Human induced pluripotent stem cell-derived cardiomyocytes as an in vitro model for coxsackievirus B3-induced myocarditis and antiviral drug screening platform

Circulation Research

Volumn 115, Issue 6, 2014, Pages 556-566

  Sharma, Arun ^a   Marceau, Caleb ^a   Hamaguchi, Ryoko ^a   Burridge, Paul W ^a   Rajarajan, Kuppusamy ^a   Churko, Jared M ^a   Wu, Haodi ^a   Sallam, Karim I ^a   Matsa, Elena ^a   Sturzu, Anthony C ^a   Che, Yonglu ^a   Ebert, Antje ^a   Diecke, Sebastian ^a   Liang, Ping ^a   Red Horse, Kristy ^a   Carette, Jan E ^a   Wu, Sean M ^a   Wu, Joseph C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cardiac; myocarditis; myocytes; stem cells

Indexed keywords

ALPHA ACTININ; ALPHA SMOOTH MUSCLE ACTIN; ANTIVIRUS AGENT; BETA1 INTERFERON; CALCIUM; FLUOXETINE; PYRROLIDINE DITHIOCARBAMATE; RENILLA LUCIFERIN 2 MONOOXYGENASE; RIBAVIRIN; TROPONIN T; VIRUS PROTEIN; VIRUS RNA;

ANTIVIRAL ACTIVITY; ARTICLE; BIOLUMINESCENCE; CALCIUM CELL LEVEL; CELL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; COXSACKIE VIRUS B3; CYTOPATHOGENIC EFFECT; DRUG EFFICACY; DRUG SCREENING; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; NONHUMAN; NORMAL HUMAN; PATHOGENESIS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VIRAL CLEARANCE; VIRUS CAPSID; VIRUS MYOCARDITIS; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN;

MYOCARDITIS; MYOCYTES, CARDIAC; STEM CELLS;

ANTIVIRAL AGENTS; CALCIUM; CELL PROLIFERATION; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; ENTEROVIRUS B, HUMAN; ENTEROVIRUS INFECTIONS; HUMANS; MODELS, CARDIOVASCULAR; MYOCARDITIS; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; RNA, VIRAL; TREATMENT OUTCOME;

EID: 84907140891     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.303810     Document Type: Article

References (50)

