Endocrine immune-related adverse effects of immune-checkpoint inhibitors

References

• Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science. 1996;271(5256):1734–1736. doi: 10.1126/science.271.5256.1734
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–264. doi: 10.1038/nrc3239
   PubMed Web of Science ®Google Scholar
• Freeman GJ, Long AJ, Iwai Y, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med. 2000;192(7):1027–1034. doi: 10.1084/jem.192.7.1027
   PubMed Web of Science ®Google Scholar
• Ljunggren HG, Jonsson R, Höglund P, et al. Seminal immunologic discoveries with direct clinical implications: the 2018 nobel prize in physiology or medicine honours discoveries in cancer immunotherapy. Scand J Immunol. 2018;88(6):e12731. doi: 10.1111/sji.12731
   PubMed Web of Science ®Google Scholar
• Iwai Y, Hamanishi J, Chamoto K, et al. Cancer immunotherapies targeting the PD-1 signaling pathway. J Biomed Sci. 2017;24(1):26. doi: 10.1186/s12929-017-0329-9
   PubMedGoogle Scholar
• Sacher AG, Gandhi L. Biomarkers for the clinical use of PD-1/PD-L1 inhibitors in non-small-cell lung cancer: a review. JAMA Oncol. 2016;2(9):1217–1222. doi: 10.1001/jamaoncol.2016.0639
   PubMed Web of Science ®Google Scholar
• Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348(6230):56–61. doi: 10.1126/science.aaa8172
   PubMed Web of Science ®Google Scholar
• Elia G, Ferrari SM, Galdiero MR, et al. New insight in endocrine-related adverse events associated to immune checkpoint blockade. Best Pract Res Clin Endocrinol Metab. 2020;34(1):101370. doi: 10.1016/j.beem.2019.101370
   PubMed Web of Science ®Google Scholar
• Neel BG, Gu H, Pao L. The ‘Shp’ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci. 2003;28(6):284–293. doi: 10.1016/S0968-0004(03)00091-4
   PubMed Web of Science ®Google Scholar
• Ahmadzadeh M, Johnson LA, Heemskerk B, et al. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood. 2009;114(8):1537–1544. doi: 10.1182/blood-2008-12-195792
   PubMed Web of Science ®Google Scholar
• Staron MM, Gray SM, Marshall HD, et al. The transcription factor FoxO1 sustains expression of the inhibitory receptor PD-1 and survival of antiviral CD8(+) T cells during chronic infection. Immunity. 2014 Nov 20;41(5):802–814. doi: 10.1016/j.immuni.2014.10.013
   PubMed Web of Science ®Google Scholar
• Xiao G, Deng A, Liu H, et al. Activator protein 1 suppresses antitumor T-cell function via the induction of programmed death 1. Proc Natl Acad Sci U S A. 2012;109(38):15419–15424. doi: 10.1073/pnas.1206370109
   PubMed Web of Science ®Google Scholar
• Bally AP, Lu P, Tang Y, et al. NF-κB regulates PD-1 expression in macrophages. J Immunol. 2015;194(9):4545–4554. doi: 10.4049/jimmunol.1402550
   PubMed Web of Science ®Google Scholar
• Topalian SL, Drake CG, Pardoll DM. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol. 2013;24(2):207–212. doi: 10.1016/j.coi.2011.12.009
   Web of Science ®Google Scholar
• Lu P, Youngblood BA, Austin JW, et al. Blimp-1 represses CD8 T cell expression of PD-1 using a feed-forward transcriptional circuit during acute viral infection. J Exp Med. 2014;211(3):515–527. doi: 10.1084/jem.20130208
   PubMed Web of Science ®Google Scholar
