Journal Home > Volume 2 , Issue 6
Cancer Innovation 2023, 2(6): 439-447 https://doi.org/10.1002/cai2.100
Review | Open Access | Issue | Published: 28 November 2023

Advances in research on molecular markers in immune checkpoint inhibitor‐associated myocarditis

Show Author's Information Jun Shao1,,  Chuanbin Liu2,,  Jing Wang1 ( )
Department of General Medicine, First Medical Center of PLA General Hospital, Beijing, China
Western Medical Branch of PLA General Hospital, Beijing, China

Jun Shao and Chuanbin Liu contributed equally to this study and shared the first authorship.

Keywords:
immune checkpoint inhibitors, tumor immunotherapy, molecular marker, myocarditis
Cite this article:
Shao J, Liu C, Wang J. Advances in research on molecular markers in immune checkpoint inhibitor‐associated myocarditis. Cancer Innovation, 2023, 2(6): 439-447. https://doi.org/10.1002/cai2.100
Download citation
EndNote(RIS)
BibTeX

175

Views

23

Downloads

Citations

0

Crossref

N/A

WoS

0

Scopus

N/A

CSCD

Abstract Full text About this article

Immune checkpoint inhibitors (ICIs) play a crucial role in the immunotherapy of malignant tumors, preventing immune evasion by tumor cells and activating autoimmune cells to eliminate the tumor. Despite their proven effectiveness in antitumor therapy, potential immune‐related adverse effects must be recognized, particularly ICI‐associated myocarditis (ICIAM). ICIAM is the most lethal form of organ immunotoxicity, with a significant impact on short‐term mortality. However, ICIAM is predominantly asymptomatic or mildly nonspecific. It is difficult to diagnose, especially due to the lack of unique molecular markers. This article aims to provide a comprehensive overview of the progress made in identifying molecular markers for ICIAM.


menu
Abstract
Full text
Outline
About this article

Advances in research on molecular markers in immune checkpoint inhibitor‐associated myocarditis

Show Author's information Jun Shao1,, Chuanbin Liu2,, Jing Wang1 ( )
Department of General Medicine, First Medical Center of PLA General Hospital, Beijing, China
Western Medical Branch of PLA General Hospital, Beijing, China

Jun Shao and Chuanbin Liu contributed equally to this study and shared the first authorship.

Abstract

Immune checkpoint inhibitors (ICIs) play a crucial role in the immunotherapy of malignant tumors, preventing immune evasion by tumor cells and activating autoimmune cells to eliminate the tumor. Despite their proven effectiveness in antitumor therapy, potential immune‐related adverse effects must be recognized, particularly ICI‐associated myocarditis (ICIAM). ICIAM is the most lethal form of organ immunotoxicity, with a significant impact on short‐term mortality. However, ICIAM is predominantly asymptomatic or mildly nonspecific. It is difficult to diagnose, especially due to the lack of unique molecular markers. This article aims to provide a comprehensive overview of the progress made in identifying molecular markers for ICIAM.

Keywords: immune checkpoint inhibitors, tumor immunotherapy, molecular marker, myocarditis

References(85)

1

Moslehi J, Lichtman AH, Sharpe AH, Galluzzi L, Kitsis RN. Immune checkpoint inhibitor‐associated myocarditis: manifestations and mechanisms. J Clin Invest. 2021;131(5):e145186. https://doi.org/10.1172/jci145186
DOI Google Scholar
2

Donini C, Galvagno F, Rotolo R, Massa A, Merlini A, Scagliotti GV, et al. PD‐1 receptor outside the main paradigm: tumour‐intrinsic role and clinical implications for checkpoint blockade. Br J Cancer. 2023;129(9):1409–16. https://doi.org/10.1038/s41416-023-02363-2
DOI Google Scholar
3

Hosseini A, Gharibi T, Marofi F, Babaloo Z, Baradaran B. CTLA‐4: from mechanism to autoimmune therapy. Int Immunopharmacol. 2020;80:106221. https://doi.org/10.1016/j.intimp.2020.106221
DOI Google Scholar
4

Hu JR, Florido R, Lipson EJ, Naidoo J, Ardehali R, Tocchetti CG, et al. Cardiovascular toxicities associated with immune checkpoint inhibitors. Cardiovasc Res. 2019;115(5):854–68. https://doi.org/10.1093/cvr/cvz026
DOI Google Scholar
5

