Genetic risk analysis of a patient with fulminant autoimmune type 1 diabetes mellitus secondary to combination ipilimumab and nivolumab immunotherapy

Journal for ImmunoTherapy of Cancer

Volumn 4, Issue 1, 2016, Pages

  Lowe, Jared R ^a   Perry, Daniel J ^b   Salama, April K S ^a   Mathews, Clayton E ^b   Moss, Larry G ^a   Hanks, Brent A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Advanced melanoma; Autoimmune endocrinopathy; Genetic risk analysis; HLA risk allele; Ipilimumab; Nivolumab; Single nucleotide polymorphism; Type I diabetes

Indexed keywords

GLUTAMATE DECARBOXYLASE; IPILIMUMAB; LEVOTHYROXINE; LIOTHYRONINE; LOPERAMIDE; METHYLPREDNISOLONE; METOPROLOL; MICROSOME ANTIBODY; NIVOLUMAB; PREDNISONE; THYROTROPIN; THYROTROPIN RECEPTOR ANTIBODY; THYROXINE;

ADULT; ARTICLE; AUTOIMMUNE THYROIDITIS; CANCER IMMUNOTHERAPY; CASE REPORT; COLITIS; DIABETIC KETOACIDOSIS; DIARRHEA; DRUG DOSE REDUCTION; DRUG SUBSTITUTION; DRUG WITHDRAWAL; FINE NEEDLE ASPIRATION BIOPSY; GENETIC PREDISPOSITION; GENETIC RISK; HOT FLUSH; HUMAN; HUMAN TISSUE; HYPERTRANSAMINASEMIA; HYPOTHYROIDISM; INSULIN DEPENDENT DIABETES MELLITUS; LIVER TOXICITY; LYMPH NODE DISSECTION; MALE; MELANOMA; MIDDLE AGED; MULTIPLE CYCLE TREATMENT; MYALGIA; NAUSEA AND VOMITING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RASH; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; TACHYCARDIA; WEAKNESS;

EID: 85006761390     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-016-0196-z     Document Type: Article

References (40)

