دورية أكاديمية

Preclinical models of cardiotoxicity from immune checkpoint inhibitor therapy.

التفاصيل البيبلوغرافية
العنوان: Preclinical models of cardiotoxicity from immune checkpoint inhibitor therapy.
المؤلفون: Buehning F; Department of Cardiology and Vascular Medicine, West German Heart and Vascular Center, University Hospital Essen, Hufelandstraße 55, 45147, Essen, Germany., Lerchner T; Department of Cardiology and Vascular Medicine, West German Heart and Vascular Center, University Hospital Essen, Hufelandstraße 55, 45147, Essen, Germany., Vogel J; Department of Cardiology and Vascular Medicine, West German Heart and Vascular Center, University Hospital Essen, Hufelandstraße 55, 45147, Essen, Germany., Hendgen-Cotta UB; Department of Cardiology and Vascular Medicine, West German Heart and Vascular Center, University Hospital Essen, Hufelandstraße 55, 45147, Essen, Germany., Totzeck M; Department of Cardiology and Vascular Medicine, West German Heart and Vascular Center, University Hospital Essen, Hufelandstraße 55, 45147, Essen, Germany., Rassaf T; Department of Cardiology and Vascular Medicine, West German Heart and Vascular Center, University Hospital Essen, Hufelandstraße 55, 45147, Essen, Germany., Michel L; Department of Cardiology and Vascular Medicine, West German Heart and Vascular Center, University Hospital Essen, Hufelandstraße 55, 45147, Essen, Germany. lars.michel@uk-essen.de.
المصدر: Basic research in cardiology [Basic Res Cardiol] 2024 Jul 22. Date of Electronic Publication: 2024 Jul 22.
Publication Model: Ahead of Print
نوع المنشور: Journal Article; Review
اللغة: English
بيانات الدورية: Publisher: Steinkopff Country of Publication: Germany NLM ID: 0360342 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1435-1803 (Electronic) Linking ISSN: 03008428 NLM ISO Abbreviation: Basic Res Cardiol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Darmstadt, Steinkopff.
مستخلص: Immune checkpoint inhibitor (ICI) therapy represents a ground-breaking paradigm in cancer treatment, harnessing the immune system to combat malignancies by targeting checkpoints such as cytotoxic T-lymphocyte-associated protein 4 (CTLA-4) and programmed cell death protein 1 (PD-1). The use of ICI therapy generates distinctive immune-related adverse events (irAEs) including cardiovascular toxicity, necessitating targeted research efforts. This comprehensive review explores preclinical models dedicated to ICI-mediated cardiovascular complications including myocarditis. Tailored preclinical models of ICI-mediated myocardial toxicities highlight the key role of CD8 + T cells, emphasizing the profound impact of immune checkpoints on maintaining cardiac integrity. Cytokines and macrophages were identified as possible driving factors in disease progression, and at the same time, initial data on possible cardiac antigens responsible are emerging. The implications of contributing factors including thoracic radiation, autoimmune disorder, and the presence of cancer itself are increasingly understood. Besides myocarditis, mouse models unveiled an accelerated progression of atherosclerosis, adding another layer for a thorough understanding of the diverse processes involving cardiovascular immune checkpoint signalling. This review aims to discuss current preclinical models of ICI cardiotoxicity and their potential for improving enhanced risk assessment and diagnostics, offering potential targets for innovative cardioprotective strategies. Lessons from ICI therapy can drive novel approaches in cardiovascular research, extending insights to areas such as myocardial infarction and heart failure.
(© 2024. The Author(s).)
References: Addison D, Branch M, Baik AH, Fradley MG, Okwuosa T, Reding KW, Simpson KE, Suero-Abreu GA, Yang EH, Yancy CW (2023) Equity in cardio-oncology care and research: a scientific statement from the American Heart Association. Circulation 148:297–308. https://doi.org/10.1161/CIR.0000000000001158. (PMID: 10.1161/CIR.000000000000115837377045)
Afanasyeva M, Georgakopoulos D, Rose NR (2004) Autoimmune myocarditis: cellular mediators of cardiac dysfunction. Autoimmun Rev 3:476–486. https://doi.org/10.1016/j.autrev.2004.08.009. (PMID: 10.1016/j.autrev.2004.08.00915546794)