Dutta S, Ganguly A, Chatterjee K, Spada S, Mukherjee S. Targets of immune escape mechanisms in cancer: basis for development and evolution of cancer immune checkpoint inhibitors. Biology. 2023;12(2):218. https://doi.org/10.3390/biology12020218
DOI Google Scholar
6

Tocchetti CG, Cadeddu C, Di Lisi D, Femminò S, Madonna R, Mele D, et al. From molecular mechanisms to clinical management of antineoplastic drug‐induced cardiovascular toxicity: a translational overview. Antioxid Redox Signal. 2019;30(18):2110–53. https://doi.org/10.1089/ars.2016.6930
DOI Google Scholar
7

Herrmann J. Adverse cardiac effects of cancer therapies: cardiotoxicity and arrhythmia. Nat Rev Cardiol. 2020;17(8):474–502. https://doi.org/10.1038/s41569-020-0348-1
DOI Google Scholar
8

Ederhy S, Cautela J, Ancedy Y, Escudier M, Thuny F, Cohen A. Takotsubo‐like syndrome in cancer patients treated with immune checkpoint inhibitors. JACC Cardiovasc Imaging. 2018;11(8):1187–90. https://doi.org/10.1016/j.jcmg.2017.11.036
DOI Google Scholar
9

Yang S, Asnani A. Cardiotoxicities associated with immune checkpoint inhibitors. Curr Probl Cancer. 2018;42(4):422–32. https://doi.org/10.1016/j.currproblcancer.2018.07.002
DOI Google Scholar
10

Rubio‐Infante N, Ramírez‐Flores YA, Castillo EC, Lozano O, García‐Rivas G, Torre‐Amione G. Cardiotoxicity associated with immune checkpoint inhibitor therapy: a meta‐analysis. Eur J Heart Fail. 2021;23(10):1739–47. https://doi.org/10.1002/ejhf.2289
DOI Google Scholar
11

Wang DY, Salem JE, Cohen JV, Chandra S, Menzer C, Ye F, et al. Fatal toxic effects associated with immune checkpoint inhibitors: a systematic review and meta‐analysis. JAMA Oncol. 2018;4(12):1721–8. https://doi.org/10.1001/jamaoncol.2018.3923
DOI Google Scholar
12

Awadalla M, Mahmood SS, Groarke JD, Hassan MZO, Nohria A, Rokicki A, et al. Global longitudinal strain and cardiac events in patients with immune checkpoint inhibitor‐related myocarditis. J Am Coll Cardiol. 2020;75(5):467–78. https://doi.org/10.1016/j.jacc.2019.11.049
DOI Google Scholar
13

Johnson DB, Balko JM, Compton ML, Chalkias S, Gorham J, Xu Y, et al. Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med. 2016;375(18):1749–55. https://doi.org/10.1056/NEJMoa1609214
DOI Google Scholar
14

Yamaguchi S, Morimoto R, Okumura T, Yamashita Y, Haga T, Kuwayama T, et al. Late‐onset fulminant myocarditis with immune checkpoint inhibitor nivolumab. Can J Cardiol. 2018;34(6):812.e1–3. https://doi.org/10.1016/j.cjca.2018.03.007
DOI Google Scholar
15

Imai R, Ono M, Nishimura N, Suzuki K, Komiyama N, Tamura T. Fulminant myocarditis caused by an immune checkpoint inhibitor: a case report with pathologic findings. J Thorac Oncol. 2019;14(2):e36–8. https://doi.org/10.1016/j.jtho.2018.10.156
DOI Google Scholar
16

Topalian SL, Taube JM, Pardoll DM. Neoadjuvant checkpoint blockade for cancer immunotherapy. Science. 2020;367(6477):eaax0182. https://doi.org/10.1126/science.aax0182
DOI Google Scholar
17

Chhabra N, Kennedy J. A review of cancer immunotherapy toxicity: immune checkpoint inhibitors. J Med Toxicol. 2021;17(4):411–24. https://doi.org/10.1007/s13181-021-00833-8
DOI Google Scholar
18

Patel RP, Parikh R, Gunturu KS, Tariq RZ, Dani SS, Ganatra S, et al. Cardiotoxicity of immune checkpoint inhibitors. Curr Oncol Rep. 2021;23(7):79. https://doi.org/10.1007/s11912-021-01070-6
DOI Google Scholar
19

