Immunologic Correlates in the Course of Treatment With Immunomodulating Antibodies

Seminars in Oncology

Volumn 42, Issue 3, 2015, Pages 448-458

  Weide, Benjamin ^a   Di Giacomo, Anna Maria ^b   Fonsatti, Ester ^b   Zitvogel, Laurence ^c,d,e,f  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL OF SIENA   (Italy)

^c INSTITUT GUSTAVE ROUSSY   (France)

^d University Paris XI   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

^f Center of Clinical Investigations in Biotherapies of Cancer   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BMS 936559; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; DURVALUMAB; IMMUNOMODULATING AGENT; IPILIMUMAB; MPDL 3280A; NIVOLUMAB; PEMBROLIZUMAB; PIDILIZUMAB; TUMOR MARKER; ANTINEOPLASTIC AGENT; IMMUNOLOGIC FACTOR; MONOCLONAL ANTIBODY;

ARTICLE; BONE MARROW CELL; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CLINICAL PRACTICE; CORRELATIONAL STUDY; DRUG EFFICACY; EOSINOPHIL; FUTUROLOGY; HUMAN; IMMUNE RESPONSE GENE; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOMODULATION; LYMPHOCYTE; MULTICENTER STUDY (TOPIC); MYELOID DERIVED SUPPRESSOR CELL; NEOPLASM; NEUTROPHIL; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGULATORY T LYMPHOCYTE; SERUM; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR ASSOCIATED LEUKOCYTE; VALIDATION STUDY; ANIMAL; IMMUNOLOGY; MELANOMA; PATHOLOGY; SECONDARY; SKIN NEOPLASMS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; HUMANS; IMMUNOLOGIC FACTORS; MELANOMA; SKIN NEOPLASMS; T-LYMPHOCYTES, REGULATORY;

EID: 84929223574     PISSN: 00937754     EISSN: 15328708     Source Type: Journal    
DOI: 10.1053/j.seminoncol.2015.02.016     Document Type: Review

References (89)