Agrawal S, Feng Y, Roy A, Kollia G, Lestini B (2016) Nivolumab dose selection: challenges, opportunities, and lessons learned for cancer immunotherapy. J Immunother Cancer 4:72. https://doi.org/10.1186/s40425-016-0177-2. (PMID: 10.1186/s40425-016-0177-2278799745109842)
Alturki NA (2023) Review of the immune checkpoint inhibitors in the context of cancer treatment. J Clin Med 12:4301. https://doi.org/10.3390/jcm12134301. (PMID: 10.3390/jcm121343013744533610342855)
Andres MS, Ramalingam S, Rosen SD, Baksi J, Khattar R, Kirichenko Y, Young K, Yousaf N, Okines A, Huddart R, Harrington K, Furness AJS, Turajlic S, Pickering L, Popat S, Larkin J, Lyon AR (2022) The spectrum of cardiovascular complications related to immune-checkpoint inhibitor treatment: including myocarditis and the new entity of non inflammatory left ventricular dysfunction. Cardio-Oncol Lond Engl 8:21. https://doi.org/10.1186/s40959-022-00147-w. (PMID: 10.1186/s40959-022-00147-w)
Andrews LP, Marciscano AE, Drake CG, Vignali DAA (2017) LAG3 (CD223) as a cancer immunotherapy target. Immunol Rev 276:80–96. https://doi.org/10.1111/imr.12519. (PMID: 10.1111/imr.12519282586925338468)
Arana Y, Gálvez RI, Jacobs T (2022) Role of the PD-1/PD-L1 pathway in experimental Trypanosoma cruzi infection and potential therapeutic options. Front Immunol 13:866120. https://doi.org/10.3389/fimmu.2022.866120. (PMID: 10.3389/fimmu.2022.866120358124589260015)
Axelrod ML, Meijers WC, Screever EM, Qin J, Carroll MG, Sun X, Tannous E, Zhang Y, Sugiura A, Taylor BC, Hanna A, Zhang S, Amancherla K, Tai W, Wright JJ, Wei SC, Opalenik SR, Toren AL, Rathmell JC, Ferrell PB, Phillips EJ, Mallal S, Johnson DB, Allison JP, Moslehi JJ, Balko JM (2022) T cells specific for α-myosin drive immunotherapy-related myocarditis. Nature 611:818–826. https://doi.org/10.1038/s41586-022-05432-3. (PMID: 10.1038/s41586-022-05432-3363855249930174)
Bockstahler M, Fischer A, Goetzke CC, Neumaier HL, Sauter M, Kespohl M, Müller A-M, Meckes C, Salbach C, Schenk M, Heuser A, Landmesser U, Weiner J, Meder B, Lehmann L, Kratzer A, Klingel K, Katus HA, Kaya Z, Beling A (2020) Heart-specific immune responses in an animal model of autoimmune-related myocarditis mitigated by an immunoproteasome inhibitor and genetic ablation. Circulation 141:1885–1902. https://doi.org/10.1161/CIRCULATIONAHA.119.043171. (PMID: 10.1161/CIRCULATIONAHA.119.04317132160764)
Bu D, Tarrio M, Maganto-Garcia E, Stavrakis G, Tajima G, Lederer J, Jarolim P, Freeman GJ, Sharpe AH, Lichtman AH (2011) Impairment of the PD-1 pathway increases atherosclerotic lesion development and inflammation. Arterioscler Thromb Vasc Biol 31:1100–1107. https://doi.org/10.1161/ATVBAHA.111.224709. (PMID: 10.1161/ATVBAHA.111.224709213935833104026)
Cochain C, Chaudhari SM, Koch M, Wiendl H, Eckstein H-H, Zernecke A (2014) Programmed cell death-1 deficiency exacerbates T cell activation and atherogenesis despite expansion of regulatory T cells in atherosclerosis-prone mice. PLoS ONE 9:e93280. https://doi.org/10.1371/journal.pone.0093280. (PMID: 10.1371/journal.pone.0093280246912023972211)
Cortellini A, Tucci M, Adamo V, Stucci LS, Russo A, Tanda ET, Spagnolo F, Rastelli F, Bisonni R, Santini D, Russano M, Anesi C, Giusti R, Filetti M, Marchetti P, Botticelli A, Gelibter A, Occhipinti MA, Marconcini R, Vitale MG, Nicolardi L, Chiari R, Bareggi C, Nigro O, Tuzi A, De Tursi M, Petragnani N, Pala L, Bracarda S, Macrini S, Inno A, Zoratto F, Veltri E, Di Cocco B, Mallardo D, Vitale MG, Pinato DJ, Porzio G, Ficorella C, Ascierto PA (2020) Integrated analysis of concomitant medications and oncological outcomes from PD-1/PD-L1 checkpoint inhibitors in clinical practice. J Immunother Cancer 8:e001361. https://doi.org/10.1136/jitc-2020-001361. (PMID: 10.1136/jitc-2020-001361331541507646355)
Delombaerde D, Vervloet D, Franssen C, Croes L, Gremonprez F, Prenen H, Peeters M, Vulsteke C (2021) Clinical implications of isolated troponinemia following immune checkpoint inhibitor therapy. ESMO Open 6:100216. https://doi.org/10.1016/j.esmoop.2021.100216. (PMID: 10.1016/j.esmoop.2021.100216342713098287144)
Dolladille C, Akroun J, Morice P-M, Dompmartin A, Ezine E, Sassier M, Da-Silva A, Plane A-F, Legallois D, L’Orphelin J-M, Alexandre J (2021) Cardiovascular immunotoxicities associated with immune checkpoint inhibitors: a safety meta-analysis. Eur Heart J 42:4964–4977. https://doi.org/10.1093/eurheartj/ehab618. (PMID: 10.1093/eurheartj/ehab61834529770)