• Voron T, Colussi O, Marcheteau E, et al. VEGF-A modulates expression of inhibitory checkpoints on CD8+ T cells in tumors. J Exp Med. 2015;212(2):139–148. doi: 10.1084/jem.20140559
   PubMed Web of Science ®Google Scholar
• Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev. 2010;236(1):219–242. doi: 10.1111/j.1600-065X.2010.00923;.x
   PubMed Web of Science ®Google Scholar
• Francisco LM, Salinas VH, Brown KE, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med. 2009;206(13):3015–3029. doi: 10.1084/jem.20090847
   PubMed Web of Science ®Google Scholar
• Ohaegbulam KC, Assal A, Lazar-Molnar E, et al. Human cancer immunotherapy with antibodies to the PD-1 and PD-L1 pathway. Trends Mol Med. 2015;21(1):24–33. doi: 10.1016/j.molmed.2014.10.009
   PubMed Web of Science ®Google Scholar
• Bellucci R, Martin A, Bommarito D, et al. Interferon-γ-induced activation of JAK1 and JAK2 suppresses tumor cell susceptibility to NK cells through upregulation of PD-L1 expression. Oncoimmunology. 2015;4(6):e1008824. doi: 10.1080/2162402X.2015.1008824
   PubMed Web of Science ®Google Scholar
• Abiko K, Matsumura N, Hamanishi J, et al. IFN-γ from lymphocytes induces PD-L1 expression and promotes progression of ovarian cancer. Br J Cancer. 2015;112(9):1501–1509. doi: 10.1038/bjc.2015.101
   PubMed Web of Science ®Google Scholar
• Garcia-Diaz A, Shin DS, Moreno BH, et al. Interferon receptor signaling pathways regulating PD-L1 and PD-L2 expression. Cell Rep. 2017;19(6):1189–1201. doi: 10.1016/j.celrep.2017.04.031
   PubMed Web of Science ®Google Scholar
• Chen J, Jiang CC, Jin L, et al. Regulation of PD-L1: a novel role of pro-survival signalling in cancer. Ann Oncol. 2016;27(3):409–416. doi: 10.1093/annonc/mdv615
   PubMed Web of Science ®Google Scholar
• Sheppard KA, Fitz LJ, Lee JM, et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett. 2004;574(1–3):37–41. doi: 10.1016/j.febslet.2004.07.083
   PubMed Web of Science ®Google Scholar
• Patsoukis N, Li L, Sari D, et al. PD-1 increases PTEN phosphatase activity while decreasing PTEN protein stability by inhibiting casein kinase 2. Mol Cell Biol. 2013;33(16):3091–3098. doi: 10.1128/MCB.00319-13
   PubMed Web of Science ®Google Scholar
• Schwartz JC, Zhang X, Fedorov AA, et al. Structural basis for co-stimulation by the human CTLA-4/B7-2 complex. Nature. 2001;410(6828):604–608. doi: 10.1038/35069112
   PubMed Web of Science ®Google Scholar
• Wing K, Onishi Y, Prieto-Martin P, et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science. 2008;322(5899):271–275. doi: 10.1126/science.1160062
   PubMed Web of Science ®Google Scholar
• Yokosuka T, Kobayashi W, Takamatsu M, et al. Spatiotemporal basis of CTLA-4 costimulatory molecule-mediated negative regulation of T cell activation. Immunity. 2010;33(3):326–339. doi: 10.1016/j.immuni.2010.09.006
   PubMed Web of Science ®Google Scholar
• Takahashi T, Tagami T, Yamazaki S, et al. Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med. 2000;192(2):303–310. doi: 10.1084/jem.192.2.303
   PubMed Web of Science ®Google Scholar
• Parry RV, Chemnitz JM, Frauwirth KA, et al. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol. 2005;25(21):9543–9553. doi: 10.1128/MCB.25.21.9543-9553.2005
   PubMed Web of Science ®Google Scholar