1. Kong YCM, Wei WZ, Tomer Y. Opportunistic autoimmune disorders: From immunotherapy to immune dysregulation. Ann N Y Acad Sci. 2010;1183:222-36.
2. Haanen JBAG, van Thienen H, Blank CU. Toxicity Patterns With Immunomodulating Antibodies and Their Combinations. Semin Oncol. 2015;42:423-8.
3. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJM, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbé C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363:711-23.
4. Topalian SL, Hodi FS, Brahmer JR, Gettinger S, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, McMiller TL, Xu H, Korman AJ, Jure-Kunkel M, Agrawal S, McDonald D, Kollia GD, Gupta A, Wigginton JM, Sznol M. Safety, Activity, and Immune Correlates of Anti-PD-1 Antibody in Cancer. New Engl J Med. 2012;366:2443-54.
5. Kong YCM, Flynn JC. Opportunistic autoimmune disorders potentiated by immune-checkpoint inhibitors anti-CTLA-4 and anti-PD-1. Front Immunol. 2014;5(May):1-8.
6. Nivolumab (Opdivo®). Prescribing Information. Princeton: Bristol-Meyers Squibb Company; 2015.
7. Seiwert TY, Burtness B, Mehra R, Weiss J, Berger R, Eder JP, Heath K, McClanahan T, Lunceford J, Gause C, Cheng JD, Chow LQ. Safety and clinical activity of pembrolizumab for treatment of recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-012): an open-label, multicentre, phase 1b trial. Lancet Oncol. 2016;17:956-65.
8. Weber J. Ipilimumab: Controversies in its development, utility and autoimmune adverse events. Cancer Immunol Immunother. 2009;58:823-30.
9. Torino F, Barnabei A, De Vecchis L, Salvatori R, Corsello SM. Hypophysitis induced by monoclonal antibodies to cytotoxic T lymphocyte antigen 4: challenges from a new cause of a rare disease. Oncologist. 2012;17:525-35.
10. Gaudy C, Clévy C, Monestier S, Dubois N, Préau Y, Mallet S, Richard M-A, Grob J-J, Valéro R, Béliard S. Anti-PD1 Pembrolizumab Can Induce Exceptional Fulminant Type 1 Diabetes. Diabetes Care. 2015;38(November):e182-3.
11. Hughes J, Vudattu N, Sznol M, Gettinger S, Kluger H, Lupsa B, Herold KC. Precipitation of autoimmune diabetes with anti-PD-1 immunotherapy. Diabetes Care. 2015;38:e55-7.
12. Brahmer JR, Tykodi SS, Chow LQM, Hwu W-J, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM. Safety and Activity of Anti-PD-L1 Antibody in Patients with Advanced Cancer. N Engl J Med. 2012;366:2455-65.
13. Okamoto M, Okamoto M, Gotoh K, Masaki T, Ozeki Y, Ando H, Anai M, Sato A, Yoshida Y, Ueda S, Kakuma T, Shibata H. Fulminant Type 1 Diabetes Mellitus with Anti-programmed Cell Death-1 Therapy. J Diabetes Investig. 2016;7:1-4.
14. Miyoshi Y, Ogawa O, Oyama Y. Nivolumab, an Anti-Programmed Cell Death-1 Antibody, Induces Fulminant Type 1 Diabetes. Tohoku J Exp Med. 2016;239:155-8.
15. Martin-liberal J, Furness AJ, Joshi K, Peggs KS, Quezada SA, Larkin J. Anti-programmed cell death-1 therapy and insulin-dependent diabetes: a case report. Cancer Immunol Immunother. 2015;64:765-7.
16. Oram RA, Patel K, Hill A, Shields B, McDonald TJ, Jones A, Hattersley AT, Weedon MN. A Type 1 Diabetes Genetic Risk Score Can Aid Discrimination Between Type 1 and Type 2 Diabetes in Young Adults. Diabetes Care. 2015;39(March):337-44.
17. Iwama S, De Remigis A, Callahan MK, Slovin SF, Wolchok JD, Caturegli P. Pituitary Expression of CTLA-4 Mediates Hypophysitis Secondary to Administration of CTLA-4 Blocking Antibody. Sci Transl Med. 2014;6:230ra45.
18. Ziegler A-G. Prediction and Pathogenesis in Type 1. Diabetes. 2011;32:206-23.
19. Jaberi-Douraki M, Liu SWS, Pietropaolo M, Khadra A. Autoimmune responses in T1DM: quantitative methods to understand onset, progression, and prevention of disease. Pediatr Diabetes. 2014;15:162-74.
20. Zimmet P, Tuomi T, Mackay IR, Rowley MJ, Knowles W, Cohen M, Lang DA. Latent Autoimmune Diabetes Mellitus in Adults (LADA): the Role of Antibodies to Glutamic Acid Decarboxylase in Diagnosis and Prediction of Insulin Dependency. Diabet Med. 1994;11:299-303.
21. Imagawa A, Hanafusa T, Awata T, Ikegami H, Uchigata Y, Osawa H, Kawasaki E, Kawabata Y, Kobayashi T, Shimada A, Shimizu I, Takahashi K, Nagata M, Makino H, Maruyama T. Report of the Committee of the Japan Diabetes Society on the Research of Fulminant and Acute-onset Type 1 Diabetes Mellitus: New diagnostic criteria of fulminant type 1 diabetes mellitus (2012). J Diabetes Investig. 2012;3:536-9.