Drobni ZD, Alvi RM, Taron J, Zafar A, Murphy SP, Rambarat PK, Mosarla RC, Lee C, Zlotoff DA, Raghu VK, Hartmann SE, Gilman HK, Gong J, Zubiri L, Sullivan RJ, Reynolds KL, Mayrhofer T, Zhang L, Hoffmann U, Neilan TG (2020) Association between immune checkpoint inhibitors with cardiovascular events and atherosclerotic plaque. Circulation 142:2299–2311. https://doi.org/10.1161/CIRCULATIONAHA.120.049981. (PMID: 10.1161/CIRCULATIONAHA.120.049981330039737736526)
D’Souza M, Nielsen D, Svane IM, Iversen K, Rasmussen PV, Madelaire C, Fosbøl E, Køber L, Gustafsson F, Andersson C, Gislason G, Torp-Pedersen C, Schou M (2021) The risk of cardiac events in patients receiving immune checkpoint inhibitors: a nationwide Danish study. Eur Heart J 42:1621–1631. https://doi.org/10.1093/eurheartj/ehaa884. (PMID: 10.1093/eurheartj/ehaa88433291147)
Du S, Zhou L, Alexander GS, Park K, Yang L, Wang N, Zaorsky NG, Ma X, Wang Y, Dicker AP, Lu B (2018) PD-1 modulates radiation-induced cardiac toxicity through cytotoxic T lymphocytes. J Thorac Oncol 13:510–520. https://doi.org/10.1016/j.jtho.2017.12.002. (PMID: 10.1016/j.jtho.2017.12.00229247829)
Dulos J, Carven GJ, van Boxtel SJ, Evers S, Driessen-Engels LJA, Hobo W, Gorecka MA, de Haan AFJ, Mulders P, Punt CJA, Jacobs JFM, Schalken JA, Oosterwijk E, van Eenennaam H, Boots AM (2012) PD-1 blockade augments Th1 and Th17 and suppresses Th2 responses in peripheral blood from patients with prostate and advanced melanoma cancer. J Immunother 35:169. https://doi.org/10.1097/CJI.0b013e318247a4e7. (PMID: 10.1097/CJI.0b013e318247a4e722306905)
Efentakis P, Choustoulaki A, Kostopoulos Ι, Varela A, Georgoulis A, Tsekenis G, Gakiopoulou C, Ntanasis-Stathopoulos I, Davos C, Tsitsiloni O, Dimopoulos MA, Terpos E, Gavriatopoulou M, Andreadou I (2023) Establishment of an in vivo murine model of immune checkPoint inhibitors cardiotoxicity: emerging role of vascular permeability in pembrolizumab-induced cardiotoxicity. Eur Heart J 44(ehad655):770. https://doi.org/10.1093/eurheartj/ehad655.770. (PMID: 10.1093/eurheartj/ehad655.770)
Efentakis P, Choustoulaki A, Kwiatkowski G, Varela A, Kostopoulos IV, Tsekenis G, Ntanasis-Stathopoulos I, Georgoulis A, Vorgias CE, Gakiopoulou H, Briasoulis A, Davos CH, Kostomitsopoulos N, Tsitsilonis O, Dimopoulos MA, Terpos E, Chłopicki S, Gavriatopoulou M, Andreadou I (2024) Early microvascular coronary endothelial dysfunction precedes pembrolizumab-induced cardiotoxicity. Preventive role of high dose of atorvastatin. Basic Res Cardiol. https://doi.org/10.1007/s00395-024-01046-0. (PMID: 10.1007/s00395-024-01046-038520533)
Ewing MM, Karper JC, Abdul S, de Jong RCM, Peters HAB, de Vries MR, Redeker A, Kuiper J, Toes REM, Arens R, Jukema JW, Quax PHA (2013) T-cell co-stimulation by CD28–CD80/86 and its negative regulator CTLA-4 strongly influence accelerated atherosclerosis development. Int J Cardiol 168:1965–1974. https://doi.org/10.1016/j.ijcard.2012.12.085. (PMID: 10.1016/j.ijcard.2012.12.08523351788)
Ferdinandy P, Baczkó I, Bencsik P, Giricz Z, Görbe A, Pacher P, Varga ZV, Varró A, Schulz R (2019) Definition of hidden drug cardiotoxicity: paradigm change in cardiac safety testing and its clinical implications. Eur Heart J 40:1771–1777. https://doi.org/10.1093/eurheartj/ehy365. (PMID: 10.1093/eurheartj/ehy36529982507)
Finke D, Heckmann MB, Salatzki J, Riffel J, Herpel E, Heinzerling LM, Meder B, Völkers M, Müller OJ, Frey N, Katus HA, Leuschner F, Kaya Z, Lehmann LH (2021) Comparative transcriptomics of immune checkpoint inhibitor myocarditis identifies guanylate binding protein 5 and 6 dysregulation. Cancers 13:2498. https://doi.org/10.3390/cancers13102498. (PMID: 10.3390/cancers13102498340654198161064)
Frodermann V, Nahrendorf M (2018) Macrophages and cardiovascular health. Physiol Rev 98:2523–2569. https://doi.org/10.1152/physrev.00068.2017. (PMID: 10.1152/physrev.00068.2017301564966442921)
Ganatra S, Neilan TG (2018) Immune checkpoint inhibitor-associated myocarditis. Oncologist 23:879–886. https://doi.org/10.1634/theoncologist.2018-0130. (PMID: 10.1634/theoncologist.2018-0130298022196156176)