• Postow MA, Chesney J, Pavlick AC, et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med. 2015;372(21):2006–2017. doi: 10.1056/NEJMoa1414428
   PubMed Web of Science ®Google Scholar
• Selby M, Engelhardt J, Lu LS, et al. Antitumor activity of concurrent blockade of immune checkpoint molecules CTLA-4 and PD-1 in preclinical models. J Clin Oncol. 2013;31(15_suppl):3061. doi: 10.1200/jco.2013.31.15_suppl.3061
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122–133. doi: 10.1056/NEJMoa1302369
   PubMed Web of Science ®Google Scholar
• Adler BL, Pezhouh MK, Kim A, et al. Histopathological and immunophenotypic features of ipilimumab-associated colitis compared to ulcerative colitis. J Intern Med. 2018;283(6):568–577. doi: 10.1111/joim.12744
   PubMed Web of Science ®Google Scholar
• Chan KK, Bass AR. Autoimmune complications of immunotherapy: pathophysiology and management. BMJ. 2020;369:m736. doi: 10.1136/bmj.m736
   PubMedGoogle Scholar
• Zhai Y, Ye X, Hu F, et al. Endocrine toxicity of immune checkpoint inhibitors: a real-world study leveraging US Food and Drug administration adverse events reporting system. J Immunother Cancer. 2019;7(1):286. doi: 10.1186/s40425-019-0754-2
   PubMed Web of Science ®Google Scholar
• Barroso-Sousa R, Barry WT, Garrido-Castro AC, et al. Incidence of endocrine dysfunction following the use of different immune checkpoint inhibitor regimens: a systematic review and meta-analysis. JAMA Oncol. 2018;4(2):173–182. doi: 10.1001/jamaoncol.2017.3064
   PubMed Web of Science ®Google Scholar
• Stelmachowska-Banaś M, Czajka-Oraniec I. Management of endocrine immune-related adverse events of immune checkpoint inhibitors: an updated review. Endocr Connect. 2020;9(10):R207–R228. doi: 10.1530/EC-20-0342
   PubMed Web of Science ®Google Scholar
• Shang YH, Zhang Y, Li JH, et al. Risk of endocrine adverse events in cancer patients treated with PD-1 inhibitors: a systematic review and meta-analysis. Immunotherapy. 2017;9(3):261–272. doi: 10.2217/imt-2016-0147
   PubMed Web of Science ®Google Scholar
• de Filette J, Andreescu CE, Cools F, et al. A systematic review and meta-analysis of endocrine-related adverse events associated with immune checkpoint inhibitors. Horm Metab Res. 2019;51(3):145–156. doi: 10.1055/a-0843-3366
   PubMed Web of Science ®Google Scholar
• Ryder M, Callahan M, Postow MA, et al. Endocrine-related adverse events following ipilimumab in patients with advanced melanoma: a comprehensive retrospective review from a single institution. Endocr Relat Cancer. 2014;21(2):371–381. doi: 10.1530/ERC-13-0499
   PubMed Web of Science ®Google Scholar
• Lee H, Hodi FS, Giobbie-Hurder A, et al. Characterization of thyroid disorders in patients receiving immune checkpoint inhibition therapy. Cancer Immunol Res. 2017;5(12):1133–1140. doi: 10.1158/2326-6066.CIR-17-0208
   PubMed Web of Science ®Google Scholar
• Chang LS, Barroso-Sousa R, Tolaney SM, et al. Endocrine toxicity of cancer immunotherapy targeting immune checkpoints. Endocr Rev. 2019;40(1):17–65. doi: 10.1210/er.2018-00006
   PubMed Web of Science ®Google Scholar
• Zhan L, Feng HF, Liu HQ, et al. Immune checkpoint inhibitors-related thyroid dysfunction: epidemiology, clinical presentation, possible pathogenesis, and management. Front Endocrinol. 2021;12:649863. doi: 10.3389/fendo.2021.649863
