Drug-induced thrombocytopenia: mechanisms and relevance in preclinical safety assessment

Arepally, 2017, Heparin-induced thrombocytopenia, Blood, 129, 2864, 10.1182/blood-2016-11-709873 Arnold, 2013, Approach to the diagnosis and management of drug-induced immune thrombocytopenia, Transfus Med Rev, 27, 137, 10.1016/j.tmrv.2013.05.005 Aster, 2007, Drug-induced immune thrombocytopenia, N Engl J Med, 357, 580, 10.1056/NEJMra066469 Aster, 2009, Drug-induced immune thrombocytopenia: pathogenesis, diagnosis, and management, J Thromb Haemost, 7, 911, 10.1111/j.1538-7836.2009.03360.x Barak, 2011, Tyrosine kinase inhibitors induced immune thrombocytopenia in chronic myeloid leukemia?, Hematol Rep, 3, e29, 10.4081/hr.2011.e29 Barber, 2011, Hematologic toxicities of small molecule tyrosine kinase inhibitors, Target Oncol, 6, 203, 10.1007/s11523-011-0202-9 Bloom, 1985, Gold-induced immune thrombocytopenia in the dog, Vet Pathol, 22, 492, 10.1177/030098588502200509 Boes, 2000, Role of natural and immune IgM antibodies in immune responses, Mol Immunol, 37, 1141, 10.1016/S0161-5890(01)00025-6 Bougie, 2006, Patients with quinine-induced immune thrombocytopenia have both “drug-dependent” and “drug-specific” antibodies, Blood, 108, 922, 10.1182/blood-2006-01-009803 Bougie, 2006, Patients with quinine-induced immune thrombocytopenia have both “drug-dependent” and “drug-specific” antibodies, Blood, 108, 922, 10.1182/blood-2006-01-009803 Bougie, 2002, Acute thrombocytopenia after treatment with tirofiban or eptifibatide is associated with antibodies specific for ligand-occupied GPIIb/IIIa, Blood, 100, 2071, 10.1182/blood.V100.6.2071 Brudno, 2016, Toxicities of chimeric antigen receptor T cells: recognition and management, Blood, 127, 3321, 10.1182/blood-2016-04-703751 Brunasso, 2009, Thrombocytopenia associated with the use of anti-tumor necrosis factor-alpha agents for psoriasis, J Am Acad Dermatol, 60, 781, 10.1016/j.jaad.2008.12.001 Carey, 2003, Drug-induced myelosuppression : diagnosis and management, Drug Saf, 26, 691, 10.2165/00002018-200326100-00003 Chipinda, 2011, Haptenation: chemical reactivity and protein binding, J Allergy (Cairo ), 2011, 839682 Chong, 1995, Heparin-induced thrombocytopenia, Br J Haematol, 89, 431, 10.1111/j.1365-2141.1995.tb08346.x Chong, 2003, Heparin-induced thrombocytopenia, J Thromb Haemost, 1, 1471, 10.1046/j.1538-7836.2003.00270.x Colombo, 1999, Primary stenting and glycoprotein IIb/IIIa inhibitors in acute myocardial infarction, Am Heart J, 138, S153, 10.1016/S0002-8703(99)70336-4 Crooke, 2017, The effects of 2'-O-methoxyethyl containing antisense oligonucleotides on platelets in human clinical trials, Nucleic Acid Ther, 27, 121, 10.1089/nat.2016.0650 Crooke, 2017, Cellular uptake and trafficking of antisense oligonucleotides, Nat Biotechnol, 35, 230, 10.1038/nbt.3779 Cuker, 2011, A distinctive form of immune thrombocytopenia in a phase 2 study of alemtuzumab for the treatment of relapsing-remitting multiple sclerosis, Blood, 118, 6299, 10.1182/blood-2011-08-371138 Curtis, 2014, Drug-induced immune thrombocytopenia: incidence, clinical features, laboratory testing, and pathogenic mechanisms, Immunohematology, 30, 55, 10.21307/immunohematology-2019-099 de Goeij, 2016, New developments for antibody-drug conjugate-based therapeutic approaches, Curr Opin Immunol, 40, 14, 10.1016/j.coi.2016.02.008 Diaz, 2011, Safety and efficacy of tirofiban as adjunctive therapy for patients with ST-elevation myocardial infarction: a comparison versus placebo and