Gergely TG, Drobni ZD, Kallikourdis M, Zhu H, Meijers WC, Neilan TG, Rassaf T, Ferdinandy P, Varga ZV (2024) Immune checkpoints in cardiac physiology and pathology: therapeutic targets for heart failure. Nat Rev Cardiol. https://doi.org/10.1038/s41569-023-00986-9. (PMID: 10.1038/s41569-023-00986-938279046)
Gergely TG, Kucsera D, Tóth VE, Kovács T, Sayour NV, Drobni ZD, Ruppert M, Petrovich B, Ágg B, Onódi Z, Fekete N, Pállinger É, Buzás EI, Yousif LI, Meijers WC, Radovits T, Merkely B, Ferdinandy P, Varga ZV (2023) Characterization of immune checkpoint inhibitor-induced cardiotoxicity reveals interleukin-17A as a driver of cardiac dysfunction after anti-PD-1 treatment. Br J Pharmacol 180:740–761. https://doi.org/10.1111/bph.15984. (PMID: 10.1111/bph.1598436356191)
Glembotski CC (2011) Functions for the cardiomyokine, MANF, in cardioprotection, hypertrophy and heart failure. J Mol Cell Cardiol 51:512–517. https://doi.org/10.1016/j.yjmcc.2010.10.008. (PMID: 10.1016/j.yjmcc.2010.10.00820970425)
Glembotski CC, Thuerauf DJ, Huang C, Vekich JA, Gottlieb RA, Doroudgar S (2012) Mesencephalic astrocyte-derived neurotrophic factor protects the heart from ischemic damage and is selectively secreted upon sarco/endoplasmic reticulum calcium depletion. J Biol Chem 287:25893–25904. https://doi.org/10.1074/jbc.M112.356345. (PMID: 10.1074/jbc.M112.356345226374753406674)
Goldstein DA, Ratain MJ, Saltz LB (2020) Weight-based dosing of pembrolizumab every 6 weeks in the time of COVID-19. JAMA Oncol 6:1694–1695. https://doi.org/10.1001/jamaoncol.2020.2493. (PMID: 10.1001/jamaoncol.2020.249332459313)
Gotsman I, Grabie N, Dacosta R, Sukhova G, Sharpe A, Lichtman AH (2007) Proatherogenic immune responses are regulated by the PD-1/PD-L pathway in mice. J Clin Investig 117:2974–2982. https://doi.org/10.1172/JCI31344. (PMID: 10.1172/JCI31344178539431974866)
Grabie N, Delfs MW, Westrich JR, Love VA, Stavrakis G, Ahmad F, Seidman CE, Seidman JG, Lichtman AH (2003) IL-12 is required for differentiation of pathogenic CD8+ T cell effectors that cause myocarditis. J Clin Investig 111:671–680. https://doi.org/10.1172/JCI200316867. (PMID: 10.1172/JCI20031686712618521151896)
Grabie N, Gotsman I, DaCosta R, Pang H, Stavrakis G, Butte MJ, Keir ME, Freeman GJ, Sharpe AH, Lichtman AH (2007) Endothelial programmed death-1 ligand 1 (PD-L1) regulates CD8+ T-cell-mediated injury in the heart. Circulation 116:2062–2071. https://doi.org/10.1161/CIRCULATIONAHA.107.709360. (PMID: 10.1161/CIRCULATIONAHA.107.70936017938288)
Grievink HW, Smit V, Verwilligen RAF, Bernabé Kleijn MNA, Smeets D, Binder CJ, Yagita H, Moerland M, Kuiper J, Bot I, Foks AC (2021) Stimulation of the PD-1 pathway decreases atherosclerotic lesion development in Ldlr deficient mice. Front Cardiovasc Med 8:740531. https://doi.org/10.3389/fcvm.2021.740531. (PMID: 10.3389/fcvm.2021.740531347907078591266)
Gutierrez FRS, Mariano FS, Oliveira CJF, Pavanelli WR, Guedes PMM, Silva GK, Campanelli AP, Milanezi CM, Azuma M, Honjo T, Teixeira MM, Aliberti JCS, Silva JS (2011) Regulation of Trypanosoma cruzi-induced myocarditis by programmed death cell receptor 1. Infect Immun 79:1873–1881. https://doi.org/10.1128/IAI.01047-10. (PMID: 10.1128/IAI.01047-10213577173088162)
Hansen AK, Hansen CHF (2021) The microbiome and rodent models of immune mediated diseases. Mamm Genome 32:251–262. https://doi.org/10.1007/s00335-021-09866-4. (PMID: 10.1007/s00335-021-09866-4337927998012743)
Herrmann J (2020) Adverse cardiac effects of cancer therapies: cardiotoxicity and arrhythmia. Nat Rev Cardiol 17:474–502. https://doi.org/10.1038/s41569-020-0348-1. (PMID: 10.1038/s41569-020-0348-1322313328782611)
Heusch G (2020) Myocardial ischaemia-reperfusion injury and cardioprotection in perspective. Nat Rev Cardiol 17:773–789. https://doi.org/10.1038/s41569-020-0403-y. (PMID: 10.1038/s41569-020-0403-y32620851)
Heusch G (2023) Cardioprotection in cardio-oncology: a case for concern? Cardiovasc Res 119:e144–e145. https://doi.org/10.1093/cvr/cvad111. (PMID: 10.1093/cvr/cvad11137587745)
Huang YV, Lee D, Sun Y, Chou H, Xu B, Lin Z, Branche C, Bayer A, Waliany S, Neal J, Wakelee H, Witteles R, Nguyen P, Graves E, Alcaide P, Berry GJ, Wu SM, Zhu H (2024) A novel therapeutic approach using CXCR3 blockade to treat immune checkpoint inhibitor-mediated myocarditis. https://doi.org/10.1101/2024.01.30.576279.