   PubMed Web of Science ®Google Scholar
• Guaraldi F, La Selva R, Samà MT, et al. Characterization and implications of thyroid dysfunction induced by immune checkpoint inhibitors in real-life clinical practice: a long-term prospective study from a referral institution. J Endocrinol Invest. 2018;41(5):549–556. doi: 10.1007/s40618-017-0772-1
   PubMed Web of Science ®Google Scholar
• Delivanis DA, Gustafson MP, Bornschlegl S, et al. Pembrolizumab-induced thyroiditis: comprehensive clinical review and insights into underlying involved mechanisms. J Clin Endocrinol Metab. 2017;102(8):2770–2780. doi: 10.1210/jc.2017-00448
   PubMed Web of Science ®Google Scholar
• Kurimoto C, Inaba H, Ariyasu H, et al. Predictive and sensitive biomarkers for thyroid dysfunctions during treatment with immune-checkpoint inhibitors. Cancer Sci. 2020;111(5):1468–1477. doi: 10.1111/cas.14363
   PubMed Web of Science ®Google Scholar
• Kimbara S, Fujiwara Y, Iwama S, et al. Association of antithyroglobulin antibodies with the development of thyroid dysfunction induced by nivolumab. Cancer Sci. 2018;109(11):3583–3590. doi: 10.1111/cas.13800
   PubMed Web of Science ®Google Scholar
• Kobayashi T, Iwama S, Yasuda Y, et al. Patients with antithyroid antibodies are prone to develop destructive thyroiditis by Nivolumab: a prospective study. J Endocr Soc. 2018 6;2(3):241–251. doi: 10.1210/js.2017-00432
   PubMed Web of Science ®Google Scholar
• Bhattacharya S, Goyal A, Kaur P, et al. Anticancer drug-induced thyroid dysfunction. Eur Endocrinol. 2020;16(1):32–39. doi: 10.17925/EE.2020.16.1.32
   PubMedGoogle Scholar
• Krieg C, Nowicka M, Guglietta S, et al. High-dimensional single-cell analysis predicts response to anti-PD-1 immunotherapy. Nat Med. 2018;24(2):144–153. doi: 10.1038/nm.4466
   PubMed Web of Science ®Google Scholar
• Cooksley T, Girotra M, Ginex P, et al. Multinational association of supportive care in cancer (MASCC) 2020 clinical practice recommendations for the management of immune checkpoint inhibitor endocrinopathies and the role of advanced practice providers in the management of immune-mediated toxicities. Support Care Cancer. 2020;28(12):6175–6181. doi: 10.1007/s00520-020-05709-1
   PubMed Web of Science ®Google Scholar
• Haanen J, Obeid M, Spain L, et al. ESMO guidelines Committee. Electronic address: [email protected]. Management of toxicities from immunotherapy: ESMO clinical practice guideline for diagnosis, treatment and follow-up. Ann Oncol. 2022;33(12):1217–1238. doi: 10.1016/j.annonc.2022.10.001
   PubMed Web of Science ®Google Scholar
• Patrizio A, Fallahi P, Antonelli A, et al. Immune checkpoint inhibitor-induced thyroid disorders: a single center experience. Curr Pharm Des. 2023;29(4):295–299. doi: 10.2174/1381612828666220518151509
   PubMed Web of Science ®Google Scholar
• Caturegli P, Newschaffer C, Olivi A, et al. Autoimmune hypophysitis. Endocr Rev. 2005;26(5):599–614. doi: 10.1210/er.2004-0011
   PubMed Web of Science ®Google Scholar
• Araujo PB, Coelho MC, Arruda M, et al. Ipilimumab-induced hypophysitis: review of the literature. J Endocrinol Invest. 2015;38(11):1159–1166. doi: 10.1007/s40618-015-0301-z
   PubMed Web of Science ®Google Scholar