1. R.R. Ji, S.D. Chasalow, and L. Wang An immune-active tumor microenvironment favors clinical response to ipilimumab Cancer Immunol Immunother 61 2012 1019 1031
2. P.A. Ascierto, M. Kalos, D.A. Schaer, M.K. Callahan, and J.D. Wolchok Biomarkers for immunostimulatory monoclonal antibodies in combination strategies for melanoma and other tumor types Clin Cancer Res 19 2013 1009 1020
3. T. Fu, Q. He, and P. Sharma The ICOS/ICOSL pathway is required for optimal antitumor responses mediated by anti-CTLA-4 therapy Cancer Res 71 2011 5445 5454
4. S.A. Quezada, T.R. Simpson, and K.S. Peggs Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts J Exp Med 207 2010 637 650
5. D. Hannani, M. Vetizou, and D. Enot Anticancer immunotherapy by CTLA-4 blockade: obligatory contribution of IL-2 receptors and negative prognostic impact of soluble CD25 Cell Res 25 2015 208 224
6. D.M. Berman, J. Wolchok, J. Weber, O. Hamid, S. O'Day, and S.D. Chasalow Association of peripheral blood absolute lymphocyte count (ALC) and clinical activity in patients (pts) with advanced melanoma treated with ipilimumab ASCO Meeting Abstracts 27 2009 3020
7. M.A. Postow, S.D. Chasalow, and J. Yuan Pharmacodynamic effect of ipilimumab on absolute lymphocyte count (ALC) and association with overall survival in patients with advanced melanoma ASCO Meeting Abstracts 31 2013 9052
8. J.D. Wolchok, and Y. Saenger The mechanism of anti-CTLA-4 activity and the negative regulation of T-cell activation Oncologist 13 Suppl 4 2008 2 9
9. W. Wang, D. Yu, and A.A. Sarnaik Biomarkers on melanoma patient T cells associated with ipilimumab treatment J Transl Med 10 2012 146
10. A. Ribas, M.R. Benz, and M.S. Allen-Auerbach Imaging of CTLA4 blockade-induced cell replication with (18)F-FLT PET in patients with advanced melanoma treated with tremelimumab J Nucl Med 51 2010 340 346
11. A.A. Sarnaik, B. Yu, and D. Yu Extended dose ipilimumab with a peptide vaccine: immune correlates associated with clinical benefit in patients with resected high-risk stage IIIc/IV melanoma Clin Cancer Res 17 2011 896 906
12. B. Comin-Anduix, H. Sazegar, and T. Chodon Modulation of cell signaling networks after CTLA4 blockade in patients with metastatic melanoma PLoS One 5 2010 e12711
13. G.Y. Ku, J. Yuan, and D.B. Page Single-institution experience with ipilimumab in advanced melanoma patients in the compassionate use setting: lymphocyte count after 2 doses correlates with survival Cancer 116 2010 1767 1775
14. S. Wilgenhof, S. Du Four, and F. Vandenbroucke Single-center experience with ipilimumab in an expanded access program for patients with pretreated advanced melanoma J Immunother 36 2013 215 222
15. S. Kelderman, B. Heemskerk, and H. van Tinteren Lactate dehydrogenase as a selection criterion for ipilimumab treatment in metastatic melanoma Cancer Immunol Immunother 63 2014 449 458
16. J. Delyon, C. Mateus, and D. Lefeuvre Experience in daily practice with ipilimumab for the treatment of patients with metastatic melanoma: an early increase in lymphocyte and eosinophil counts is associated with improved survival Ann Oncol 24 2013 1697 1703
17. A.M. Di Giacomo, R. Danielli, and L. Calabro Ipilimumab experience in heavily pretreated patients with melanoma in an expanded access program at the University Hospital of Siena (Italy) Cancer Immunol Immunother 60 2011 467 477
18. E. Simeone, G. Gentilcore, and A. Romano Immunological and biological changes during ipilimumab (Ipi) treatment and their correlation with clinical response and survival ASCO Meeting Abstracts 30 2012 8573
19. F.J. Ibarrondo, O.O. Yang, and T. Chodon Natural killer T cells in advanced melanoma patients treated with tremelimumab PLoS One 8 2013 e76829
20. E. Cha, M. Klinger, and Y. Hou Improved survival with T cell clonotype stability after anti-CTLA-4 treatment in cancer patients Sci Transl Med 6 2014 238ra70
21. B. Weide, H. Zelba, and E. Derhovanessian Functional T cells targeting NY-ESO-1 or Melan-A are predictive for survival of patients with distant melanoma metastasis J Clin Oncol 30 2012 1835 1841