Huo J-L, Wang Y-T, Fu W-J, Lu N, Liu Z-S (2022) The promising immune checkpoint LAG-3 in cancer immunotherapy: from basic research to clinical application. Front Immunol 13:956090. (PMID: 10.3389/fimmu.2022.956090359585639361790)
Ji C, Roy MD, Golas J, Vitsky A, Ram S, Kumpf SW, Martin M, Barletta F, Meier WA, Hooper AT, Sapra P, Khan NK, Finkelstein M, Guffroy M, Buetow BS (2019) Myocarditis in cynomolgus monkeys following treatment with immune checkpoint inhibitors. Clin Cancer Res 25:4735–4748. https://doi.org/10.1158/1078-0432.CCR-18-4083. (PMID: 10.1158/1078-0432.CCR-18-408331085720)
Johnson DB, Balko JM, Compton ML, Chalkias S, Gorham J, Xu Y, Hicks M, Puzanov I, Alexander MR, Bloomer TL, Becker JR, Slosky DA, Phillips EJ, Pilkinton MA, Craig-Owens L, Kola N, Plautz G, Reshef DS, Deutsch JS, Deering RP, Olenchock BA, Lichtman AH, Roden DM, Seidman CE, Koralnik IJ, Seidman JG, Hoffman RD, Taube JM, Diaz LA, Anders RA, Sosman JA, Moslehi JJ (2016) Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med 375:1749–1755. https://doi.org/10.1056/NEJMoa1609214. (PMID: 10.1056/NEJMoa1609214278062335247797)
Kim ST, Bittar M, Kim HJ, Neelapu SS, Zurita AJ, Nurieva R, Suarez-Almazor ME (2019) Recurrent pseudogout after therapy with immune checkpoint inhibitors: a case report with immunoprofiling of synovial fluid at each flare. J Immunother Cancer 7:126. https://doi.org/10.1186/s40425-019-0597-x. (PMID: 10.1186/s40425-019-0597-x310885756518723)
Klocke K, Sakaguchi S, Holmdahl R, Wing K (2016) Induction of autoimmune disease by deletion of CTLA-4 in mice in adulthood. Proc Natl Acad Sci U S A 113:E2383–E2392. https://doi.org/10.1073/pnas.1603892113. (PMID: 10.1073/pnas.1603892113270711304855592)
Lafuse WP, Wozniak DJ, Rajaram MVS (2020) Role of cardiac macrophages on cardiac inflammation. Fibros Tissue Repair Cells 10:51. https://doi.org/10.3390/cells10010051. (PMID: 10.3390/cells10010051)
Li N, Wang Y, Forbes K, Vignali KM, Heale BS, Saftig P, Hartmann D, Black RA, Rossi JJ, Blobel CP, Dempsey PJ, Workman CJ, Vignali DAA (2007) Metalloproteases regulate T-cell proliferation and effector function via LAG-3. EMBO J 26:494–504. https://doi.org/10.1038/sj.emboj.7601520. (PMID: 10.1038/sj.emboj.7601520172454331783452)
Liu Y, Chen Y, Zeng Z, Liu A (2022) Arrhythmic events associated with immune checkpoint inhibitors therapy: a real-world study based on the Food and Drug Administration Adverse Event Reporting System database. Cancer Med 12:6637–6648. https://doi.org/10.1002/cam4.5438. (PMID: 10.1002/cam4.54383642638210067122)
Love VA, Grabie N, Duramad P, Stavrakis G, Sharpe A, Lichtman A (2007) CTLA-4 ablation and interleukin-12-driven differentiation synergistically augment cardiac pathogenicity of cytotoxic T lymphocytes. Circ Res 101:248–257. https://doi.org/10.1161/CIRCRESAHA.106.147124. (PMID: 10.1161/CIRCRESAHA.106.14712417569889)
Lucas JA, Menke J, Rabacal WA, Schoen FJ, Sharpe AH, Kelly VR (2008) PD-L1 Regulates a critical checkpoint for autoimmune myocarditis and pneumonitis in MRL mice. J Immunol Baltim Md 1950 181:2513–2521.
Ma K, Lv S, Liu B, Liu Z, Luo Y, Kong W, Xu Q, Feng J, Wang X (2013) CTLA4-IgG ameliorates homocysteine-accelerated atherosclerosis by inhibiting T-cell overactivation in apoE−/− mice. Cardiovasc Res 97:349–359. https://doi.org/10.1093/cvr/cvs330. (PMID: 10.1093/cvr/cvs33023118130)
Mahmood SS, Fradley MG, Cohen JV, Nohria A, Reynolds KL, Heinzerling LM, Sullivan RJ, Damrongwatanasuk R, Chen CL, Gupta D, Kirchberger MC, Awadalla M, Hassan MZO, Moslehi JJ, Shah SP, Ganatra S, Thavendiranathan P, Lawrence DP, Groarke JD, Neilan TG (2018) Myocarditis in patients treated with immune checkpoint inhibitors. J Am Coll Cardiol 71:1755–1764. https://doi.org/10.1016/j.jacc.2018.02.037. (PMID: 10.1016/j.jacc.2018.02.037295672106196725)
Martins F, Sofiya L, Sykiotis GP, Lamine F, Maillard M, Fraga M, Shabafrouz K, Ribi C, Cairoli A, Guex-Crosier Y, Kuntzer T, Michielin O, Peters S, Coukos G, Spertini F, Thompson JA, Obeid M (2019) Adverse effects of immune-checkpoint inhibitors: epidemiology, management and surveillance. Nat Rev Clin Oncol 16:563–580. https://doi.org/10.1038/s41571-019-0218-0. (PMID: 10.1038/s41571-019-0218-031092901)
Matsumoto T, Sasaki N, Yamashita T, Emoto T, Kasahara K, Mizoguchi T, Hayashi T, Yodoi K, Kitano N, Saito T, Yamaguchi T, Hirata K-I (2016) Overexpression of cytotoxic T-lymphocyte-associated antigen-4 prevents atherosclerosis in mice. Arterioscler Thromb Vasc Biol 36:1141–1151. https://doi.org/10.1161/ATVBAHA.115.306848. (PMID: 10.1161/ATVBAHA.115.30684827055906)