abciximab, Cardiovasc Hematol Agents Med Chem, 9, 147, 10.2174/187152511797037475 Donaghy, 2016, Effects of antibody, drug and linker on the preclinical and clinical toxicities of antibody-drug conjugates, mAbs, 8, 659, 10.1080/19420862.2016.1156829 Dourakis, 1996, Immune thrombocytopenia and alpha-interferon therapy, J Hepatol, 25, 972, 10.1016/S0168-8278(96)80304-7 Dy, 2013, Understanding, recognizing, and managing toxicities of targeted anticancer therapies, CA Cancer J Clin, 63, 249, 10.3322/caac.21184 Everds, 2013, Unexpected thrombocytopenia and anemia in cynomolgus monkeys induced by a therapeutic human monoclonal antibody, Toxicol Pathol, 41, 951, 10.1177/0192623312474727 Everds, 2013, Unexpected hematologic effects of biotherapeutics in nonclinical species and in humans, Toxicol Pathol, 41, 280, 10.1177/0192623312467400 Ganser, 1987, Effect of recombinant interferons alpha and gamma on human bone marrow-derived megakaryocytic progenitor cells, Blood, 70, 1173, 10.1182/blood.V70.4.1173.1173 Greinacher, 2017, Autoimmune heparin-induced thrombocytopenia, J Thromb Haemost, 15, 2099, 10.1111/jth.13813 Harker, 2000, Effects of megakaryocyte growth and development factor on platelet production, platelet life span, and platelet function in healthy human volunteers, Blood, 95, 2514, 10.1182/blood.V95.8.2514 Hartmann, 2009, Tyrosine kinase inhibitors - a review on pharmacology, metabolism and side effects, Curr. Drug Metab, 10, 470, 10.2174/138920009788897975 Henry, 2017, Assessment of the effects of 2'-methoxyethyl antisense oligonucleotides on platelet count in cynomolgus nonhuman primates, Nucleic Acid Ther, 27, 197, 10.1089/nat.2017.0666 Kelton, 1994, Immunoglobulin G from patients with heparin-induced thrombocytopenia binds to a complex of heparin and platelet factor 4, Blood, 83, 3232, 10.1182/blood.V83.11.3232.3232 Kenney, 2009, Drug-induced thrombocytopenia, Arch Pathol Lab Med, 133, 309, 10.5858/133.2.309 Kessler, 2012, Risk of significant cytopenias after treatment with tocilizumab in systemic juvenile arthritis patients with a history of macrophage activation syndrome, Pediatr Rheumatol Online J, 10, 30, 10.1186/1546-0096-10-30 Kumar, 2009, Myelosuppression and kinase selectivity of multikinase angiogenesis inhibitors, Br J Cancer, 101, 1717, 10.1038/sj.bjc.6605366 Kuter, 2015, Managing thrombocytopenia associated with cancer chemotherapy, Oncology (Williston Park), 29, 282 Lagace-Wiens, 2012, Adverse reactions to beta-lactam antimicrobials, Expert Opin Drug Saf, 11, 381, 10.1517/14740338.2012.643866 Lahouel, 1987, Haematotoxicity of doxorubicin and 1-(2-chloroethyl)-3-cyclohexyl-1-nitrosourea (CCNU) and of their association in rats, Drugs Exp Clin Res, 13, 593 Litvack, 2010, Review: soluble innate immune pattern-recognition proteins for clearing dying cells and cellular components: implications on exacerbating or resolving inflammation, Innate Immun, 16, 191, 10.1177/1753425910369271 Loo, 2012, Antimicrobial drug-induced thrombocytopenia: a review of the literature, Semin Thromb Hemost, 38, 818, 10.1055/s-0032-1328882 Machlus, 2013, The incredible journey: from megakaryocyte development to platelet formation, J Cell Biol, 201, 785, 10.1083/jcb.201304054 Machlus, 2017, Selinexor-induced thrombocytopenia results from inhibition of thrombopoietin signaling in early megakaryopoiesis, Blood, 130, 1132, 10.1182/blood-2016-11-752840 Mackarehtschian, 1995, Targeted disruption of the flk2/flt3 gene leads to deficiencies in primitive hematopoietic progenitors, Immunity, 