22. H. Zelba, B. Weide, and A. Martens Circulating CD4+T cells that produce IL4 or IL17 when stimulated by Melan-A but not by NY-ESO-1 have negative impacts on survival of patients with stage IV melanoma Clin Cancer Res 20 2014 4390 4399
23. S.A. Rosenberg, J.C. Yang, and R.M. Sherry Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy Clin Cancer Res 17 2011 4550 4557
24. P.F. Robbins, R.A. Morgan, and S.A. Feldman Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1 J Clin Oncol 29 2011 917 924
25. A.A. Tarhini, H. Edington, and L.H. Butterfield Immune monitoring of the circulation and the tumor microenvironment in patients with regionally advanced melanoma receiving neoadjuvant ipilimumab PLoS One 9 2014 e87705
26. C.I. Liakou, A. Kamat, and D.N. Tang CTLA-4 blockade increases IFNgamma-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients Proc Natl Acad Sci U S A 105 2008 14987 14992
27. J. Yuan, M. Adamow, and B.A. Ginsberg Integrated NY-ESO-1 antibody and CD8+T-cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab Proc Natl Acad Sci U S A 108 2011 16723 16728
28. J. Yuan, S. Gnjatic, and H. Li CTLA-4 blockade enhances polyfunctional NY-ESO-1 specific T cell responses in metastatic melanoma patients with clinical benefit Proc Natl Acad Sci U S A 105 2008 20410 20415
29. J. Yuan, B. Ginsberg, and D. Page CTLA-4 blockade increases antigen-specific CD8(+) T cells in prevaccinated patients with melanoma: three cases Cancer Immunol Immunother 60 2011 1137 1146
30. K. Sanderson, R. Scotland, and P. Lee Autoimmunity in a phase I trial of a fully human anti-cytotoxic T-lymphocyte antigen-4 monoclonal antibody with multiple melanoma peptides and Montanide ISA 51 for patients with resected stages III and IV melanoma J Clin Oncol 23 2005 741 750
31. P. Attia, G.Q. Phan, and A.V. Maker Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic T-lymphocyte antigen-4 J Clin Oncol 23 2005 6043 6053
32. F.S. Hodi, S.J. O'Day, and D.F. McDermott Improved survival with ipilimumab in patients with metastatic melanoma N Engl J Med 363 2010 711 723
33. J.S. Weber, O. Hamid, and S.D. Chasalow Ipilimumab increases activated T cells and enhances humoral immunity in patients with advanced melanoma J Immunother 35 2012 89 97
34. A.M. Di Giacomo, L. Calabro, and R. Danielli Long-term survival and immunological parameters in metastatic melanoma patients who responded to ipilimumab 10 mg/kg within an expanded access programme Cancer Immunol Immunother 62 2013 1021 1028
35. H. Chen, C.I. Liakou, and A. Kamat Anti-CTLA-4 therapy results in higher CD4+ICOShi T cell frequency and IFN-gamma levels in both nonmalignant and malignant prostate tissues Proc Natl Acad Sci U S A 106 2009 2729 2734
36. B.C. Carthon, J.D. Wolchok, and J. Yuan Preoperative CTLA-4 blockade: tolerability and immune monitoring in the setting of a presurgical clinical trial Clin Cancer Res 16 2010 2861 2871
37. L. Calabro, A. Morra, and E. Fonsatti Tremelimumab for patients with chemotherapy-resistant advanced malignant mesothelioma: an open-label, single-arm, phase 2 trial Lancet Oncol 14 2013 1104 1111
38. T.J. Curiel, G. Coukos, and L. Zou Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival Nat Med 10 2004 942 949
39. P.A. Antony, C.A. Piccirillo, and A. Akpinarli CD8+T cell immunity against a tumor/self-antigen is augmented by CD4+T helper cells and hindered by naturally occurring T regulatory cells J Immunol 174 2005 2591 2601
40. C. Menard, F. Ghiringhelli, and S. Roux Ctla-4 blockade confers lymphocyte resistance to regulatory T-cells in advanced melanoma: surrogate marker of efficacy of tremelimumab? Clin Cancer Res 14 2008 5242 5249
41. A.V. Maker, G.Q. Phan, and P. Attia Tumor regression and autoimmunity in patients treated with cytotoxic T lymphocyte-associated antigen 4 blockade and interleukin 2: a phase I/II study Ann Surg Oncol 12 2005 1005 1016
42. S.J. Santegoets, A.G. Stam, and S.M. Lougheed T cell profiling reveals high CD4+CTLA-4+T cell frequency as dominant predictor for survival after prostate GVAX/ipilimumab treatment Cancer Immunol Immunother 62 2013 245 256