Mahmood SS, Fradley MG, Cohen JV, Nohria A, Reynolds KL, Heinzerling LM, et al. Myocarditis in patients treated with immune checkpoint inhibitors. J Am Coll Cardiol. 2018;71(16):1755–64. https://doi.org/10.1016/j.jacc.2018.02.037
DOI Google Scholar
20

Salem JE, Manouchehri A, Moey M, Lebrun‐Vignes B, Bastarache L, Pariente A, et al. Cardiovascular toxicities associated with immune checkpoint inhibitors: an observational, retrospective, pharmacovigilance study. Lancet Oncol. 2018;19(12):1579–89. https://doi.org/10.1016/s1470-2045(18)30608-9
DOI Google Scholar
21

Dolladille C, Akroun J, Morice PM, Dompmartin A, Ezine E, Sassier M, et al. Cardiovascular immunotoxicities associated with immune checkpoint inhibitors: a safety meta‐analysis. Eur Heart J. 2021;42(48):4964–77. https://doi.org/10.1093/eurheartj/ehab618
DOI Google Scholar
22

Schneider BJ, Naidoo J, Santomasso BD, Lacchetti C, Adkins S, Anadkat M, et al. Management of immune‐related adverse events in patients treated with immune checkpoint inhibitor therapy: ASCO guideline update. J Clin Oncol. 2021;39(36):4073–126. https://doi.org/10.1200/jco.21.01440
DOI Google Scholar
23

Lyon AR, López‐Fernández T, Couch LS, Asteggiano R, Aznar MC, Bergler‐Klein J, et al. 2022 ESC Guidelines on cardio‐oncology developed in collaboration with the European Hematology Association (EHA), the European Society for Therapeutic Radiology and Oncology (ESTRO) and the International Cardio‐Oncology Society (IC‐OS). Eur Heart J. 2022;43(41):4229–361. https://doi.org/10.1093/eurheartj/ehac244
DOI Google Scholar
24

Sury K, Perazella MA, Shirali AC. Cardiorenal complications of immune checkpoint inhibitors. Nat Rev Nephrol. 2018;14(9):571–88. https://doi.org/10.1038/s41581-018-0035-1
DOI Google Scholar
25

Zhang C, Chen ZL, Mo CH, Gao DS, Zhu YX, Qin S, et al. Real‐world cardiovascular toxicity of immune checkpoint inhibitors in cancer patients: a retrospective controlled cohort study. Am J Cancer Res. 2021;11(12):6074–85.
Google Scholar
26

Li CH, Bhatti SA, Ying J. Immune checkpoint inhibitors‐associated cardiotoxicity. Cancers. 2022;14(5):1145. https://doi.org/10.3390/cancers14051145
DOI Google Scholar
27

Dolladille C, Ederhy S, Allouche S, Dupas Q, Gervais R, Madelaine J, et al. Late cardiac adverse events in patients with cancer treated with immune checkpoint inhibitors. J Immunother Cancer. 2020;8(1):e000261. https://doi.org/10.1136/jitc-2019-000261
DOI Google Scholar
28

Hu JX, Tian RY, Ma YJ, Zhen HC, Ma X, Su Q, et al. Risk of cardiac adverse events in patients treated with immune checkpoint inhibitor regimens: a systematic review and meta‐analysis. Front Oncol. 2021;11:645245. https://doi.org/10.3389/fonc.2021.645245
DOI Google Scholar
29

Stein‐Merlob AF, Rothberg MV, Ribas A, Yang EH. Cardiotoxicities of novel cancer immunotherapies. Heart. 2021;107(21):1694–703. https://doi.org/10.1136/heartjnl-2020-318083
DOI Google Scholar
30

Zhou YW, Zhu YJ, Wang MN, Xie Y, Chen CY, Zhang T, et al. Immune checkpoint inhibitor‐associated cardiotoxicity: current understanding on its mechanism, diagnosis and management. Front Pharmacol. 2019;10:1350. https://doi.org/10.3389/fphar.2019.01350
DOI Google Scholar
31

Goitein O, Matetzky S, Beinart R, Di Segni E, Hod H, Bentancur A, et al. Acute myocarditis: noninvasive evaluation with cardiac MRI and transthoracic echocardiography. Am J Roentgenol. 2009;192(1):254–8. https://doi.org/10.2214/ajr.08.1281
DOI Google Scholar
32