• Dillard T, Yedinak CG, Alumkal J, et al. Anti-CTLA-4 antibody therapy associated autoimmune hypophysitis: serious immune related adverse events across a spectrum of cancer subtypes. Pituitary. 2010;13(1):29–38. doi: 10.1007/s11102-009-0193-z
   PubMed Web of Science ®Google Scholar
• Zhang B, Wu Q, Zhou YL, et al. Immune-related adverse events from combination immunotherapy in cancer patients: a comprehensive meta-analysis of randomized controlled trials. Int Immunopharmacol. 2018;63:292–298. doi: 10.1016/j.intimp.2018.08.014
   PubMed Web of Science ®Google Scholar
• Caturegli P, Di Dalmazi G, Lombardi M, et al. Hypophysitis secondary to Cytotoxic T-Lymphocyte-associated protein 4 blockade: insights into pathogenesis from an autopsy series. Am J Pathol. 2016;186(12):3225–3235. doi: 10.1016/j.ajpath.2016.08.020
   PubMed Web of Science ®Google Scholar
• Tan MH, Iyengar R, Mizokami-Stout K, et al. Spectrum of immune checkpoint inhibitors-induced endocrinopathies in cancer patients: a scoping review of case reports. Clin Diabetes Endocrinol. 2019;5:1. doi: 10.1186/s40842-018-0073-4
   PubMedGoogle Scholar
• Ascierto PA, Del Vecchio M, Robert C, et al. Ipilimumab 10 mg/kg versus ipilimumab 3 mg/kg in patients with unresectable or metastatic melanoma: a randomised, double-blind, multicentre, phase 3 trial. Lancet Oncol. 2017;18(5):611–622. doi: 10.1016/S1470-2045(17)30231-0
   PubMed Web of Science ®Google Scholar
• Lupi I, Brancatella A, Cosottini M, et al. Clinical heterogeneity of hypophysitis secondary to PD-1/PD-L1 blockade: insights from four cases. Endocrinol Diabetes Metab Case Rep. 2019;2019:19–0102. doi: 10.1530/EDM-19-0102
   PubMedGoogle Scholar
• Puzanov I, Diab A, Abdallah K, et al. Society for Immunotherapy of Cancer Toxicity Management Working Group. Managing toxicities associated with immune checkpoint inhibitors: consensus recommendations from the Society for immunotherapy of cancer (SITC) toxicity management working group. J Immunother Cancer. 2017;5(1):95. doi: 10.1186/s40425-017-0300-z
   PubMed Web of Science ®Google Scholar
• Amereller F, Deutschbein T, Joshi M, et al. Differences between immunotherapy-induced and primary hypophysitis-a multicenter retrospective study. Pituitary. 2022;25(1):152–158. doi: 10.1007/s11102-021-01182-z
   PubMed Web of Science ®Google Scholar
• Khoja L, Day D, Wei-Wu Chen T, et al. Tumour- and class-specific patterns of immune-related adverse events of immune checkpoint inhibitors: a systematic review. Ann Oncol. 2017;28(10):2377–2385. doi: 10.1093/annonc/mdx286
   PubMed Web of Science ®Google Scholar
• June CH, Warshauer JT, Bluestone JA. Is autoimmunity the Achilles’ heel of cancer immunotherapy? Nat Med. Nature Med. 2017;23(5):540–547. doi: 10.1038/nm.4321
   PubMed Web of Science ®Google Scholar
• Iwama S, De Remigis A, Callahan MK, et al. Pituitary expression of CTLA-4 mediates hypophysitis secondary to administration of CTLA-4 blocking antibody. Sci Transl Med. 2014;6(230):230ra45. doi: 10.1126/scitranslmed.3008002
   PubMed Web of Science ®Google Scholar
• Javorsky BR, Aron DC, Findling JW, et al. Hypothalamus and pituitary gland. In: Shoback D, editor. Greenspan’s basic and clinical endocrinology 9th ed. Gardner, D.G:Mc Graw-Hill Lange; 2011. p. 65–114.
