abstr 357)
13. Wood C, Srivastava P, Bukowski R, Lacombe L, Gorelov AI, Gorelov S, Mulders P, Zielinski H, Hoos A, Teofilovici F, et al. An adjuvant autologous therapeutic vaccine (HSPPC-96; vitespen) versus observation alone for patients at high risk of recurrence after nephrectomy for renal cell carcinoma: a multicentre, open-label, randomised phase III trial. Lancet 2008; 372 (9633):145-54; PMID:18602688; http://dx.doi.org/ 10.1016/S0140-6736(08)60697-2
14. Jocham D, Richter A, Hoffmann L, Iwig K, Fahlenkamp D, Zakrzewski G, Schmitt E, Dannenberg T, Lehmacher W, von Wietersheim J, et al. Adjuvant autologous renal tumour cell vaccine and risk of tumour progression in patients with renal-cell carcinoma after radical nephrectomy: phase III, randomised controlled trial. Lancet 2004; 363(9409):594-9; PMID:14987883; http://dx.doi.org/10.1016/S0140-6736(04)15590-6
15. Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, Szczylik C, Staehler M, Brugger W, Dietrich PY, Mendrzyk R, et al. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 2012; 18(8), 1254-61; PMID:22842478; http:// dx.doi.org/10.1038/nm.2883
16. IMA901 in Patients Receiving Sunitinib for Advanced/ Metastatic Renal Cell Carcinoma. http://clinicaltrials. gov/ct2/show/NCT01265901.
17. Phase 3 Trial of Autologous Dendritic Cell Immunotherapy (AGS-003) Plus Standard Treatment of Advanced Renal Cell Carcinoma (RCC) (ADAPT). http://clinicaltrials.gov/show/NCT01582672.
18. Burnet M. Cancer; a biological approach. I. The processes of control. Br Med J 1957; 1(5022):779-86; PMID:13404306; http://dx.doi.org/10.1136/ bmj.1.5022.779
19. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immun 2002; 3(11):991-8; PMID:12407406; http://dx.doi.org/10.1038/ni1102-991
20. Thomas L. "Discussion" Cellular and Humoral Aspects of the Hypersensitive States. Lawrence HS (ed.), New York: Hoeber-Harper; 1957:529-33.
21. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 2010; 22(2):231-7; PMID:20144856; http://dx.doi.org/10.1016/j.coi.2010.01.009
22. Bedke J, Gouttefangeas C, Singh-Jasuja H, Stevanovic S, Behnes CL, Stenzl A. Targeted therapy in renal cell carcinoma: moving from molecular agents to specific immunotherapy. World J Urol 2014; 32(1); 31-8; PMID:23404195; http://dx.doi.org/10.1007/s00345-013-1033-3
23. Curiel TJ. Tregs and rethinking cancer immunotherapy. J Clin Invest 2007; 117(5):1167-74; PMID:17476346; http://dx.doi.org/10.1172/ JCI31202
24. Kusmartsev S, Su Z, Heiser A, Dannull J, Eruslanov E, Kübler H, Yancey D, Dahm P, Vieweg J. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin Cancer Res 2008; 14(24):8270-8; PMID:19088044; http://dx.doi. org/10.1158/1078-0432.CCR-08-0165
25. Greenwald RJ, Freeman GJ, Sharpe AH. The B7 family revisited. Ann Rev Immunol 2005; 23:515-48; PMID:15771580; http://dx.doi.org/10.1146/annurev. immunol.23.021704.115611
26. Salomon B, Bluestone JA. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Ann Rev Immunol 2001; 19:225-52; PMID:11244036; http://dx.doi.org/10.1146/annurev. immunol.19.1.225
27. Probst HC, McCoy K, Okazaki T, Honjo T, van den Broek M. Resting dendritic cells induce peripheral CD8C T cell tolerance through PD-1 and CTLA-4. Nat Immunol 2005; 6(3):280-6; PMID:15685176; http://dx.doi.org/10.1038/ni1165
28. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Ann Rev Immunol 2003; 21:685-711; PMID:12615891; http://dx.doi.org/10.1146/ annurev.immunol.21.120601.141040