3, 147, 10.1016/1074-7613(95)90167-1 Mazharian, 2011, Dasatinib enhances megakaryocyte differentiation but inhibits platelet formation, Blood, 117, 5198, 10.1182/blood-2010-12-326850 Mitta, 2019, Drug-induced thrombocytopenia: 2019 Update of clinical and laboratory data, Am J Hematol, 94, E76, 10.1002/ajh.25379 Mizuno, 2012, Impact of genetic variation in breast cancer resistance protein (BCRP/ABCG2) on sunitinib pharmacokinetics, Drug Metab Pharmacokinet, 27, 631, 10.2133/dmpk.DMPK-12-RG-026 Mochon, 1993, Evaluation of OKT3 monoclonal antibody and anti-thymocyte globulin in the treatment of steroid-resistant acute allograft rejection in pediatric renal transplants, Pediatr Nephrol, 7, 259, 10.1007/BF00853214 Narayanan, 2018, Investigation into the mechanism(s) that leads to platelet decreases in cynomolgus monkeys during administration of ISIS 104838, a 2'-MOE-modified antisense oligonucleotide, Toxicol Sci, 164, 613, 10.1093/toxsci/kfy119 Ogden, 2005, IGM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo, Autoimmunity, 38, 259, 10.1080/08916930500124452 Ohno, 1993, Haematological toxicity of carboplatin and cisplatin combined with whole body hyperthermia in rats, Br J Cancer, 68, 469, 10.1038/bjc.1993.372 Olaharski, 2009, In vitro to in vivo concordance of a high throughput assay of bone marrow toxicity across a diverse set of drug candidates, Toxicol Lett, 188, 98, 10.1016/j.toxlet.2009.03.012 Perras, 2004, Gefitinib for advanced or metastatic non-small cell lung cancer, Issues Emerg Health Technol, 1 Petursson, 1982, Megakaryocytopoiesis and granulopoiesis following cyclophosphamide, J Lab Clin Med, 100, 682 Poon, 2013, Preclinical safety profile of trastuzumab emtansine (T-DM1): mechanism of action of its cytotoxic component retained with improved tolerability, Toxicol Appl Pharmacol, 273, 298, 10.1016/j.taap.2013.09.003 Quach, 2018, Mechanisms of platelet clearance and translation to improve platelet storage, Blood, 131, 1512, 10.1182/blood-2017-08-743229 Quintas-Cardama, 2009, Dynamics and management of cytopenias associated with dasatinib therapy in patients with chronic myeloid leukemia in chronic phase after imatinib failure, Cancer, 115, 3935, 10.1002/cncr.24432 Rauova, 2006, Role of platelet surface PF4 antigenic complexes in heparin-induced thrombocytopenia pathogenesis: diagnostic and therapeutic implications, Blood, 107, 2346, 10.1182/blood-2005-08-3122 Reilly, 2002, Insights from mouse models of heparin-induced thrombocytopenia and thrombosis, Curr Opin Hematol, 9, 395, 10.1097/00062752-200209000-00002 Reilly, 2001, Heparin-induced thrombocytopenia/thrombosis in a transgenic mouse model requires human platelet factor 4 and platelet activation through FcgammaRIIA, Blood, 98, 2442, 10.1182/blood.V98.8.2442 Rich, 2003, In vitro hematotoxicity testing in drug development: a review of past, present and future applications, Curr Opin Drug Discov Devel, 6, 100 Rich, 2005, Validation and development of a predictive paradigm for hemotoxicology using a multifunctional bioluminescence colony-forming proliferation assay, Toxicol Sci, 87, 427, 10.1093/toxsci/kfi250 Rognoni, 2011, Update on glycoprotein IIb/IIIa: role in primary coronary intervention, Cardiovasc Hematol Agents Med Chem, 9, 106, 10.2174/187152511796196524 Rudmann, 2012, Rat-specific decreases in platelet count caused by a humanized monoclonal antibody against sclerostin, Toxicol Sci, 125, 586, 10.1093/toxsci/kfr318 Sakamoto, 2001, A novel Fc receptor for IgA and IgM is expressed on both