43. K. Schindler, K. Harmankaya, and M.A. Postow Pretreatment levels of absolute and relative eosinophil count to improve overall survival (OS) in patients with metastatic melanoma under treatment with ipilimumab, an anti CTLA-4 antibody ASCO Meeting Abstracts 31 2013 9024
44. D.I. Gabrilovich, and S. Nagaraj Myeloid-derived suppressor cells as regulators of the immune system Nat Rev Immunol 9 2009 162 174
45. D.I. Gabrilovich, S. Ostrand-Rosenberg, and V. Bronte Coordinated regulation of myeloid cells by tumours Nat Rev Immunol 12 2012 253 268
46. C.M. Diaz-Montero, M.L. Salem, M.I. Nishimura, E. Garrett-Mayer, D.J. Cole, and A.J. Montero Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy Cancer Immunol Immunother 58 2009 49 59
47. E. Eruslanov, M. Neuberger, and I. Daurkin Circulating and tumor-infiltrating myeloid cell subsets in patients with bladder cancer Int J Cancer 130 2012 1109 1119
48. X.K. Yuan, X.K. Zhao, Y.C. Xia, X. Zhu, and P. Xiao Increased circulating immunosuppressive CD14(+)HLA-DR(-/low) cells correlate with clinical cancer stage and pathological grade in patients with bladder carcinoma J Int Med Res 39 2011 1381 1391
49. B. Schilling, A. Sucker, and K. Griewank Vemurafenib reverses immunosuppression by myeloid derived suppressor cells Int J Cancer 133 2013 1653 1663
50. S. Solito, E. Falisi, and C.M. Diaz-Montero A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells Blood 118 2011 2254 2265
51. S. Walter, T. Weinschenk, and A. Stenzl Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival Nat Med 18 2012 1254 1261
52. S. Kalathil, A.A. Lugade, A. Miller, R. Iyer, and Y. Thanavala Higher frequencies of GARP+CTLA-4+Foxp3+T regulatory cells and myeloid-derived suppressor cells in hepatocellular carcinoma patients are associated with impaired T-cell functionality Cancer Res 73 2013 2435 2444
53. B. Weide, A. Martens, and H. Zelba Myeloid-derived suppressor cells predict survival of patients with advanced melanoma: comparison with regulatory T cells and NY-ESO-1- or Melan-A-specific T cells Clin Cancer Res 20 2014 1601 1609
54. C. Meyer, L. Cagnon, and C.M. Costa-Nunes Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab Cancer Immunol Immunother 63 2014 247 257
55. S. Kitano, M.A. Postow, and C. Cortez Myeloid-derived suppressor cell quantity prior to treatment with ipilimumab at 10mg/kg to predict for overall survival in patients with metastatic melanoma ASCO Meeting Abstracts 30 2012 2518
56. F.S. Hodi, M. Butler, and D.A. Oble Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients Proc Natl Acad Sci U S A 105 2008 3005 3010
57. M. Jinushi, F.S. Hodi, and G. Dranoff Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity Proc Natl Acad Sci U S A 103 2006 9190 9195
58. R.R. Huang, J. Jalil, and J.S. Economou CTLA4 blockade induces frequent tumor infiltration by activated lymphocytes regardless of clinical responses in humans Clin Cancer Res 17 2011 4101 4109
59. O. Hamid, H. Schmidt, and A. Nissan A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma J Transl Med 9 2011 204
60. M.E. Keir, M.J. Butte, G.J. Freeman, and A.H. Sharpe PD-1 and its ligands in tolerance and immunity Annu Rev Immunol 26 2008 677 704
61. J.D. Wolchok, H. Kluger, and M.K. Callahan Nivolumab plus ipilimumab in advanced melanoma N Engl J Med 369 2013 122 133
62. S.L. Topalian, F.S. Hodi, and J.R. Brahmer Safety, activity, and immune correlates of anti-PD-1 antibody in cancer N Engl J Med 366 2012 2443 2454
63. J.M. Taube, A. Klein, and J.R. Brahmer 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 20 2014 5064 5074
64. M.K. Callahan, C.E. Horak, and M.A. Curran Peripheral and tumor immune correlates in patients with advanced melanoma treated with combination nivolumab (anti-PD-1, BMS-936558, ONO-4538) and ipilimumab ASCO Meeting Abstracts 31 2013 3003
65. R. Kefford, A. Ribas, and O. Hamid Clinical efficacy and correlation with tumor PD-L1 expression in patients (pts) with melanoma (MEL) treated with the anti-PD-1 monoclonal antibody MK-3475 ASCO Meeting Abstracts 32 2014 3005
66. M. Sznol, and L. Chen Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer Clin Cancer Res 19 2013 1021 1034
