Inflammatory bowel disease and cancer response due to anti-CTLA-4: is it in the flora?

Seminars in Immunopathology

Volumn 39, Issue 3, 2017, Pages 327-331

  Carbonnel, Franck ^a,b   Soularue, Emilie ^a,b   Coutzac, Clélia ^c   Chaput, Nathalie ^b,c   Mateus, Christine ^d   Lepage, Patricia ^b   Robert, Caroline ^d  

^a BICÊTRE HOSPITAL   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c CNRS UMS3655   (France)

^d INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IPILIMUMAB; MONOCLONAL ANTIBODY;

CANCER IMMUNOTHERAPY; CLINICAL FEATURE; CLINICAL STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE MARKER; ENTEROCOLITIS; HOMEOSTASIS; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; INTESTINE FUNCTION; MALIGNANT NEOPLASM; NONHUMAN; PARALLEL DESIGN; PATHOPHYSIOLOGY; REGULATORY T LYMPHOCYTE; REVIEW; ANTAGONISTS AND INHIBITORS; COLITIS; COMPLICATION; DRUG EFFECTS; IMMUNOLOGY; IMMUNOMODULATION; IMMUNOTHERAPY; INFLAMMATORY BOWEL DISEASES; INTESTINE; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; PROCEDURES;

ANTIBODIES, MONOCLONAL; COLITIS; CTLA-4 ANTIGEN; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; INFLAMMATORY BOWEL DISEASES; INTESTINES; MOLECULAR TARGETED THERAPY; NEOPLASMS;

EID: 85009461435     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-016-0613-x     Document Type: Review

References (55)