Ammirati E, Moslehi JJ. Diagnosis and treatment of acute myocarditis: a review. JAMA. 2023;329(13):1098–113. https://doi.org/10.1001/jama.2023.3371
DOI Google Scholar
33

Moreira A, Loquai C, Pföhler C, Kähler KC, Knauss S, Heppt MV, et al. Myositis and neuromuscular side‐effects induced by immune checkpoint inhibitors. Eur J Cancer. 2019;106:12–23. https://doi.org/10.1016/j.ejca.2018.09.033
DOI Google Scholar
34

Grabie N, Lichtman AH, Padera R. T cell checkpoint regulators in the heart. Cardiovasc Res. 2019;115(5):869–77. https://doi.org/10.1093/cvr/cvz025
DOI Google Scholar
35

Zito C, Manganaro R, Ciappina G, Spagnolo CC, Racanelli V, Santarpia M, et al. Cardiotoxicity induced by immune checkpoint inhibitors: what a cardio‐oncology team should know and do. Cancers. 2022;14(21):5403. https://doi.org/10.3390/cancers14215403
DOI Google Scholar
36

Grabie N, Gotsman I, DaCosta R, Pang H, Stavrakis G, Butte MJ, et al. Endothelial programmed death‐1 ligand 1 (PD‐L1) regulates CD8+ T‐cell mediated injury in the heart. Circulation. 2007;116(18):2062–71. https://doi.org/10.1161/circulationaha.107.709360
DOI Google Scholar
37

Wang SJ, Dougan SK, Dougan M. Immune mechanisms of toxicity from checkpoint inhibitors. Trends Cancer. 2023;9(7):543–53. https://doi.org/10.1016/j.trecan.2023.04.002
DOI Google Scholar
38

Cihakova D, Rose NR. Pathogenesis of myocarditis and dilated cardiomyopathy. Adv Immunol. 2008;99:95–114. https://doi.org/10.1016/s0065-2776(08)00604-4
DOI Google Scholar
39

Caforio ALP, Bonifacio E, Stewart JT, Neglia D, Parodi O, Bottazzo GF, et al. Novel organ‐specific circulating cardiac autoantibodies in dilated cardiomyopathy. J Am Coll Cardiol. 1990;15(7):1527–34. https://doi.org/10.1016/0735-1097(90)92821-i
DOI Google Scholar
40

Caforio ALP, Goldman JH, Haven AJ, Baig KM, Libera LD, McKenna WJ. Circulating cardiac‐specific autoantibodies as markers of autoimmunity in clinical and biopsy‐proven myocarditis. Eur Heart J. 1997;18(2):270–5. https://doi.org/10.1093/oxfordjournals.eurheartj.a015230
DOI Google Scholar
41

Neumann DA, Lynne Burek C, Baughman KL, Rose NR, Herskowitz A. Circulating heart‐reactive antibodies in patients with myocarditis or cardiomyopathy. J Am Coll Cardiol. 1990;16(6):839–46. https://doi.org/10.1016/s0735-1097(10)80331-6
DOI Google Scholar
42

Lucas JA, Menke J, Rabacal WA, Schoen FJ, Sharpe AH, Kelley VR. Programmed death ligand 1 regulates a critical checkpoint for autoimmune myocarditis and pneumonitis in MRL mice. J Immunol. 2008;181(4):2513–21. https://doi.org/10.4049/jimmunol.181.4.2513
DOI Google Scholar
43

Lipes MA, Galderisi A. Cardiac autoimmunity as a novel biomarker, mediator, and therapeutic target of heart disease in type 1 diabetes. Curr Diab Rep. 2015;15(5):30. https://doi.org/10.1007/s11892-015-0598-1
DOI Google Scholar
44

Caforio AL, Grazzini M, Mann JM, Keeling PJ, Bottazzo GF, McKenna WJ, et al. Identification of alpha‐ and beta‐cardiac myosin heavy chain isoforms as major autoantigens in dilated cardiomyopathy. Circulation. 1992;85(5):1734–42. https://doi.org/10.1161/01.cir.85.5.1734
DOI Google Scholar
45