   Google Scholar
• Mei Y, Bi WL, Greenwald NF, et al. Increased expression of programmed death ligand 1 (PD-L1) in human pituitary tumors. Oncotarget. 2016;7(47):76565–76576. doi: 10.18632/oncotarget.12088
   PubMedGoogle Scholar
• Da Gama Duarte J, Parakh S, Andrews MC, et al. Autoantibodies may predict immune-related toxicity: results from a phase I study of intralesional bacillus calmette-guérin followed by ipilimumab in patients with advanced metastatic melanoma. Front Immunol. 2018;9:411. doi: 10.3389/fimmu.2018.00411
   PubMed Web of Science ®Google Scholar
• Gowen MF, Giles KM, Simpson D, et al. Baseline antibody profiles predict toxicity in melanoma patients treated with immune checkpoint inhibitors. J Transl Med. 2018;16(1):82. doi: 10.1186/s12967-018-1452-4
   PubMedGoogle Scholar
• Leiter A, Gnjatic S, Fowkes M, et al. A COMMON PITUITARY AUTOANTIBODY in TWO PATIENTS with IMMUNE CHECKPOINT INHIBITOR-MEDIATED HYPOPHYSITIS: ZCCHC8. AACE Clin Case Rep. 2020;6(4):e151–e160. PMID: 32671216. doi: 10.4158/ACCR-2019-0585
   PubMedGoogle Scholar
• Molitch ME, Clemmons DR, Malozowski S, et al. Evaluation and treatment of adult growth hormone deficiency: an endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2011;96(6):1587–1609. doi: 10.1210/jc.2011-0179
   PubMed Web of Science ®Google Scholar
• Roos A, Linn-Rasker SP, van Domburg RT, et al. The starting dose of levothyroxine in primary hypothyroidism treatment: a prospective, randomized, double-blind trial. Arch Intern Med. 2005;165(15):1714–1720. doi: 10.1001/archinte.165.15.1714
   PubMed Web of Science ®Google Scholar
• Banitt PF, Munson AK. Addisonian crisis after thyroid replacement. Hosp Pract (Off Ed). 1986;21(5):132, 134.
   PubMed Web of Science ®Google Scholar
• Fleseriu M, Hashim IA, Karavitaki N, et al. Hormonal replacement in hypopituitarism in Adults: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2016;101(11):3888–3921. doi: 10.1210/jc.2016-2118
   PubMed Web of Science ®Google Scholar
• Mohamad NV, Wong SK, Wan Hasan WN, et al. The relationship between circulating testosterone and inflammatory cytokines in men. Aging Male. 2019;22(2):129–140. doi: 10.1080/13685538.2018.1482487
   PubMed Web of Science ®Google Scholar
• Alwani M, Al-Zoubi RM, Al-Qudimat A, et al. The impact of long-term testosterone therapy (TTh) in renal function (RF) among hypogonadal men: an observational cohort study. Ann Med Surg (Lond). 2021;69:102748. doi: 10.1016/j.amsu.2021.102748
   PubMed Web of Science ®Google Scholar
• Stamatouli AM, Quandt Z, Perdigoto AL, et al. Collateral damage: insulin-dependent diabetes induced with checkpoint inhibitors. Diabetes. 2018;67(8):1471–1480. doi: 10.2337/dbi18-0002
   PubMed Web of Science ®Google Scholar
• Wright JJ, Salem JE, Johnson DB, et al. Increased reporting of immune checkpoint inhibitor-associated diabetes. Diabetes Care. 2018;41(12):e150–e151. doi: 10.2337/dc18-1465
   PubMed Web of Science ®Google Scholar
• Lühder F, Höglund P, Allison JP, et al. Cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) regulates the unfolding of autoimmune diabetes. J Exp Med. 1998;187(3):427–432. doi: 10.1084/jem.187.3.427
   PubMed Web of Science ®Google Scholar
• Ansari MJ, Salama AD, Chitnis T et al. The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med. 2003;198(1): 63–69. doi: 10.1084/jem.20022125PMC2196083
