Transgenic expression of replication-restricted enteroviral genomes in heart muscle induces defective excitation-contraction coupling and dilated cardiomyopathy

Journal of Clinical Investigation

Volumn 102, Issue 7, 1998, Pages 1444-1453

  Wessely, Rainer ^a,d   Klingel, Karin ^b   Santana, L F ^c   Dalton, Nancy ^a   Hongo, Minoru ^a   Lederer, W Jonathan ^c   Kandolf, Reinhard ^b   Knowlton, Kirk U ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Calcium; Enterovirus; Heart failure; Myocarditis; Picornavirus

Indexed keywords

CALCIUM; COMPLEMENTARY DNA; MESSENGER RNA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; COXSACKIE VIRUS B3; ENTEROVIRUS; GENE EXPRESSION; HEART DILATATION; HEART FAILURE; MOUSE; NONHUMAN; PICORNAVIRUS; PRIORITY JOURNAL; TRANSGENIC MOUSE; VIRUS GENOME; VIRUS MYOCARDITIS; VIRUS REPLICATION;

EID: 0032189260     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1972     Document Type: Article

References (48)

1. Martino, T.A., P. Liu, and M.J. Sole. 1994. Viral infection and the pathogenesis of dilated cardiomyopathy. Circ. Res. 74:182-188.
2. Kandolf, R., K. Klingel, R. Zell, H.C. Selinka, U. Raab, W. Schneider-Brachert, and B. Bultmann. 1993. Molecular pathogenesis of enterovirus-induced myocarditis: virus persistence and chronic inflammation. Intervirology. 35:140-151.
3. Hosenpud, J.D., R.J. Novick, L.E. Bennett, B.M. Keck, B. Fiol, and O.P. Daily. 1996. The Registry of the International Society for Heart and Lung Transplantation: thirteenth official report - 1996. J. Heart Lung Transplant. 15: 655-674.
4. McManus, B.M., and R. Kandolf. 1991. Evolving concepts of cause, consequence, and control in myocarditis. Curr. Opin. Cardiol. 6:418-427.
5. Klingel, K., C. Hohenadl, A. Canu, M. Albrecht, M. Seemann, G. Mall, and R. Kandolf. 1992. Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proc. Natl. Acad. Sci. USA. 89:314-318.
6. Borzakian, S., T. Couderc, Y. Barbier, G. Attai, I. Pelletier, and F. Colbere-Garapin. 1992. Persistent poliovirus infection: establishment and maintenance involve distinct mechanisms. Virology. 186:398-408.
7. Brahic, M., W.G. Stroop, and J.R. Baringer. 1981. Theiler's virus persists in glial cells during demyelinating disease. Cell. 26:123-128.
8. Carp, R.I. 1981. Persistent infection of human lymphoid cells with poliovirus and development of temperature-sensitive mutants. Intervirology. 15:49-56.
9. Colbere-Garapin, F., C. Christodoulou, R. Crainic, and I. Pelletier. 1989. Persistent poliovirus infection of human neuroblastoma cells. Proc. Natl. Acad. Sci. USA. 86:7590-7594.
10. de la Torre, J.C., M. Davila, F. Sobrino, J. Ortin, and E. Domingo. 1985. Establishment of cell lines persistently infected with foot-and-mouth disease virus. Virology. 145:24-35.
11. Sharief, M.K., R. Hentges, and M. Ciardi. 1991. Intrathecal immune response in patients with the post-polio syndrome. N. Engl. J. Med. 325:749-755.
12. Kandolf, R., A. Canu, and P.H. Hofschneider. 1985. Coxsackic B3 virus can replicate in cultured human foetal heart cells and is inhibited by interferon. J. Mol. Cell Cardiol. 17:167-181.
13. Matteucci, D., M. Paglianti, A.M. Giangregorio, M.R. Capobianchi, F. Dianzani, and M. Bendinelli. 1985. Group B Coxsackieviruses readily establish persistent infections in human lymphoid cell lines. J. Virol. 56:651-654.
14. Cao, Y., and D.P. Schnurr. 1988. Persistent infection of YAC-1 cells by Coxsackievirus B3. J. Gen. Virol. 69:59-65.