1. Hodi FS, O’Day SJ, Sosman JA et al (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711–723
2. Robert C, Thomas L, Bondarenko I et al (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364(26):2517–2526
3. Lynch TJ, Bondarenko I, Luft A et al (2012) Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol 30(17):2046–2054
4. Hodi FS, Mihm MC, Soiffer RJ et al (2003) Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci U S A 100(8):4712–4717
5. Hodi FS, Butler M, Oble DA et al (2008) 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(8):3005–3010
6. Yang JC, Hughes M, Kammula U et al (2007) Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J Immunother 30(8):825–830
7. Fong L, Kwek SS, O’Brien S et al (2009) Potentiating endogenous antitumor immunity to prostate cancer through combination immunotherapy with CTLA4 blockade and GM-CSF. Cancer Res 69(2):609–615
8. Kwon ED, Drake CG, Scher HI et al (2014) Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. Lancet Oncol 15(7):700–712
9. Tarhini AA, Cherian J, Moschos SJ et al (2012) Safety and efficacy of combination immunotherapy with interferon alfa-2b and tremelimumab in patients with stage IV melanoma. J Clin Oncol 30(3):322–328
10. Kirkwood JM, Lorigan P, Hersey P et al (2010) Phase II trial of tremelimumab (CP-675,206) in patients with advanced refractory or relapsed melanoma. Clin Cancer Res 16(3):1042–1048
11. Ribas A, Kefford R, Marshall MA et al (2013) Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol 31(5):616–622
12. Calabrò L, Morra A, Fonsatti E et al (2013) Tremelimumab for patients with chemotherapy-resistant advanced malignant mesothelioma: an open-label, single-arm, phase 2 trial. Lancet Oncol 14(11):1104–1111
13. McNeel DG, Smith HA, Eickhoff JC et al (2012) Phase I trial of tremelimumab in combination with short-term androgen deprivation in patients with PSA-recurrent prostate cancer. Cancer Immunol Immunother 61(7):1137–1147
14. Aglietta M, Barone C, Sawyer MB et al (2014) A phase I dose escalation trial of tremelimumab (CP-675,206) in combination with gemcitabine in chemotherapy-naive patients with metastatic pancreatic cancer. Ann Oncol 25(9):1750–1755
15. Sangro B, Gomez-Martin C, De la Mata M et al (2013) A clinical trial of CTLA-4 blockade with tremelimumab in patients with hepatocellular carcinoma and chronic hepatitis C. J Hepatol 59(1):81–88
16. Weber JS, Kähler KC, Hauschild A (2012) Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol 30(21):2691–2697
17. Beck KE et al (2006) Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 24(15):2283–2289
18. Gupta A, De Felice KM, Loftus EV, Khanna S (2015) Systematic review: colitis associated with anti-CTLA-4 therapy. Aliment Pharmacol Ther 42(4):406–417
19. Marthey L et al (2016) Cancer immunotherapy with anti-CTLA-4 monoclonal antibodies induces an inflammatory bowel disease. J Crohns Colitis 10(4):395–401
20. Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M, Larkin J, Lorigan P, Neyns B, Blank CU, Hamid O, Mateus C, Shapira-Frommer R, Kosh M, Zhou H, Ibrahim N, Ebbinghaus S, Ribas A (2015) Keynote-006 investigators. Pembrolizumab versus Ipilimumab in Advanced Melanoma. N Engl J Med 372(26):2521–2532
21. Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, Ferrucci PF, Hill A, Wagstaff J, Carlino MS, Haanen JB, Maio M, Marquez-Rodas I, McArthur GA, Ascierto PA, Long GV, Callahan MK, Postow MA, Grossmann K, Sznol M, Dreno B, Bastholt L, Yang A, Rollin LM, Horak C, Hodi FS, Wolchok JD (2015) Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 373(1):23–34
22. Boutros C, Tarhini A, Routier E, Lambotte O, Ladurie FL, Carbonnel F, Izzeddine H, Marabelle A, Champiat S, Berdelou A, Lanoy E, Texier M, Libenciuc C, Eggermont AM, Soria JC, Mateus C, Robert C (2016) Safety profiles of anti-CTLA-4 and anti-PD-1 antibodies alone and in combination. Nat Rev Clin Oncol 13(8):473–486
23. Genovese MC, Becker JC, Schiff M, Luggen M, Sherrer Y, Kremer J, Birbara C, Box J, Natarajan K, Nuamah I, Li T, Aranda R, Hagerty DT, Dougados M (2005) Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 353(11):1114–1123
24. Sandborn WJ, Colombel JF, Sands BE, Rutgeerts P, Targan SR, Panaccione R, Bressler B, Geboes K, Schreiber S, Aranda R, Gujrathi S, Luo A, Peng Y, Salter-Cid L, Hanauer SB (2012) Abatacept for Crohn’s disease and ulcerative colitis. Gastroenterology 143(1):62–69
25. Freeman GJ, Gribben JG, Boussiotis VA, Ng JW, Restivo VA, Lombard LA, Gray SS, Nadler LM (1993) Cloning of B7-2: a CTLA-4 counter-receptor that costimulates human T cell proliferation. Science 262(5135):909–911
26. Azuma M, Ito D, Yagita H, Okumura K, Phillips JH, Lanier LL, Somoza C (1993) B70 antigen is a second ligand for CTLA-4 and CD28. Nature 366(6450):76–79
27. Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, Schmidt EM, Baker J, Jeffery LE, Kaur S, Briggs Z, Hou TZ, Futter CE, Anderson G, Walker LS, Sansom DM (2011) Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 332(6029):600–603
28. Krummel MF, Allison JP (1995) CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 182(2):459–465
29. Mc Coy KD, Le Gros G (1999) The role of CTLA-4 in the regulation of T cell immune responses. Immunol Cell Biol 77(1):1–10