hematopoietic and non-hematopoietic tissues, Eur J Immunol, 31, 1310, 10.1002/1521-4141(200105)31:5<1310::AID-IMMU1310>3.0.CO;2-N Santostefano, 2012, Off-target platelet activation in macaques unique to a therapeutic monoclonal antibody, Toxicol Pathol, 40, 899, 10.1177/0192623312444029 Sata, 1997, Mechanisms of thrombocytopenia induced by interferon therapy for chronic hepatitis B, J Gastroenterol, 32, 206, 10.1007/BF02936369 Senn, 2005, Non-CpG-containing antisense 2'-methoxyethyl oligonucleotides activate a proinflammatory response independent of Toll-like receptor 9 or myeloid differentiation factor 88, J Pharmacol Exp Ther, 314, 972, 10.1124/jpet.105.084004 Short, 2019, Emerging treatment paradigms with FLT3 inhibitors in acute myeloid leukemia, Ther Adv Hematol, 10, 10.1177/2040620719827310 Stathopoulos, 2010, Serious hematologic complications following erlotinib treatment, Anticancer Res, 30, 973 Suntharalingam, 2006, Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412, N Engl J Med, 355, 1018, 10.1056/NEJMoa063842 Thompson, 2018, Phase I trials of anti-ENPP3 antibody-drug conjugates in advanced Refractory renal cell Carcinomas, Clin Cancer Res, 24, 4399, 10.1158/1078-0432.CCR-18-0481 Thon, 2012, High-content live-cell imaging assay used to establish mechanism of trastuzumab emtansine (T-DM1)--mediated inhibition of platelet production, Blood, 120, 1975, 10.1182/blood-2012-04-420968 Thushara, 2014, Therapeutic drug-induced platelet apoptosis: an overlooked issue in pharmacotoxicology, Arch Toxicol, 88, 185, 10.1007/s00204-013-1185-3 Uppal, 2015, Potential mechanisms for thrombocytopenia development with trastuzumab emtansine (T-DM1), Clin Cancer Res, 21, 123, 10.1158/1078-0432.CCR-14-2093 Visentin, 1994, Antibodies from patients with heparin-induced thrombocytopenia/thrombosis are specific for platelet factor 4 complexed with heparin or bound to endothelial cells, J Clin Invest, 93, 81, 10.1172/JCI116987 Visentin, 2007, Drug-induced thrombocytopenia, Hematol Oncol Clin North Am, 21, 685, 10.1016/j.hoc.2007.06.005 von dem Borne, 1986, Thrombocytopenia associated with gold therapy: a drug-induced autoimmune disease?, Br J Haematol, 63, 509, 10.1111/j.1365-2141.1986.tb07528.x Warkentin, 2014, Overcoming myelosuppression due to synthetic lethal toxicity for FLT3-targeted acute myeloid leukemia therapy, Elife, 3, 10.7554/eLife.03445 Warkentin, 2005, Immune thrombocytopenia associated with efalizumab therapy for psoriasis, Ann Intern Med, 143, 761, 10.7326/0003-4819-143-10-200511150-00028 Weltzien, 1998, Molecular features of penicillin allergy, J Invest Dermatol, 110, 203, 10.1046/j.1523-1747.1998.00122.x Weycker, 2019, Risk and consequences of chemotherapy-induced thrombocytopenia in US clinical practice, BMC Cancer, 19, 151, 10.1186/s12885-019-5354-5 Yamane, 2008, Interferon-alpha 2b-induced thrombocytopenia is caused by inhibition of platelet production but not proliferation and endomitosis in human megakaryocytes, Blood, 112, 542, 10.1182/blood-2007-12-125906 Yeager, 1983, The effects of 5-fluorouracil on hematopoiesis: studies of murine megakaryocyte-CFC, granulocyte-macrophage-CFC, and peripheral blood cell levels, Exp Hematol, 11, 944 Zhao, 2017, Inhibition of megakaryocyte differentiation by antibody-drug conjugates (ADCs) is mediated by macropinocytosis: implications for ADC-induced thrombocytopenia, Mol Cancer Ther, 16, 1877, 10.1158/1535-7163.MCT-16-0710 Zufferey, 2017, Pathogenesis and therapeutic mechanisms in immune thrombocytopenia (ITP), J Clin Med, 6