15. Wessely, R., A. Henke, R. Zell, R. Kandolf, and K.U. Knowlton. 1998. Low level expression of a mutant Coxsackieviral cDNA induces a myocytopathic effect in culture: an approach to the study of enteroviral persistence in cardiac myocytes. Circulation. 98:450-457.
16. Lee, K.J., R.S. Ross, H.A. Rockman, A.N. Harris, T.X. O'Brien, M. Van Bilsen, H.E. Shubeita, R. Kandolf, G. Brem, and J. Price. 1992. Myosin light chain-2 luciferase transgenic mice reveal distinct regulatory programs for cardiac and skeletal muscle-specific expression of a single contractile protein gene. J. Biol. Chem. 267:15875-15885.
17. Gomez, A.M., H.H. Valdivia, H. Cheng, M.R. Lederer, L.F. Santana, M.B. Cannell, S.A. McCune, R.A. Altschuld, and W.J. Lederer. 1997. Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science. 276:800-806.
18. Kandolf, R., and P.H. Hofschneider. 1985. Molecular cloning of the genome of a cardiotropic Coxsackie B3 virus: full-length reverse-transcribed recombinant cDNA generates infectious virus in mammalian cells. Proc. Natl. Acad. Sci. USA. 82:4818-4822.
19. Klump, W.M., I. Bergmann, B.C. Muller, D. Ameis, and R. Kandolf. 1990. Complete nucleotide sequence of infectious Coxsackievirus B3 cDNA: two initial 5′ uridine residues are regained during plus-strand RNA synthesis. J. Virol. 64:1573-1583.
20. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
21. Hunter, J.J., N. Tanaka, H.A. Rockman, J. Ross, Jr., and K.R. Chien. 1995. Ventricular expression of a MLC-2v Ras fusion gene induces cardiac hypertrophy and selective diastolic dysfunction in transgenic mice. J. Biol. Chem. 270:23173-23178.
22. Hohenadl, C., K. Klingel, J. Mertsching, P.H. Hofschneider, and R. Kandolf. 1991. Strand-specific detection of enteroviral RNA in myocardial tissue by in situ hybridization. Mol. Cell Probes. 5:11-20.
23. Tanaka, N., N. Dalton, L. Mao, H.A. Rockman, K.R. Gottshall, J. Hunter, K.R. Chien, and J. Ross, Jr. 1996. Transthoracic echocardiography in models of cardiac disease in the mouse. Circulation. 94:1109-1117.
24. Santana, L.F., E.G. Kranias, and W.J. Lederer. 1997. Calcium sparks and excitation-contraction coupling in phospholamban-deficient mouse ventricular myocytes. J. Physiol. 503:21-29.
25. + channels: slip-mode conductance. Science. 279:1027-1033.
26. Hogan, B., F. Constantini, and E. Lacy. 1986. Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
27. Kandolf, R., D. Ameis, P. Kirschner, A. Canu, and P.H. Hofschneider. 1987. In situ detection of enteroviral genomes in myocardial cells by nucleic acid hybridization: an approach to the diagnosis of viral heart disease. Proc. Natl. Acad. Sci. USA. 84:6272-6276.
28. Chien, K.R., K.U. Knowlton, H. Zhu, and S. Chien. 1991. Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. FASEB (Fed. Am. Soc. Exp. Biol.) J. 5:3037-3046.
29. Chien, K.R., H. Zhu, K.U. Knowlton, W. Miller-Hance, M. van-Bilsen, T.X. O'Brien, and S.M. Evans. 1993. Transcriptional regulation during cardiac growth and development. Annu. Rev. Phvsiol. 55:77-95.
30. Parker, T.G., and M.D. Schneider. 1991. Growth factors, proto-oncogenes, and plasticity of the cardiac phenotype. Annu. Rev. Physiol. 53:179-200.
31. Schwarz, E.M., C. Badorff, T.S. Hiura, R. Wessely, A. Badorff, I.M. Verma, and K.U. Knowlton. 1998. NF-kappa B-mediated inhibition of apoptosis is required for encephalomyocarditis virus virulence: a mechanism of resistance in p50 knockout mice. J. Virol. 72:5654-5660.
32. 2+ sparks and local control theories for cardiac excitation-contraction coupling. Circ. Res. 78: 166-171.