Lv H, Havari E, Pinto S, Gottumukkala RVSRK, Cornivelli L, Raddassi K, et al. Impaired thymic tolerance to α‐myosin directs autoimmunity to the heart in mice and humans. J Clin Invest. 2011;121(4):1561–73. https://doi.org/10.1172/jci44583
DOI Google Scholar
46

Gottumukkala RVSRK, Lv H, Cornivelli L, Wagers AJ, Kwong RY, Bronson R, et al. Myocardial infarction triggers chronic cardiac autoimmunity in type 1 diabetes. Sci Transl Med. 2012;4(138):138ra80. https://doi.org/10.1126/scitranslmed.3003551
DOI Google Scholar
47

Ma GY, Wang C, Lv BY, Jiang YZ, Wang L. Proteinase‐activated receptor‐2 enhances Bcl2‐like protein‐12 expression in lung cancer cells to suppress p53 expression. Arch Med Sci. 2019;15(5):1147–53. https://doi.org/10.5114/aoms.2019.86980
DOI Google Scholar
48

Stegh AH, Brennan C, Mahoney JA, Forloney KL, Jenq HT, Luciano JP, et al. Glioma oncoprotein Bcl2L12 inhibits the p53 tumor suppressor. Genes Dev. 2010;24(19):2194–204. https://doi.org/10.1101/gad.1924710
DOI Google Scholar
49

Li JX, Yang G, Luo XQ, Mo LH, Qiu SY, Yang LT, et al. Interaction between Ras and Bcl2L12 in B cells suppresses IL‐10 expression. Clin Immunol. 2021;229:108775. https://doi.org/10.1016/j.clim.2021.108775
DOI Google Scholar
50

Xue JM, Yang LT, Yang G, Geng XR, Liu ZQ, Wang S, et al. Protease‐activated receptor‐2 suppresses interleukin (IL)‐10 expression in B cells via upregulating Bcl2L12 in patients with allergic rhinitis. Allergy. 2017;72(11):1704–12. https://doi.org/10.1111/all.13186
DOI Google Scholar
51

Guo X, Li MG, Li SS, Liu FH, Liu ZJ, Yang PC. Tumor necrosis factor suppresses interleukin 10 in peripheral B cells via upregulating Bcl2‐like protein 12 in patients with inflammatory bowel disease. Cell Biochem Funct. 2017;35(2):77–82. https://doi.org/10.1002/cbf.3250
DOI Google Scholar
52

Chen X, Zeng XH, Wang M, Chen L, Zhang N, Rao M, et al. Bcl2‐Like protein 12 is required for the aberrant T Helper‐2 polarization in the heart by enhancing Interleukin‐4 expression and compromising apoptotic machinery in CD4+ T cells. Circulation. 2018;138(22):2559–68. https://doi.org/10.1161/circulationaha.118.033890
DOI Google Scholar
53

Hang W, Chen C, Seubert JM, Wang DW. Fulminant myocarditis: a comprehensive review from etiology to treatments and outcomes. Signal Transduct Target Ther. 2020;5(1):287. https://doi.org/10.1038/s41392-020-00360-y
DOI Google Scholar
54

Ji C, Roy MD, Golas J, Vitsky A, Ram S, Kumpf SW, et al. Myocarditis in cynomolgus monkeys following treatment with immune checkpoint inhibitors. Clin Cancer Res. 2019;25(15):4735–48. https://doi.org/10.1158/1078-0432.Ccr-18-4083
DOI Google Scholar
55

Humblin E, Kamphorst AO. CXCR3‐CXCL9: it's all in the tumor. Immunity. 2019;50(6):1347–9. https://doi.org/10.1016/j.immuni.2019.05.013
DOI Google Scholar
56

Aldinucci D, Borghese C, Casagrande N. The CCL5/CCR5 axis in cancer progression. Cancers. 2020;12(7):1765. https://doi.org/10.3390/cancers12071765
DOI Google Scholar
57

Lu HX, Zong GJ, Zhou SS, Jiang YY, Chen R, Su ZL, et al. Angiotensin Ⅱ‐C‐C chemokine receptor2/5 axis‐dependent monocyte/macrophage recruitment contributes to progression of experimental autoimmune myocarditis. Microbiol Immunol. 2017;61(12):539–46. https://doi.org/10.1111/1348-0421.12548
DOI Google Scholar
58

Hunter CA, Jones SA. IL‐6 as a keystone cytokine in health and disease. Nature Immunol. 2015;16(5):448–57. https://doi.org/10.1038/ni.3153
DOI Google Scholar
59