Meng C, Fan L, Wang X, Wang Y, Li Y, Pang S, Lv S, Zhang J (2022) Preparation and evaluation of animal models of cardiotoxicity in antineoplastic therapy. Oxid Med Cell Longev 2022:e3820591. https://doi.org/10.1155/2022/3820591. (PMID: 10.1155/2022/3820591)
Michel L, Helfrich I, Hendgen-Cotta UB, Mincu R-I, Korste S, Mrotzek SM, Spomer A, Odersky A, Rischpler C, Herrmann K, Umutlu L, Coman C, Ahrends R, Sickmann A, Löffek S, Livingstone E, Ugurel S, Zimmer L, Gunzer M, Schadendorf D, Totzeck M, Rassaf T (2022) Targeting early stages of cardiotoxicity from anti-PD1 immune checkpoint inhibitor therapy. Eur Heart J 43:316–329. https://doi.org/10.1093/eurheartj/ehab430. (PMID: 10.1093/eurheartj/ehab43034389849)
Michel L, Hendgen-Cotta UB, Mincu RI, Helfrich I, Korste S, Mrotzek SM, Rischpler C, Herrmann K, Ugurel S, Zimmer L, Coman C, Ahrends R, Schadendorf D, Rassaf T, Totzeck M (2020) Preclinical and clinical assessment of immune checkpoint inhibitor-associated left ventricular dysfunction. Eur Heart J 41(ehaa946):3260. https://doi.org/10.1093/ehjci/ehaa946.3260. (PMID: 10.1093/ehjci/ehaa946.3260)
Michel L, Korste S, Spomer A, Hendgen-Cotta UB, Rassaf T, Totzeck M (2022) PD1 deficiency modifies cardiac immunity during baseline conditions and in reperfused acute myocardial infarction. Int J Mol Sci 23:7533. https://doi.org/10.3390/ijms23147533. (PMID: 10.3390/ijms23147533358868789321105)
Michot JM, Bigenwald C, Champiat S, Collins M, Carbonnel F, Postel-Vinay S, Berdelou A, Varga A, Bahleda R, Hollebecque A, Massard C, Fuerea A, Ribrag V, Gazzah A, Armand JP, Amellal N, Angevin E, Noel N, Boutros C, Mateus C, Robert C, Soria JC, Marabelle A, Lambotte O (2006) Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer Oxf Engl 1990 54:139–148. https://doi.org/10.1016/j.ejca.2015.11.016. (PMID: 10.1016/j.ejca.2015.11.016)
Moradi A, Kodali A, Okoye C, Klein DH, Mohamoud I, Olanisa OO, Parab P, Chaudhary P, Mukhtar S, Mohammed L (2023) A systematic review of myocarditis induced by immune checkpoint inhibitors: how concerning is the most common cardiotoxicity of immune checkpoint inhibitors? Cureus 15:e42071. https://doi.org/10.7759/cureus.42071. (PMID: 10.7759/cureus.420713760212510434730)
Mrotzek SM, Rassaf T, Totzeck M (2020) Cardiovascular damage associated with chest irradiation. Front Cardiovasc Med 7:41. https://doi.org/10.3389/fcvm.2020.00041. (PMID: 10.3389/fcvm.2020.00041322662947103638)
Mulholland M, Kritikou E, Katra P, Nilsson J, Björkbacka H, Lichtman AH, Rodriguez A, Engelbertsen D (2022) LAG3 regulates T cell activation and plaque infiltration in atherosclerotic mice. JACC CardioOncol 4:635–645. https://doi.org/10.1016/j.jaccao.2022.09.005. (PMID: 10.1016/j.jaccao.2022.09.005366364469830219)
Mullick N, Nambudiri VE (2023) Relatlimab-nivolumab: a practical overview for dermatologists. J Am Acad Dermatol 89:1031–1037. https://doi.org/10.1016/j.jaad.2023.06.024. (PMID: 10.1016/j.jaad.2023.06.02437343829)
Myers CJ, Lu B (2017) Decreased survival after combining thoracic irradiation and an anti-PD-1 antibody is correlated with increased T cell infiltration into cardiac and lung tissues. Int J Radiat Oncol Biol Phys 99:1129–1136. https://doi.org/10.1016/j.ijrobp.2017.06.2452. (PMID: 10.1016/j.ijrobp.2017.06.2452291652835726785)
Newman JL, Stone JR (2019) Immune checkpoint inhibition alters the inflammatory cell composition of human coronary artery atherosclerosis. Cardiovasc Pathol 43:107148. https://doi.org/10.1016/j.carpath.2019.107148. (PMID: 10.1016/j.carpath.2019.10714831518915)
Nicolás-Ávila JA, Pena-Couso L, Muñoz-Cánoves P, Hidalgo A (2022) Macrophages, metabolism and heterophagy in the heart. Circ Res 130:418–431. https://doi.org/10.1161/CIRCRESAHA.121.319812. (PMID: 10.1161/CIRCRESAHA.121.31981235113662)
Nishimura H, Okazaki T, Tanaka Y, Nakatani K, Hara M, Matsumori A, Sasayama S, Mizoguchi A, Hiai H, Minato N, Honjo T (2001) Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291:319–322. https://doi.org/10.1126/science.291.5502.319. (PMID: 10.1126/science.291.5502.31911209085)
Okazaki T, Okazaki I, Wang J, Sugiura D, Nakaki F, Yoshida T, Kato Y, Fagarasan S, Muramatsu M, Eto T, Hioki K, Honjo T (2011) PD-1 and LAG-3 inhibitory co-receptors act synergistically to prevent autoimmunity in mice. J Exp Med 208:395–407. https://doi.org/10.1084/jem.20100466. (PMID: 10.1084/jem.20100466213009123039848)
Okazaki T, Tanaka Y, Nishio R, Mitsuiye T, Mizoguchi A, Wang J, Ishida M, Hiai H, Matsumori A, Minato N, Honjo T (2003) Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat Med 9:1477–1483. https://doi.org/10.1038/nm955. (PMID: 10.1038/nm95514595408)
Ottaviano M, De Placido S, Ascierto PA (2019) Recent success and limitations of immune checkpoint inhibitors for cancer: a lesson from melanoma. Virchows Arch 474:421–432. https://doi.org/10.1007/s00428-019-02538-4. (PMID: 10.1007/s00428-019-02538-430747264)