33. Tazelaar, H.D., and M.E. Billingham. 1986. Leukocyte infiltrates in idiopathic dilated cardiomyopathy: a source of confusion with active myocarditis. Am. J. Surg. Pathol. 10:405-412.
34. O'Brien, T.X., K.J. Lee, and K.R. Chien. 1993. Positional specification of ventricular myosin light chain 2 expression in the primitive murine heart tube. Proc. Natl. Acad. Sci. USA. 90:5157-5161.
35. Geisterfer-Lowrance, A.A., M. Christe, D.A. Conner, J.S. Ingwall, F.J. Schoen, C.E. Seidman, and J.G. Seidman. 1996. A mouse model of familial hypertrophic cardiomyopathy. Science. 272:731-734.
36. Gottshall, K.R., J.J. Hunter, N. Tanaka, N. Dalton, K.D. Becker, J. Ross, Jr., and K.R. Chien. 1997. Ras-dependent pathways induce obstructive hypertrophy in echo-selected transgenic mice. Proc. Natl. Acad. Sci. USA. 94: 4710-4715.
37. Arber, S., J.J. Hunter, J. Ross, Jr., M. Hongo, G. Sansig, J. Borg, J.C. Perriard, K.R. Chien, and P. Caroni. 1997. MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell. 88:393-403.
38. Chisari, F.V., K. Klopchin, T. Moriyama, C. Pasquinelli, H.A. Dunsford, S. Sell, C.A. Pinkert, R.L. Brinster, and R.D. Palmiter. 1989. Molecular pathogenesis of hepatocellular carcinoma in hepatitis B virus transgenic mice. Cell. 59:1145-1156.
39. Kopp, J.B., M.E. Klotman, S.H. Adler, L.A. Bruggeman, P. Dickie, N.J. Marinos, M. Eckhaus, J.L. Bryant, A.L. Notkins, and P.E. Klotman. 1992. Progressive glomerulosclerosis and enhanced renal accumulation of basement membrane components in mice transgenic for human immunodeficiency virus type 1 genes. Proc. Natl. Acad. Sci. USA. 89:1577-1581.
40. Santoro, TJ., J.L. Bryant, J. Pellicoro, M.E. Klotman, J.B. Kopp, L.A. Bruggeman, R.R. Franks, A.L. Notkins, and P.E. Klotman. 1994. Growth failure and AIDS-like cachexia syndrome in HIV-1 transgenic mice. Virology. 201: 147-151.
41. Thomas, F.P., C. Chalk, R. Lalonde, Y. Robitaille, and P. Jolicoeur. 1994. Expression of human immunodeficiency virus type 1 in the nervous system of transgenic mice leads to neurological disease. J. Virol. 68:7099-7107.
42. Lamphear, B.J., R. Yan, F. Yang, D. Waters, H.D. Liebig, H. Klump, E. Kuechler, T. Skern, and R.E. Rhoads. 1993. Mapping the cleavage site in protein synthesis initiation factor eIF-4 gamma of the 2A proteases from human Coxsackievirus and rhinovirus. J. Biol. Chem. 268:19200-19203.
43. Lamphear, B.J., R. Kirchweger, T. Skern, and R.E. Rhoads. 1995. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem. 270:21975-21983.
44. Clark, M.E., P.M. Lieberman, A.J. Berk, and A. Dasgupta. 1993. Direct cleavage of human TATA-binding protein by poliovirus protease 3C in vivo and in vitro. Mol. Cell Biol. 13:1232-1237.
45. Yalamanchili, P., K. Harris, E. Wimmer, and A. Dasgupta. 1996. Inhibition of basal transcription by poliovirus: a virus-encoded protease (3Cpro) inhibits formation of TBP-TATA box complex in vitro. J. Virol. 70:2922-2929.
46. Sha, W.C., H.C. Liou, E.I. Tuomanen, and D. Baltimore. 1995. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell. 80:321-330.
47. Zhu, Z., W. Tang, A. Ray, Y. Wu, O. Einarsson, M.L. Landry, J. Gwaltney, Jr., and J.A. Elias. 1996. Rhinovirus stimulation of interleukin-6 in vivo and in vitro. Evidence for nuclear factor kappa B-dependent transcriptional activation. J. Clin. Invest. 97:421-430.
48. Yang, Y.L., L.F. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B.R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO (Eur. Mol. Biol. Organ.) J. 14:6095-6106.