22. Imagawa A, Hanafusa T. Pathogenesis of Fulminant Type 1 Diabetes. Rev Diabet Stud. 2006;3:169-77.
23. Szablewski L. Role of immune system in type 1 diabetes mellitus pathogenesis. Int Immunopharmacol. 2014;22:182-91.
24. Leiter E. NOD mice and related strains: origins, husbandry, and biology introduction. In: Leiter E, Atkinson M, editors. NOD Mice and Related Strains: Research Applications in Diabetes, AIDS, Cancer, and Other Diseases. Austin: R. G. Landes Company; 1998. p. 1-26.
25. Kochupurakkal NM, Kruger AJ, Tripathi S, Zhu B, Adams LT, Rainbow DB, Rossini A, Greiner DL, Sayegh MH, Wicker LS, Guleria I. Blockade of the programmed death-1 (PD1) pathway undermines potent genetic protection from type 1 diabetes. PLoS One. 2014;9:e89561.
26. Ansari MJI, Salama AD, Chitnis T, Smith RN, Yagita H, Akiba H, Yamazaki T, Azuma M, Iwai H, Khoury SJ, Auchincloss H, Sayegh MH. The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med. 2003;198:63-9.
27. Waterhouse P, Penninger JM, Timms E, Wakeham A. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270(80-):985.
28. Fife BT, Pauken KE, Eagar TN, Obu T, Wu J, Tang Q, Azuma M, Krummel MF, Bluestone J. Interactions between programmed death-1 and programmed death ligand-1 promote tolerance by blocking the T cell receptor- induced stop signal. Nat Immunol. 2009;10:1185.
29. Tsutsumi Y, Jie X, Ihara K, Nomura A, Kanemitsu S, Takada H, Hara T. Phenotypic and genetic analyses of T-cell-mediated immunoregulation in patients with Type 1 diabetes. Diabet Med. 2006;23:1145-50.
30. Fife BT, Bluestone JA. Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev. 2008;224:166-82.
31. Wang J, Liu L, Ma J, Sun F, Zhao Z, Gu M. Common variants on cytotoxic T lymphocyte antigen-4 polymorphisms contributes to type 1 diabetes susceptibility: Evidence based on 58 studies. PLoS One. 2014;9:1-9.
32. Momin S, Flores S, Angel BB, Codner DE, Carrasco PE, Perez-Bravo F. Interactions between programmed death 1 (PD-1) and cytotoxic T lymphocyte antigen 4 (CTLA-4) gene polymorphisms in type 1 diabetes. Diabetes Res Clin Pract. 2009;83:289-94.
33. Nielsen C, Hansen D, Husby S, Jacobsen BB, Lillevang ST. Association of a putative regulatory polymorphism in the PD-1 gene with susceptibility to type 1 diabetes. Tissue Antigens. 2003;62:492-7.
34. El Wafai RJ, Chmaisse HN, Makki RF, Fakhoury H. Association of HLA Class II Alleles and CTLA-4 Polymorphism with Type 1 Diabetes. Saudi J Kidney Dis Transplant. 2011;22:273-81.
35. Klitz W, Bugawan TL, Panelo A, Solfelix CM, Buzzetti R, Pozzilli P, Steiner L, Alejandrino M, Erlich HA. Association of CTLA-4 variation with type I diabetes in Filipinos. Immunogenetics. 2002;54:310-3.
36. Noble JA, Valdes AM. Genetics of the HLA Region in the Prediction of Type 1 Diabetes. Curr Diab Rep. 2011;11:533-42.
37. Hofmann L, Forschner A, Loquai C, Goldinger SM, Zimmer L, Ugurel S, Schmidgen MI, Gutzmer R, Utikal JS, Hassel JC, Meier F, Tietze JK, Thomas I, Weishaupt C, Leverkus M, Wahl R, Dietrich U, Garbe C, Kirchberger MC, Eigentler T, Berking C, Gesierich A, Krackhardt AM, Schadendorf D, Schuler G, Dummer R, Heinzerling LM. Cutaneous, gastrointestinal, hepatic, endocrine, and renal side-effects of anti-PD-1 therapy. Eur J Cancer. 2016;60:190-209.
38. Erlich H, Valdes AM, Noble J, Carlson J, Varney M, Concannon P, Mychaleckyj JC, Todd J, Bonella P, Fear AL, Lavant E, Louey A, Moonsamy P, Consortium T 1 DG. HLA DR-DQ Haplotypes and Genotypes and Type 1 Diabetes Risk. Diabetes. 2008;57:1084-92.
39. Valdes AM, Thomson G, Graham J, Zarghami M, McNeney B, Kockum I, Smith A, Lathrop M, Steenkiste AR, Dorman JS, Noble JA, Hansen JA, Pugliese A, Lernmark A, Swedish Childhood Study Group, Diabetes Incidence in Sweden Study Group, Type 1 Diabetes Component of the 13th International Histocompatibility Working Group. D6S265*15 marks a DRB1*15, DQB1*0602 haplotype associated with attenuated protection from type 1 diabetes mellitus. Diabetologia. 2005;48:2540-3.
40. Wolchok JD, Kluger H, Callahan MK, Postow M, Rizvi N, Lesokhin AM, Segal NH, Ariyan CE, Gordon R-A, Reed K, Burke MM, Caldwell A, Kronenberg S, Agunwamba BU, Zhang X, Lowy I, Inzunza HD, Feely W, Horak CE, Hong Q, Korman AJ, Wigginton JM, Gupta A, Sznol M. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369:122-33.