Huseni MA, Wang L, Klementowicz JE, Yuen K, Breart B, Orr C, et al. CD8+ T cell‐intrinsic IL‐6 signaling promotes resistance to anti‐PD‐L1 immunotherapy. Cell Rep Med. 2023;4(1):100878. https://doi.org/10.1016/j.xcrm.2022.100878
DOI Google Scholar
60

Liu LH, Shi ZH, Ji XH, Zhang WQ, Luan JW, Zahr T, et al. Adipokines, adiposity, and atherosclerosis. Cell Mol Life Sci. 2022;79(5):272. https://doi.org/10.1007/s00018-022-04286-2
DOI Google Scholar
61

Qu D, Liu J, Lau CW, Huang Y. IL‐6 in diabetes and cardiovascular complications. Br J Pharmacol. 2014;171(15):3595–603. https://doi.org/10.1111/bph.12713
DOI Google Scholar
62

Jiang WY, Lian JY, Yue Y, Zhang Y. IL‐33/ST2 as a potential target for tumor immunotherapy. Eur J Immunol. 2021;51(8):1943–55. https://doi.org/10.1002/eji.202149175
DOI Google Scholar
63

Heidenreich PA, Bozkurt B, Aguilar D, Allen LA, Byun JJ, Colvin MM, et al. 2022 AHA/ACC/HFSA guideline for the management of heart failure: executive summary: a report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. Circulation. 2022;145(18):e876–94. https://doi.org/10.1161/cir.0000000000001062
DOI Google Scholar
64

Meijers WC, Bayes‐Genis A, Mebazaa A, Bauersachs J, Cleland JGF, Coats AJS, et al. Circulating heart failure biomarkers beyond natriuretic peptides: review from the Biomarker Study Group of the Heart Failure Association (HFA), European Society of Cardiology (ESC). Eur J Heart Fail. 2021;23(10):1610–32. https://doi.org/10.1002/ejhf.2346
DOI Google Scholar
65

Li Z, Wang Y, Lin JY, Zhao SH, Chen JH, Zhou YH, et al. Predictive value of soluble growth‐stimulated expression gene 2 protein on the prognosis of immune checkpoint inhibitor‐associated myocarditis (in Chinese). Chinese Journal of Clinical Medicine. 2021;28(02):159–63.
Google Scholar
66

Wang J, He MY, Li HH, Chen YH, Nie X, Cai YY, et al. Soluble ST2 is a sensitive and specific biomarker for fulminant myocarditis. J Am Heart Assoc. 2022;11(7):e024417. https://doi.org/10.1161/jaha.121.024417
DOI Google Scholar
67

Bayés‐Genis A, González A, Lupón J. ST2 in heart failure. Circ Heart Fail. 2018;11(12):e005582. https://doi.org/10.1161/circheartfailure.118.005582
DOI Google Scholar
68

Asensio‐Lopez MC, Sassi Y, Soler F, Fernandez Del Palacio MJ, Pascual‐Figal D, Lax A. The miRNA199a/SIRT1/P300/Yy1/sST2 signaling axis regulates adverse cardiac remodeling following MI. Sci Rep. 2021;11(1):3915. https://doi.org/10.1038/s41598-021-82745-9
DOI Google Scholar
69

Van der Jeught K, Sun Y, Fang Y, Zhou Z, Jiang H, Yu T, et al. ST2 as checkpoint target for colorectal cancer immunotherapy. JCI Insight. 2020;5(9):e136073. https://doi.org/10.1172/jci.insight.136073
DOI Google Scholar
70

Kakkar R, Lee RT. The IL‐33/ST2 pathway: therapeutic target and novel biomarker. Nat Rev Drug Discov. 2008;7(10):827–40. https://doi.org/10.1038/nrd2660
DOI Google Scholar
71

Marjot J, Kaier TE, Martin ED, Reji SS, Copeland O, Iqbal M, et al. Quantifying the release of biomarkers of myocardial necrosis from cardiac myocytes and intact myocardium. Clin Chem. 2017;63(5):990–6. https://doi.org/10.1373/clinchem.2016.264648
DOI Google Scholar
72