   PubMed Web of Science ®Google Scholar
• Fife BT, Guleria I, Gubbels Bupp M, et al. Insulin-induced remission in new-onset NOD mice is maintained by the PD-1-PD-L1 pathway. J Exp Med. 2006;203(12):2737–2747. doi: 10.1084/jem.20061577
   PubMed Web of Science ®Google Scholar
• Fife BT, Pauken KE, Eagar TN, et al. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat Immunol. 2009;10(11):1185–1192. doi: 10.1038/ni.1790
   PubMed Web of Science ®Google Scholar
• Pizarro C, García-Díaz DF, Codner E, et al. PD-L1 gene polymorphisms and low serum level of PD-L1 protein are associated to type 1 diabetes in Chile. Diabetes Metab Res Rev. 2014;30(8):761–766. doi: 10.1002/dmrr.2552
   PubMed Web of Science ®Google Scholar
• Byun DJ, Wolchok JD, Rosenberg LM, et al. Cancer immunotherapy - immune checkpoint blockade and associated endocrinopathies. Nat Rev Endocrinol. 2017;13(4):195–207. doi: 10.1038/nrendo.2016.205
   PubMed Web of Science ®Google Scholar
• Hersh EM, O’Day SJ, Powderly J, et al. A phase II multicenter study of ipilimumab with or without dacarbazine in chemotherapy-naïve patients with advanced melanoma. Invest New Drugs. 2011;29(3):489–498. doi: 10.1007/s10637-009-9376-8
   PubMed Web of Science ®Google Scholar
• Bornstein SR, Allolio B, Arlt W, et al. Diagnosis and treatment of primary adrenal insufficiency: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2016 Feb;101(2):364–389. doi: 10.1210/jc.2015-1710
   PubMed Web of Science ®Google Scholar
• Hescot S, Haissaguerre M, Pautier P, et al. Immunotherapy-induced Addison’s disease: a rare, persistent and potentially lethal side-effect. Eur J Cancer. 2018;97:57–58. doi: 10.1016/j.ejca.2018.04.001
   PubMed Web of Science ®Google Scholar
• Paepegaey AC, Lheure C, Ratour C, et al. Polyendocrinopathy resulting from pembrolizumab in a patient with a malignant melanoma. J Endocr Soc. 2017;1(6):646–649. doi: 10.1210/js.2017-00170
   PubMedGoogle Scholar
• Deligiorgi MV, Trafalis DT. Reversible primary adrenal insufficiency related to anti-programmed cell-death 1 protein active immunotherapy: insight into an unforeseen outcome of a rare immune-related adverse event. Int Immunopharmacol. 2020;89(Pt B):107050. doi: 10.1016/j.intimp.2020.107050
   PubMedGoogle Scholar
• Bacanovic S, Burger IA, Stolzmann P, et al. Ipilimumab-Induced Adrenalitis: a possible pitfall in 18F-FDG-PET/CT. Clin Nucl Med. 2015;40(11):e518–9. doi: 10.1097/RLU.0000000000000887
   PubMed Web of Science ®Google Scholar
• Min L, Ibrahim N. Ipilimumab-induced autoimmune adrenalitis. Lancet Diabetes Endocrinol. 2013;1(3):e15. doi: 10.1016/S2213-8587(13)70031-7
   PubMed Web of Science ®Google Scholar
• Win MA, Thein KZ, Qdaisat A, et al. Acute symptomatic hypocalcemia from immune checkpoint therapy-induced hypoparathyroidism. Am J Emerg Med. 2017;35(7):e1039.5–.e1039.7. doi: 10.1016/j.ajem.2017.02.048
   Web of Science ®Google Scholar
• Umeguchi H, Takenoshita H, Inoue H, et al. Autoimmune-related primary hypoparathyroidism possibly induced by the administration of pembrolizumab: a case report. J Oncol Pract. 2018;14(7):449–451. doi: 10.1200/JOP.18.00076
   PubMed Web of Science ®Google Scholar
• Trinh B, Sanchez GO, Herzig P, et al. Inflammation-induced hypoparathyroidism triggered by combination immune checkpoint blockade for melanoma. J Immunother Cancer. 2019;7(1):52. doi: 10.1186/s40425-019-0528-x