Poels K, van Leent MMT, Boutros C, Tissot H, Roy S, Meerwaldt AE, Toner YCA, Reiche ME, Kusters PJH, Malinova T, Huveneers S, Kaufman AE, Mani V, Fayad ZA, de Winther MPJ, Marabelle A, Mulder WJM, Robert C, Seijkens TTP, Lutgens E (2020) Immune checkpoint inhibitor therapy aggravates T cell-driven plaque inflammation in atherosclerosis. JACC CardioOncol 2:599–610. https://doi.org/10.1016/j.jaccao.2020.08.007. (PMID: 10.1016/j.jaccao.2020.08.007343962718352210)
Poels K, van Leent MMT, Reiche ME, Kusters PJH, Huveneers S, de Winther MPJ, Mulder WJM, Lutgens E, Seijkens TTP (2020) Antibody-mediated inhibition of CTLA4 aggravates atherosclerotic plaque inflammation and progression in hyperlipidemic mice. Cells 9:1987. https://doi.org/10.3390/cells9091987. (PMID: 10.3390/cells9091987328723937565685)
Ross R (1999) Atherosclerosis—an inflammatory disease. N Engl J Med 340:115–126. https://doi.org/10.1056/NEJM199901143400207. (PMID: 10.1056/NEJM1999011434002079887164)
Roth ME, Muluneh B, Jensen BC, Madamanchi C, Lee CB (2016) Left ventricular dysfunction after treatment with ipilimumab for metastatic melanoma. Am J Ther 23:e1925–e1928. https://doi.org/10.1097/MJT.0000000000000430. (PMID: 10.1097/MJT.000000000000043026885708)
Rowshanravan B, Halliday N, Sansom DM (2018) CTLA-4: a moving target in immunotherapy. Blood 131:58–67. https://doi.org/10.1182/blood-2017-06-741033. (PMID: 10.1182/blood-2017-06-74103329118008)
Rubio-Infante N, Ramírez-Flores YA, Castillo EC, Lozano O, García-Rivas G, Torre-Amione G (2021) Cardiotoxicity associated with immune checkpoint inhibitor therapy: a meta-analysis. Eur J Heart Fail 23:1739–1747. https://doi.org/10.1002/ejhf.2289. (PMID: 10.1002/ejhf.228934196077)
Sager HB, Hulsmans M, Lavine KJ, Moreira MB, Heidt T, Courties G, Sun Y, Iwamoto Y, Tricot B, Khan OF, Dahlman JE, Borodovsky A, Fitzgerald K, Anderson DG, Weissleder R, Libby P, Swirski FK, Nahrendorf M (2016) Proliferation and recruitment contribute to myocardial macrophage expansion in chronic heart failure. Circ Res 119:853–864. https://doi.org/10.1161/CIRCRESAHA.116.309001. (PMID: 10.1161/CIRCRESAHA.116.309001274447555378496)
Sharpe AH, Pauken KE (2018) The diverse functions of the PD1 inhibitory pathway. Nat Rev Immunol 18:153–167. https://doi.org/10.1038/nri.2017.108. (PMID: 10.1038/nri.2017.10828990585)
Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, Mendelsohn M, Charron J, Datta M, Young F, Stall AM (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:855–867. https://doi.org/10.1016/0092-8674(92)90029-c. (PMID: 10.1016/0092-8674(92)90029-c1547487)
Taleb S (2016) Inflammation in atherosclerosis. Arch Cardiovasc Dis 109:708–715. https://doi.org/10.1016/j.acvd.2016.04.002. (PMID: 10.1016/j.acvd.2016.04.00227595467)
Tao L, Reese TA (2017) Making mouse models that reflect human immune responses. Trends Immunol 38:181–193. https://doi.org/10.1016/j.it.2016.12.007. (PMID: 10.1016/j.it.2016.12.00728161189)
Tarrio ML, Grabie N, Bu D, Sharpe AH, Lichtman AH (2012) PD-1 protects against inflammation and myocyte damage in T cell mediated myocarditis. J Immunol Baltim Md 1950 188:4876–4884. https://doi.org/10.4049/jimmunol.1200389. (PMID: 10.4049/jimmunol.1200389)
Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH (1995) Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3:541–547. https://doi.org/10.1016/1074-7613(95)90125-6. (PMID: 10.1016/1074-7613(95)90125-67584144)
Totzeck M, Schuler M, Stuschke M, Heusch G, Rassaf T (2019) Cardio-oncology - strategies for management of cancer-therapy related cardiovascular disease. Int J Cardiol 280:163–175. https://doi.org/10.1016/j.ijcard.2019.01.038. (PMID: 10.1016/j.ijcard.2019.01.03830661849)
Wang DY, Salem J-E, Cohen JV, Chandra S, Menzer C, Ye F, Zhao S, Das S, Beckermann KE, Ha L, Rathmell WK, Ancell KK, Balko JM, Bowman C, Davis EJ, Chism DD, Horn L, Long GV, Carlino MS, Lebrun-Vignes B, Eroglu Z, Hassel JC, Menzies AM, Sosman JA, Sullivan RJ, Moslehi JJ, Johnson DB (2018) Fatal toxic effects associated with immune checkpoint inhibitors: a systematic review and meta-analysis. JAMA Oncol 4:1721–1728. https://doi.org/10.1001/jamaoncol.2018.3923. (PMID: 10.1001/jamaoncol.2018.3923302423166440712)
Wang J, Okazaki I-M, Yoshida T, Chikuma S, Kato Y, Nakaki F, Hiai H, Honjo T, Okazaki T (2010) PD-1 deficiency results in the development of fatal myocarditis in MRL mice. Int Immunol 22:443–452. https://doi.org/10.1093/intimm/dxq026. (PMID: 10.1093/intimm/dxq02620410257)