Petricciuolo S, Delle Donne MG, Aimo A, Chella A, De Caterina R. Pre‐treatment high‐sensitivity troponin T for the short‐term prediction of cardiac outcomes in patients on immune checkpoint inhibitors. Eur J Clin Invest. 2021;51(4):e13400. https://doi.org/10.1111/eci.13400
DOI Google Scholar
73

Yuan M, Zang L, Xu AQ, Gong MQ, Liu Q, Huo B, et al. Dynamic changes of serum heart type‐fatty acid binding protein in cancer patients treated with immune checkpoint inhibitors. Front Pharmacol. 2021;12:748677. https://doi.org/10.3389/fphar.2021.748677
DOI Google Scholar
74

Pozniak T, Shcharbin D, Bryszewska M. Circulating microRNAs in medicine. Int J Mol Sci. 2022;23(7):3996. https://doi.org/10.3390/ijms23073996
DOI Google Scholar
75

Climent M, Viggiani G, Chen YW, Coulis G, Castaldi A. MicroRNA and ROS crosstalk in cardiac and pulmonary diseases. Int J Mol Sci. 2020;21(12):4370. https://doi.org/10.3390/ijms21124370
DOI Google Scholar
76

Wang GK, Zhu JQ, Zhang JT, Li Q, Li Y, He J, et al. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J. 2010;31(6):659–66. https://doi.org/10.1093/eurheartj/ehq013
DOI Google Scholar
77

Blanco‐Domínguez R, Sánchez‐Díaz R, de la Fuente H, Jiménez‐Borreguero LJ, Matesanz‐Marín A, Relaño M, et al. A novel circulating noncoding small RNA for the detection of acute myocarditis. N Engl J Med. 2021;384(21):2014–27. https://doi.org/10.1056/NEJMoa2003608
DOI Google Scholar
78

Wang J, Han B. Dysregulated CD4+ T cells and microRNAs in myocarditis. Front Immunol. 2020;11:539. https://doi.org/10.3389/fimmu.2020.00539
DOI Google Scholar
79

Zhang F, Jiang JJ, Qian H, Yan YM, Xu WR. Exosomal circRNA: emerging insights into cancer progression and clinical application potential. J Hematol Oncol. 2023;16(1):67. https://doi.org/10.1186/s13045-023-01452-2
DOI Google Scholar
80

Tang Y, Bao J, Hu J, Liu L, Xu DY. Circular RNA in cardiovascular disease: expression, mechanisms and clinical prospects. J Cell Mol Med. 2021;25(4):1817–24. https://doi.org/10.1111/jcmm.16203
DOI Google Scholar
81

Mei XH, Chen SY. Circular RNAs in cardiovascular diseases. Pharmacol Ther. 2022;232:107991. https://doi.org/10.1016/j.pharmthera.2021.107991
DOI Google Scholar
82

Zhang L, Han B, Wang J, Liu QQ, Kong Y, Jiang DD, et al. Differential expression profiles and functional analysis of circular RNAs in children with fulminant myocarditis. Epigenomics. 2019;11(10):1129–41. https://doi.org/10.2217/epi-2019-0101
DOI Google Scholar
83

Zhang L, Han B, Liu H, Wang J, Feng X, Sun W, et al. Circular RNA circACSL1 aggravated myocardial inflammation and myocardial injury by sponging miR‐8055 and regulating MAPK14 expression. Cell Death Dis. 2021;12(5):487. https://doi.org/10.1038/s41419-021-03777-7
DOI Google Scholar
84

Ganesh S, Zhong P, Zhou XY. Cardiotoxicity induced by immune checkpoint inhibitor: the complete insight into mechanisms, monitoring, diagnosis, and treatment. Front Cardiovasc Med. 2022;9:997660. https://doi.org/10.3389/fcvm.2022.997660
DOI Google Scholar
85

Michel L, Helfrich I, Hendgen‐Cotta UB, Mincu RI, Korste S, Mrotzek SM, et al. Targeting early stages of cardiotoxicity from anti‐PD1 immune checkpoint inhibitor therapy. Eur Heart J. 2022;43(4):316–29. https://doi.org/10.1093/eurheartj/ehab430
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 30 June 2023
Accepted: 04 September 2023
Published: 28 November 2023
Issue date: December 2023

Copyright

© 2023 The Authors. Tsinghua University Press.

Acknowledgements

ACKNOWLEDGMENTS

None.

Rights and permissions

This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial‐NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

Return