   PubMedGoogle Scholar
• Piranavan P, Li Y, Brown E, et al. Immune checkpoint inhibitor-induced hypoparathyroidism associated with calcium-sensing receptor-activating autoantibodies. J Clin Endocrinol Metab. 2019;104(2):550–556. doi: 10.1210/jc.2018-01151
   PubMed Web of Science ®Google Scholar
• Lupi I, Brancatella A, Cetani F, et al. Activating antibodies to the calcium-sensing receptor in immunotherapy-induced hypoparathyroidism. J Clin Endocrinol Metab. 2020;105(5):dgaa092. doi: 10.1210/clinem/dgaa092
   PubMed Web of Science ®Google Scholar
• Dadu R, Rodgers TE, Trinh VA, et al. Calcium-sensing receptor autoantibody-mediated hypoparathyroidism associated with immune checkpoint inhibitor therapy: diagnosis and long-term follow-up. J Immunother Cancer. 2020;8(1):e000687. doi: 10.1136/jitc-2020-000687
   PubMed Web of Science ®Google Scholar
• Arima H, Iwama S, Inaba H, et al. Management of immune-related adverse events in endocrine organs induced by immune checkpoint inhibitors: clinical guidelines of the Japan endocrine Society. Endocr J. 2019;66(7):581–586. doi: 10.1507/endocrj.EJ19-0163
   PubMed Web of Science ®Google Scholar
• Clines GA. Mechanisms and treatment of hypercalcemia of malignancy. Curr Opin Endocrinol Diabetes Obes. 2011;18(6):339–346. doi: 10.1097/MED.0b013e32834b4401
   PubMed Web of Science ®Google Scholar
• Deligiorgi MV, Panayiotidis MI, Trafalis DT. Parathyroid hormone related protein (PTHrP)-mediated hypercalcemia in malignancy associated with anti-PD-1 immune checkpoint inhibitor treatment and related inflammatory reactions. Int Immunopharmacol. 2019;77:105942. doi: 10.1016/j.intimp.2019.105942
   PubMed Web of Science ®Google Scholar
• Araújo-Vilar D, Santini F. Diagnosis and treatment of lipodystrophy: a step-by-step approach. J Endocrinol Invest. 2019;42(1):61–73. doi: 10.1007/s40618-018-0887-z
   PubMed Web of Science ®Google Scholar
• Chiquette E, Oral EA, Garg A, et al. Estimating the prevalence of generalized and partial lipodystrophy: findings and challenges. Diabetes Metab Syndr Obes. 2017;10:375–383. doi: 10.2147/DMSO.S130810
   PubMedGoogle Scholar
• Hussain I, Garg A. Lipodystrophy syndromes. Endocrinol Metab Clin North Am. 2016;45(4):783–797. doi: 10.1016/j.ecl.2016.06.012
   PubMed Web of Science ®Google Scholar
• Simha V, Garg A. Lipodystrophy: lessons in lipid and energy metabolism. Curr Opin Lipidol. 2006;17(2):162–169. doi: 10.1097/01.mol.0000217898.52197.18
   PubMed Web of Science ®Google Scholar
• Haque WA, Shimomura I, Matsuzawa Y, et al. Serum adiponectin and leptin levels in patients with lipodystrophies. J Clin Endocrinol Metab. 2002;87(5):2395. doi: 10.1210/jcem.87.5.8624
   PubMed Web of Science ®Google Scholar
• Weyer C, Funahashi T, Tanaka S, et al. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001;86(5):1930–1935. doi: 10.1210/jcem.86.5.7463
   PubMed Web of Science ®Google Scholar
• Gnanendran SS, Miller JA, Archer CA, et al. Acquired lipodystrophy associated with immune checkpoint inhibitors. Melanoma Res. 2020;30(6):599–602. doi: 10.1097/CMR.0000000000000660
   PubMed Web of Science ®Google Scholar
• Brown RJ, Araujo-Vilar D, Cheung PT, et al. The diagnosis and management of lipodystrophy syndromes: a multi-society practice guideline. J Clin Endocrinol Metab. 2016;101(12):4500–4511. doi: 10.1210/jc.2016-2466
   PubMed Web of Science ®Google Scholar