30. Sansom DM, Walker LS (2006) The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology. Immunol Rev 212:131–148
31. Bulliard Y, Jolicoeur R, Windman M, Rue SM, Ettenberg S, Knee DA, Wilson NS, Dranoff G, Brogdon JL (2013) Activating Fc γ receptors contribute to the antitumor activities of immunoregulatory receptor-targeting antibodies. J Exp Med 210(9):1685–1693
32. Wang CJ, Kenefeck R, Wardzinski L, Attridge K, Manzotti C, Schmidt EM, Qureshi OS, Sansom DM, Walker LS (2012) Cutting edge: cell-extrinsic immune regulation by CTLA-4 expressed on conventional T cells. J Immunol 189(3):1118–1122
33. Romano E, Kusio-Kobialka M, Foukas PG, Baumgaertner P, Meyer C, Ballabeni P, Michielin O, Weide B, Romero P, Speiser DE (2015) Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc Natl Acad Sci U S A 112(19):6140–6145
34. Selby MJ, Engelhardt JJ, Quigley M, Henning KA, Chen T, Srinivasan M, Korman AJ (2013) Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells. Cancer Immunol Res 1(1):32–42
35. Peggs KS (2009) Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med 206(8):1717–25
36. Marabelle A, Kohrt H, Sagiv-Barfi I, Ajami B, Axtell RC, Zhou G, Rajapaksa R, Green MR, Torchia J, Brody J, Luong R, Rosenblum MD, Steinman L, Levitsky HI, Tse V, Levy R (2013) Depleting tumor-specific tregs at a single site eradicates disseminated tumors. J Clin Invest 123(6):2447–2463
37. Pardoll DM (2012) The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12(4):252–264
38. Postow MA, Callahan MK, Wolchok JD (2015) Immune checkpoint blockade in cancer therapy. J Clin Oncol 33(17):1974–1982
39. Read S, Greenwald R, Izcue A, Robinson N, Mandelbrot D, Francisco L, Sharpe AH, Powrie F (2006) Blockade of CTLA-4 on CD4 + CD25+ regulatory T cells abrogates their function in vivo. J Immunol 177(7):4376–4383
40. Barnes MJ, Griseri T, Johnson AM et al (2013) CTLA-4 promotes Foxp3 induction and regulatory T cell accumulation in the intestinal lamina propria. Mucosal Immunol 6(2):324–334
41. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, Santacruz N, Peterson DA, Stappenbeck TS, Hsieh CS (2011) Peripheral education of the immune system by colonic commensal microbiota. Nature 478(7368):250–254
42. Zeissig S, Petersen BS, Tomczak M, Melum E, Huc-Claustre E, Dougan SK, Laerdahl JK, Stade B, Forster M, Schreiber S, Weir D, Leichtner AM, Franke A, Blumberg RS (2015) Early-onset Crohn’s disease and autoimmunity associated with a variant in CTLA-4. Gut 64(12):1889–1897
43. Schubert D, Bode C, Kenefeck R, Hou TZ, Wing JB, Kennedy A, Bulashevska A, Petersen BS, Schäffer AA, Grüning BA, Unger S, Frede N, Baumann U, Witte T, Schmidt RE, Dueckers G, Niehues T, Seneviratne S, Kanariou M, Speckmann C, Ehl S, Rensing-Ehl A, Warnatz K, Rakhmanov M, Thimme R, Hasselblatt P, Emmerich F, Cathomen T, Backofen R, Fisch P, Seidl M, May A, Schmitt-Graeff A, Ikemizu S, Salzer U, Franke A, Sakaguchi S, Walker LS, Sansom DM, Grimbacher B (2014) Autosomal dominant immune dysregulation syndrome in humans with CTLA4 mutations. Nat Med 20(12):1410–1416
44. Kuehn HS, Ouyang W, Lo B, Deenick EK, Niemela JE, Avery DT, Schickel JN, Tran DQ, Stoddard J, Zhang Y, Frucht DM, Dumitriu B, Scheinberg P, Folio LR, Frein CA, Price S, Koh C, Heller T, Seroogy CM, Huttenlocher A, Rao VK, Su HC, Kleiner D, Notarangelo LD, Rampertaap Y, Olivier KN, McElwee J, Hughes J, Pittaluga S, Oliveira JB, Meffre E, Fleisher TA, Holland SM, Lenardo MJ, Tangye SG, Uzel G (2014) Immune dysregulation in human subjects with heterozygous germline mutations in CTLA4. Science 345(6204):1623–1627
45. Maynard CL, Elson CO, Hatton RD, Weaver CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489(7415):231–241
46. Jostins L (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491(7422):119–24
47. Chassaing B, Darfeuille-Michaud A (2011) The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology 140(6):1720–1728
48. Taurog JD, Richardson JA, Croft JT, Zhou M, Simmons WA et al (1994) The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med 180:2359–2364
49. Iqbal N, Oliver JR, Wagner FH, Lazenby AS, Elson CO, Weaver CT (2002) T helper 1 and T helper 2 cells are pathogenic in an antigen-specific model of colitis. J Exp Med 195:71–84
50. Cong Y, Brandwein SL, McCabe RP, Lazenby A, Birkenmeier EH et al (1998) CD4+ T cells reactive to enteric bacterial antigens in spontaneously colitic C3H/HeJBir mice: increased T helper cell type 1 response and ability to transfer disease. J Exp Med 187:855–864
51. Vernier G, Sendid B, Poulain D, Colombel JF (2004) Relevance of serologic studies in inflammatory bowel disease. Curr Gastroenterol Rep 6(6):482–487
52. Calderón-Gómez E, Bassolas-Molina H, Mora-Buch R, Dotti I, Planell N, Esteller M, Gallego M, Martí M, Garcia-Martín C, Martínez-Torró C, Ordás I, Singh S, Panés J, Benítez-Ribas D, Salas A (2016) Commensal-specific CD4(+) cells from patients with Crohn’s disease have a T-helper 17 inflammatory profile. Gastroenterology 151(3):489–500
53. Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH (2007) Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 131(1):33–45
54. Dubin K et al (2016) Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis. Nat Commun 7:10391
55. Vétizou M et al (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350(6264):1079–1084