1. Cooper LT Jr. Myocarditis. N Engl J Med. 2009;360:1526-1538.
2. Dec GW Jr, Palacios IF, Fallon JT, Aretz HT, Mills J, Lee DC, Johnson RA. Active myocarditis in the spectrum of acute dilated cardiomyopathies. Clinical features, histologic correlates, and clinical outcome. N Engl J Med. 1985;312:885-890.
3. Drory Y, Turetz Y, Hiss Y, Lev B, Fisman EZ, Pines A, Kramer MR. Sudden unexpected death in persons less than 40 years of age. Am J Cardiol. 1991;68:1388-1392.
4. Maron BJ, Doerer JJ, Haas TS, Tierney DM, Mueller FO. Sudden deaths in young competitive athletes: analysis of 1866 deaths in the United States, 1980-2006. Circulation. 2009;119:1085-1092.
5. Baughman KL. Diagnosis of myocarditis: death of Dallas criteria. Circulation. 2006;113:593-595.
6. Feldman AM, McNamara D. Myocarditis. N Engl J Med. 2000;343:1388-1398.
7. Bowles NE, Richardson PJ, Olsen EG, Archard LC. Detection of Coxsackie-B-virus-specific RNA sequences in myocardial biopsy samples from patients with myocarditis and dilated cardiomyopathy. Lancet. 1986;1:1120-1123.
8. Kim KS, Hufnagel G, Chapman NM, Tracy S. The group B coxsackieviruses and myocarditis. Rev Med Virol. 2001;11:355-368.
9. Knowlton KU. CVB infection and mechanisms of viral cardiomyopathy. Curr Top Microbiol Immunol. 2008;323:315-335.
10. Kandolf R, Canu A, Hofschneider PH. Coxsackie B3 virus can replicate in cultured human foetal heart cells and is inhibited by interferon. J Mol Cell Cardiol. 1985;17:167-181.
11. Asher DR, Cerny AM, Weiler SR, Horner JW, Keeler ML, Neptune MA, Jones SN, Bronson RT, Depinho RA, Finberg RW. Coxsackievirus and adenovirus receptor is essential for cardiomyocyte development. Genesis. 2005;42:77-85.
12. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci USA. 2001;98:15191-15196.
13. Nalbantoglu J, Pari G, Karpati G, Holland PC. Expression of the primary coxsackie and adenovirus receptor is downregulated during skeletal muscle maturation and limits the efficacy of adenovirus-mediated gene delivery to muscle cells. Hum Gene Ther. 1999;10:1009-1019.
14. Kashimura T, Kodama M, Hotta Y, Hosoya J, Yoshida K, Ozawa T, Watanabe R, Okura Y, Kato K, Hanawa H, Kuwano R, Aizawa Y. Spatiotemporal changes of coxsackievirus and adenovirus receptor in rat hearts during postnatal development and in cultured cardiomyocytes of neonatal rat. Virchows Arch. 2004;444:283-292.
15. Fechner H, Noutsias M, Tschoepe C, Hinze K, Wang X, Escher F, Pauschinger M, Dekkers D, Vetter R, Paul M, Lamers J, Schultheiss HP, Poller W. Induction of coxsackievirus-adenovirus-receptor expression during myocardial tissue formation and remodeling: identification of a cell-to-cell contact-dependent regulatory mechanism. Circulation. 2003;107:876-882.
16. Noutsias M, Fechner H, de Jonge H, Wang X, Dekkers D, Houtsmuller AB, Pauschinger M, Bergelson J, Warraich R, Yacoub M, Hetzer R, Lamers J, Schultheiss HP, Poller W. Human coxsackie-adenovirus receptor is colocalized with integrins alpha(v)beta(3) and alpha(v)beta(5) on the cardiomyocyte sarcolemma and upregulated in dilated cardiomyopathy: implications for cardiotropic viral infections. Circulation. 2001;104:275-280.
17. Mitcheson JS, Hancox JC, Levi AJ. Cultured adult cardiac myocytes: future applications, culture methods, morphological and electrophysiological properties. Cardiovasc Res. 1998;39:280-300.
18. Lombardi R, Bell A, Senthil V, Sidhu J, Noseda M, Roberts R, Marian AJ. Differential interactions of thin filament proteins in two cardiac troponin T mouse models of hypertrophic and dilated cardiomyopathies. Cardiovasc Res. 2008;79:109-117.
19. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917-1920.
20. Burridge PW, Keller G, Gold JD, Wu JC. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell. 2012;10:16-28.
21. Mukherjee A, Morosky SA, Delorme-Axford E, Dybdahl-Sissoko N, Oberste MS, Wang T, Coyne CB. The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog. 2011;7:e1001311.
22. Carthy CM, Granville DJ, Watson KA, Anderson DR, Wilson JE, Yang D, Hunt DW, McManus BM. Caspase activation and specific cleavage of substrates after coxsackievirus B3-induced cytopathic effect in HeLa cells. J Virol. 1998;72:7669-7675.
23. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA. 1998;95:2979-2984.
24. Rotbart HA. Treatment of picornavirus infections. Antiviral Res. 2002;53: 83-98.
25. Sun N, Yazawa M, Liu J, et al. Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy. Sci Transl Med. 2012;4:130ra47.
26. Churko JM, Burridge PW, Wu JC. Generation of human iPSCs from human peripheral blood mononuclear cells using non-integrative Sendai virus in chemically defined conditions. Methods Mol Biol. 2013;1036:81-88.