67. S.M. Mangsbo, L.C. Sandin, K. Anger, A.J. Korman, A. Loskog, and T.H. Totterman Enhanced tumor eradication by combining CTLA-4 or PD-1 blockade with CpG therapy J Immunother 33 2010 225 235
68. J.S. Weber, K.C. Kahler, and A. Hauschild Management of immune-related adverse events and kinetics of response with ipilimumab J Clin Oncol 30 2012 2691 2697
69. A.M. Di Giacomo, M. Biagioli, and M. Maio The emerging toxicity profiles of anti-CTLA-4 antibodies across clinical indications Semin Oncol 37 2010 499 507
70. S.G. Downey, J.A. Klapper, and F.O. Smith Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade Clin Cancer Res 13 2007 6681 6688
71. A. Tarhini, E. Lo, and D.R. Minor Releasing the brake on the immune system: ipilimumab in melanoma and other tumors Cancer Biother Radiopharm 25 2010 601 613
72. P.A. Ascierto, E. Simeone, and V.C. Sileni Clinical experience with ipilimumab 3 mg/kg: real-world efficacy and safety data from an expanded access programme cohort J Transl Med 12 2014 116
73. D. Berman, S.M. Parker, and J. Siegel Blockade of cytotoxic T-lymphocyte antigen-4 by ipilimumab results in dysregulation of gastrointestinal immunity in patients with advanced melanoma Cancer Immun 10 2010 11
74. A.M. Di Giacomo, R. Danielli, and M. Guidoboni Therapeutic efficacy of ipilimumab, an anti-CTLA-4 monoclonal antibody, in patients with metastatic melanoma unresponsive to prior systemic treatments: clinical and immunological evidence from three patient cases Cancer Immunol Immunother 58 2009 1297 1306
75. V. Shahabi, D. Berman, and S.D. Chasalow Gene expression profiling of whole blood in ipilimumab-treated patients for identification of potential biomarkers of immune-related gastrointestinal adverse events J Transl Med 11 2013 75
76. M.K. Callahan, A. Yang, and S. Tandon Evaluation of serum IL-17 levels during ipilimumab therapy: correlation with colitis ASCO Meeting Abstracts 29 2011 2505
77. K. Schindler, K. Harmankaya, and D. Kuk Correlation of absolute and relative eosinophil counts with immune-related adverse events in melanoma patients treated with ipilimumab ASCO Meeting Abstracts 32 2014 9096
78. H. Ueda, J.M. Howson, and L. Esposito Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease Nature 423 2003 506 511
79. W.B. Breunis, E. Tarazona-Santos, R. Chen, M. Kiley, S.A. Rosenberg, and S.J. Chanock Influence of cytotoxic T lymphocyte-associated antigen 4 (CTLA4) common polymorphisms on outcome in treatment of melanoma patients with CTLA-4 blockade J Immunother 31 2008 586 590
80. C. Robert, L. Thomas, and I. Bondarenko Ipilimumab plus dacarbazine for previously untreated metastatic melanoma N Engl J Med 364 2011 2517 2526
81. J. Yuan, J. Zhou, and Z. Dong Pretreatment serum VEGF is associated with clinical response and overall survival in advanced melanoma patients treated with ipilimumab Cancer Immunol Res 2 2014 127 132
82. P.F. Robbins, Y.C. Lu, and M. El-Gamil Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells Nat Med 19 2013 747 752
83. N. van Rooij, M.M. van Buuren, and D. Philips Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma J Clin Oncol 31 2013 e439 e442
84. S. Viaud, R. Daillere, and T. Yamazaki Why should we need the gut microbiota to respond to cancer therapies? Oncoimmunology 3 2014 e27574
85. S. Viaud, R. Daillere, and I.G. Boneca Harnessing the Intestinal Microbiome for Optimal Therapeutic Immunomodulation Cancer Res 74 2014 4217 4221
86. S. Viaud, F. Saccheri, and G. Mignot The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide Science 342 2013 971 976
87. P.A. Ott, F.S. Hodi, and C. Robert CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients Clin Cancer Res 19 2013 5300 5309
88. T. Okazaki, S. Chikuma, Y. Iwai, S. Fagarasan, and T. Honjo A rheostat for immune responses: the unique properties of PD-1 and their advantages for clinical application Nat Immunol 14 2013 1212 1218
89. L. Robert, C. Harview, and R. Emerson Distinct immunological mechanisms of CTLA-4 and PD-1 blockade revealed by analyzing TCR usage in blood lymphocytes Oncoimmunology 3 2014 e29244