29. Linsley PS, Brady W, Grosmaire L, Aruffo A, Damle NK, Ledbetter JA. Binding of the B cell activation antigen B7 to CD28 costimulates T cell proliferation and interleukin 2 mRNA accumulation. J Exp Med 1991; 173(3):721-30; PMID:1847722; http://dx.doi.org/ 10.1084/jem.173.3.721
30. Linsley PS, Brady W, Urnes M, Grosmaire LS, Damle NK, Ledbetter JA. CTLA-4 is a second receptor for the B cell activation antigen B7. J Exp Med 1991; 174(3), 561-9; PMID:1714933; http://dx.doi.org/10.1084/ jem.174.3.561
31. Walunas TL, Bakker CY, Bluestone JA. CTLA-4 ligation blocks CD28-dependent T cell activation. J Exp Med 1996; 183(6):2541-50; PMID:8676075; http:// dx.doi.org/10.1084/jem.183.6.2541
32. Sansom DM, Manzotti CN, Zheng Y. What's the difference between CD80 and CD86? Trends Immunol 2003; 24(6):314-9; PMID:12810107; http://dx.doi. org/10.1016/S1471-4906(03)00111-X
33. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995; 3(5):541-7; PMID:7584144; http://dx.doi.org/10.1016/1074-7613(95)90125-6
34. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996; 271(5256):1734-6; PMID:8596936; http://dx. doi.org/10.1126/science.271.5256.1734
35. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363(8):711-23; PMID:20525992; http://dx.doi.org/10.1056/NEJMoa1003466
36. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011; 364(26):2517-26; PMID:21639810; http://dx.doi. org/10.1056/NEJMoa1104621
37. Ribas A, Kefford R, Marshall MA, Punt CJ, Haanen JB, Marmol M, Garbe C, Gogas H, Schachter J, Linette G, et al. Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol 2013; 31(5):616-22; PMID:23295794; http://dx.doi. org/10.1200/JCO.2012.44.6112
38. Yang JC, Hughes M, Kammula U, Royal R, Sherry RM, Topalian SL, Suri KB, Levy C, Allen T, Mavroukakis S, et al. Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J Immunothera 2007; 30(8):825-30; PMID:18049334; http://dx.doi. org/10.1097/CJI.0b013e318156e47e
39. Rini BI, Stein M, Shannon P, Eddy S, Tyler A, Stephenson JJ Jr, Catlett L, Huang B, Healey D, Gordon M. Phase 1 dose-escalation trial of tremelimumab plus sunitinib in patients with metastatic renal cell carcinoma. Cancer 2011; 117(4):758-67; PMID:20922784; http://dx.doi.org/10.1002/ cncr.25639
40. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002; 8(8):793-800; PMID:12091876
41. Curiel TJ, Wei S, Dong H, Alvarez X, Cheng P, Mottram P, Krzysiek R, Knutson KL, Daniel B, Zimmermann MC, et al. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med 2003; 9(5):562-7; PMID:12704383; http://dx.doi. org/10.1038/nm863
42. Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci U S A 2002; 99(19):12293-7; PMID:12218188; http://dx.doi.org/10.1073/pnas.192461099
43. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366(26):2455-65; PMID:22658128; http://dx.doi.org/10.1056/ NEJMoa1200694
44. Topalian SL, Hodi FS, Brahmer JR, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366(26):2443-54; PMID:22658127; http://dx.doi. org/10.1056/NEJMoa1200690
45. Aranda F, Vacchelli E, Eggermont A, Galon J, Fridman WH, Zitvogel L, Kroemer G, Galluzzi L. Trial Watch: Immunostimulatory monoclonal antibodies in cancer therapy. Oncoimmunology 2014; 3(1):e27297; PMID:24701370; http://dx.doi.org/10.4161/ onci.27297
46. Study of BMS-936558 vs. Everolimus in Pre-Treated Advanced Or Metastatic Clear-cell RCC. http://clinical trials.gov/ct2/show/NCT01668784.
47. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, Brahmer JR, Lawrence DP, Atkins MB, Powderly JD, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014; 32(10):1020-30; PMID:24590637; http://dx. doi.org/10.1200/JCO.2013.53.0105
48. Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, Hassel JC, Rutkowski P, McNeil C, Kalinka-Warzocha E, et al. Nivolumab in Previously Untreated Melanoma without BRAF Mutation. N Engl J Med (2015); 372(4):320-30. doi: 10.1056/ NEJMoa1412082
49. Motzer RJ, Rini BI, McDermott DF, Redman BG, Kuzel T, Harrison MR, Vaishampayan UN, Drabkin HA, George S, Logan TF, et al. Nivolumab for metastatic renal cell carcinoma (mRCC): Results of a randomized, dose-ranging phase II trial. J Clin Oncol 2014; 32:5s, abstr 5009
50. Amin A, Plimack ER, Infante JR, Ernstoff MS, Rini BI, McDermott DF, Knox JJ, Pal KS, Voss MH, Sharma P, 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, abstr 5010
51. Hammers HJ, Plimack ER, Infante JR, Ernstoff MS, Rini BI, McDermott DF, Razak ARA, Pal KS, Voss MH, Sharma P, et al. Phase I study of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma (mRCC). J Clin Oncol 2014; 32:5s, abstr 4504
52. Nivolumab Combined With Ipilimumab Versus Sunitinib in Previously Untreated Advanced or Metastatic Renal Cell Carcinoma (CheckMate 214). http://clinical trials.gov/ct2/show/NCT02231749.
53. Robert C, Ribas A, Wolchok JD, Hodi FS, Hamid O, Kefford R, Weber JS, Joshua AM, Hwu WJ, Gangadhar TC, et al. Anti-programmed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. Lancet 2014; 384 (9948):1109-17; PMID:25034862; http://dx.doi.org/ 10.1016/S0140-6736(14)60958-2
54. Infante JR, Powderly JD, Burris HA, Kittaneh M, Houston Grice J, Smothers JF, Brett S, Fleming ME, May R, Marshall S, et al. Clinical and pharmacodynamic (PD) results of a phase I trial with AMP-224 (B7-DC Fc) that binds to the PD-1 receptor. J Clin Oncol 2013; 31((suppl 6); abstr 3044)
55. Armand P, Nagler A, Weller EA, Devine SM, Avigan DE, Chen YB, Kaminski MS, Holland HK, Winter JN, Mason JR, et al. Disabling immune tolerance by programmed death-1 blockade with pidilizumab after autologous hematopoietic stem-cell transplantation for diffuse large B-cell lymphoma: results of an international phase II trial. J Clin Oncol 2013; 31(33):4199-4206; PMID:24127452; http://dx.doi.org/10.1200/ JCO.2012.48.3685
56. Lutzky J, Antonia SJ, Blake-Haskins A, Li X, Robbins PB, Shalabi AM, Vasselli J, Ibrahim RA, Khleif S, Segal NH. A phase 1 study of MEDI4736, an anti-PD-L1 antibody, in patients with advanced solid tumors. J Clin Oncol 2014; 32:5s
57. Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, Bellmunt J, Burris HA, Petrylak DP, Teng SL, et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 2014; 515(7528):558-62; PMID:25428503; http://dx. doi.org/10.1038/nature13904
58. Herry CR, O'Sullivan Coyne GH, Madan RA, Schlom J, von Heydebreck A, Cuillerot JM, Sabzevari H, Gulley JL. Phase I open-label, multiple ascending dose trial of MSB0010718C, an anti-PD-L1 monoclonal antibody, in advanced solid malignancies. J Clin Oncol 2014; 32:5s, abstr 3064.
59. Brignone C, Escudier B, Grygar C, Marcu M, Triebel F. A phase I pharmacokinetic and biological correlative study of IMP321, a novel MHC class II agonist, in patients with advanced renal cell carcinoma. Clin Cancer Res 2009; 15(19):6225-6231; PMID:19755389; http://dx.doi.org/10.1158/1078-0432.CCR-09-0068