27. Lian X, Hsiao C, Wilson G, Zhu K, Hazeltine LB, Azarin SM, Raval KK, Zhang J, Kamp TJ, Palecek SP. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc Natl Acad Sci USA. 2012;109:E1848-E1857.
28. Tohyama S, Hattori F, Sano M, Hishiki T, Nagahata Y, Matsuura T, Hashimoto H, Suzuki T, Yamashita H, Satoh Y, Egashira T, Seki T, Muraoka N, Yamakawa H, Ohgino Y, Tanaka T, Yoichi M, Yuasa S, Murata M, Suematsu M, Fukuda K. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell. 2013;12:127-137.
29. Lanke KH, van der Schaar HM, Belov GA, Feng Q, Duijsings D, Jackson CL, Ehrenfeld E, van Kuppeveld FJ. GBF1, a guanine nucleotide exchange factor for Arf, is crucial for coxsackievirus B3 RNA replication. J Virol. 2009;83:11940-11949.
30. Dorner AA, Wegmann F, Butz S, Wolburg-Buchholz K, Wolburg H, Mack A, Nasdala I, August B, Westermann J, Rathjen FG, Vestweber D. Coxsackievirus- adenovirus receptor (CAR) is essential for early embryonic cardiac development. J Cell Sci. 2005;118:3509-3521.
31. Kim KS, Hufnagel G, Chapman NM, Tracy S. The group B coxsackieviruses and myocarditis. Rev Med Virol. 2001;11:355-368.
32. Pinkert S, Klingel K, Lindig V, Dörner A, Zeichhardt H, Spiller OB, Fechner H. Virus-host coevolution in a persistently coxsackievirus B3-infected cardiomyocyte cell line. J Virol. 2011;85:13409-13419.
33. Scassa ME, Jaquenod de Giusti C, Questa M, Pretre G, Richardson GA, Bluguermann C, Romorini L, Ferrer MF, Sevlever GE, Miriuka SG, Gómez RM. Human embryonic stem cells and derived contractile embryoid bodies are susceptible to Coxsakievirus B infection and respond to interferon Iβ treatment. Stem Cell Res. 2011;6:13-22.
34. Kühl U, Pauschinger M, Schwimmbeck PL, Seeberg B, Lober C, NoutsiasM, Poller W, Schultheiss HP. Interferon-beta treatment eliminates cardiotropic viruses and improves left ventricular function in patients with myocardial persistence of viral genomes and left ventricular dysfunction. Circulation. 2003;107:2793-2798.
35. Gale M Jr, Katze MG. Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol Ther. 1998;78:29-46.
36. Heim A, Grumbach I, Pring-Akerblom P, Stille-Siegener M, Müller G, Kandolf R, Figulla HR. Inhibition of coxsackievirus B3 carrier state infection of cultured human myocardial fibroblasts by ribavirin and human natural interferon-alpha. Antiviral Res. 1997;34:101-111.
37. Zuo J, Quinn KK, Kye S, Cooper P, Damoiseaux R, Krogstad P. Fluoxetine is a potent inhibitor of coxsackievirus replication. Antimicrob Agents Chemother. 2012;56:4838-4844.
38. Si X, McManus BM, Zhang J, Yuan J, Cheung C, Esfandiarei M, Suarez A, Morgan A, Luo H. Pyrrolidine dithiocarbamate reduces coxsackievirus B3 replication through inhibition of the ubiquitin-proteasome pathway. J Virol. 2005;79:8014-8023.
39. Lanke K, Krenn BM, Melchers WJ, Seipelt J, van Kuppeveld FJ. PDTC inhibits picornavirus polyprotein processing and RNA replication by transporting zinc ions into cells. J Gen Virol. 2007;88:1206-1217.
40. Deonarain R, Cerullo D, Fuse K, Liu PP, Fish EN. Protective role for interferon-beta in coxsackievirus B3 infection. Circulation. 2004;110:3540-3543.
41. Lundy SD, Zhu WZ, Regnier M, Laflamme MA. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev. 2013;22:1991-2002.
42. Saraste A, Arola A, Vuorinen T, Kytö V, Kallajoki M, Pulkki K, Voipio-Pulkki LM, Hyypiä T. Cardiomyocyte apoptosis in experimental coxsackievirus B3 myocarditis. Cardiovasc Pathol. 2003;12:255-262.
43. Badorff C, Lee GH, Lamphear BJ, Martone ME, Campbell KP, Rhoads RE, Knowlton KU. Enteroviral protease 2A cleaves dystrophin: evidence of cytoskeletal disruption in an acquired cardiomyopathy. Nat Med. 1999;5:320-326.
44. Cunningham MW, Antone SM, Gulizia JM, McManus BM, Fischetti VA, Gauntt CJ. Cytotoxic and viral neutralizing antibodies crossreact with streptococcal M protein, enteroviruses, and human cardiac myosin. Proc Natl Acad Sci USA. 1992;89:1320-1324.
45. Kannankeril PJ, Roden DM. Drug-induced long QT and torsade de pointes: recent advances. Curr Opin Cardiol. 2007;22:39-43.
46. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev. 2001;14:778-809.
47. Crotty S, Maag D, Arnold JJ, Zhong W, Lau JY, Hong Z, Andino R, Cameron CE. The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen. Nat Med. 2000;6:1375-1379.
48. Graudins A, Vossler C, Wang R. Fluoxetine-induced cardiotoxicity with response to bicarbonate therapy. Am J Emerg Med. 1997;15: 501-503.
49. Matsa E, Burridge PW, Wu JC. Human stem cells for modeling heart disease and for drug discovery. Sci Transl Med. 2014;6:239ps6.
50. Mordwinkin NM, Lee AS, Wu JC. Patient-specific stem cells and cardiovascular drug discovery. JAMA. 2013;310:2039-2040.