Waterhouse P, Penninger JM, Timms E, Wakeham A, Shahinian A, Lee KP, Thompson CB, Griesser H, Mak TW (1995) Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 270:985–988. https://doi.org/10.1126/science.270.5238.985. (PMID: 10.1126/science.270.5238.9857481803)
Wei SC, Meijers WC, Axelrod ML, Anang N-AAS, Screever EM, Wescott EC, Johnson DB, Whitley E, Lehmann L, Courand P-Y, Mancuso JJ, Himmel LE, Lebrun-Vignes B, Wleklinski MJ, Knollmann BC, Srinivasan J, Li Y, Atolagbe OT, Rao X, Zhao Y, Wang J, Ehrlich LIR, Sharma P, Salem J-E, Balko JM, Moslehi JJ, Allison JP (2021) A genetic mouse model recapitulates immune checkpoint inhibitor-associated myocarditis and supports a mechanism-based therapeutic intervention. Cancer Discov 11:614–625. https://doi.org/10.1158/2159-8290.CD-20-0856. (PMID: 10.1158/2159-8290.CD-20-085633257470)
Westdorp H, Sweep MWD, Gorris MAJ, Hoentjen F, Boers-Sonderen MJ, van der Post RS, van den Heuvel MM, Piet B, Boleij A, Bloemendal HJ, de Vries IJM (2021) Mechanisms of immune checkpoint inhibitor-mediated colitis. Front Immunol 12:768957. https://doi.org/10.3389/fimmu.2021.768957. (PMID: 10.3389/fimmu.2021.768957347773878586074)
Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, Fehervari Z, Nomura T, Sakaguchi S (2008) CTLA-4 control over Foxp3+ regulatory T cell function. Science 322:271–275. https://doi.org/10.1126/science.1160062. (PMID: 10.1126/science.116006218845758)
Won T, Kalinoski HM, Wood MK, Hughes DM, Jaime CM, Delgado P, Talor MV, Lasrado N, Reddy J, Čiháková D (2022) Cardiac myosin-specific autoimmune T cells contribute to immune-checkpoint-inhibitor-associated myocarditis. Cell Rep. https://doi.org/10.1016/j.celrep.2022.111611. (PMID: 10.1016/j.celrep.2022.1116113635141111108585)
Woo S-R, Turnis ME, Goldberg MV, Bankoti J, Selby M, Nirschl CJ, Bettini ML, Gravano D, Vogel P, Liu CL, Tangsombatvisit S, Grosso JF, Netto G, Smeltzer MP, Chaux A, Utz PJ, Workman CJ, Pardoll DM, Korman AJ, Drake CG, Vignali DAA (2012) Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T cell function to promote tumoral immune escape. Cancer Res 72:917–927. https://doi.org/10.1158/0008-5472.CAN-11-1620. (PMID: 10.1158/0008-5472.CAN-11-162022186141)
Xia W, Zou C, Chen H, Xie C, Hou M (2020) Immune checkpoint inhibitor induces cardiac injury through polarizing macrophages via modulating microRNA-34a/Kruppel-like factor 4 signaling. Cell Death Dis 11:575. https://doi.org/10.1038/s41419-020-02778-2. (PMID: 10.1038/s41419-020-02778-2327098787382486)
Ying H, Yang L, Qiao G, Li Z, Zhang L, Yin F, Xie D, Zhang J (2010) Cutting edge: CTLA-4–B7 interaction suppresses Th17 cell differentiation. J Immunol Baltim Md 1950 185:1375–1378. https://doi.org/10.4049/jimmunol.0903369. (PMID: 10.4049/jimmunol.0903369)
Zamami Y, Niimura T, Okada N, Koyama T, Fukushima K, Izawa-Ishizawa Y, Ishizawa K (2019) Factors associated with immune checkpoint inhibitor-related myocarditis. JAMA Oncol 5:1635–1637. https://doi.org/10.1001/jamaoncol.2019.3113. (PMID: 10.1001/jamaoncol.2019.3113314368026707099)
Zan H, Zhang J, Ardeshna S, Xu Z, Park S-R, Casali P (2009) Lupus-prone MRL/faslpr/lpr mice display increased AID expression and extensive DNA lesions, comprising deletions and insertions, in the immunoglobulin locus: concurrent upregulation of somatic hypermutation and class switch DNA recombination. Autoimmunity 42:89–103. https://doi.org/10.1080/08916930802629554. (PMID: 10.1080/08916930802629554191565533140875)
Zhang PL, Lun M, Teng J, Huang J, Blasick TM, Yin L, Herrera GA, Cheung JY (2004) Preinduced molecular chaperones in the endoplasmic reticulum protect cardiomyocytes from lethal injury. Ann Clin Lab Sci 34:449–457. (PMID: 15648788)
Zhang Y, Sun C, Li Y, Qin J, Amancherla K, Jing Y, Hu Q, Liang K, Zhang Z, Ye Y, Huang LA, Nguyen TK, Egranov SD, Zhao Z, Wu A, Xi Y, Yao J, Hung M-C, Calin GA, Cheng J, Lim B, Lehmann LH, Salem J-E, Johnson DB, Curran MA, Yu D, Han L, Darabi R, Yang L, Moslehi JJ, Lin C (2022) Hormonal therapies upregulate MANF and overcome female susceptibility to immune checkpoint inhibitor-myocarditis. Sci Transl Med 14:eabo1981. https://doi.org/10.1126/scitranslmed.abo1981. (PMID: 10.1126/scitranslmed.abo1981363226289809130)
معلومات مُعتمدة: RA 969/12-1 Deutsche Forschungsgemeinschaft; HE 6317/2-1 Deutsche Forschungsgemeinschaft; IFORES scholarship Medical Faculty, University Duisburg-Essen
فهرسة مساهمة: Keywords: Cardio-oncology; Cardiotoxicity; Cytotoxic T-lymphocyte-associated protein 4; Immune checkpoint inhibitor; Immune-related adverse events; Programmed cell death protein 1
تواريخ الأحداث: Date Created: 20240722 Latest Revision: 20240722
رمز التحديث: 20240723
DOI: 10.1007/s00395-024-01070-0
PMID: 39039301
قاعدة البيانات: MEDLINE
الوصف
تدمد:1435-1803
DOI:10.1007/s00395-024-01070-0