Coxsackievirus B3 replication and pathogenesis

Future Microbiology

Volumn 10, Issue 4, 2015, Pages 629-652

  Garmaroudi, Farshid S ^a   Marchant, David ^b   Hendry, Reid ^b   Luo, Honglin ^a   Yang, Decheng ^a   Ye, Xin ^a   Shi, Junyan ^a   McManus, Bruce M ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c Prevention of Organ Failure Centre of Excellence   (Canada)

Author keywords

autophagy; coxsackievirus B3; matrix metalloproteinases; miRNA; signal transduction networks; systems virology; viral myocarditis

Indexed keywords

MATRIX METALLOPROTEINASE; MICRORNA; PHOSPHOTRANSFERASE;

CELL DEATH; COXSACKIE VIRUS; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; DISEASE PREDISPOSITION; EVOLUTION; HOST CELL; HUMAN; IMMUNE RESPONSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TROPISM; VIRUS REPLICATION; ENTEROVIRUS B; HOST PATHOGEN INTERACTION; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

COXSACKIEVIRUS; RNA VIRUSES;

ENTEROVIRUS B, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; VIRULENCE; VIRUS REPLICATION;

EID: 84927752669     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.15.5     Document Type: Review

References (259)

1. Martino TA, Liu P, Sole MJ. Viral infection and the pathogenesis of dilated cardiomyopathy. Circ. Res. 74(2), 182-188 (1994).
2. Ehrenfeld E, Domingo E, Roos RP. The Picornaviruses. ASM Press, Washington, DC, USA (2010).
3. Olsen EGJ. What is myocarditis Heart Vessels 1, 1-3 (1985).
4. Dalldorf G, Sickles GM. An unidentified, filtrable agent isolated from the feces of children with paralysis. Science 108(2794), 61-62 (1948).
5. Melnick JL, Shaw EW, Curnen EC. A virus isolated from patients diagnosed as non-paralytic poliomyelitis or aseptic meningitis. Proc. Soc. Exp. Biol. Med. 71(3), 344-349 (1949).
6. Melnick JL. Portraits of viruses: the picornaviruses. Intervirology 20(2-3), 61-100 (1983).
7. Chow L, Gauntt C, McManus B. Differential effects of myocarditic variants of Coxsackievirus B3 in inbred mice. A pathologic characterization of heart tissue damage. Lab. Invest. 64(1), 55-64 (1991).
8. Van Regenmortel MH, Fauquet C, Bishop D et al. Virus Taxonomy. Classification and Nomenclature of Viruses. Seventh Report of the International Committee on Taxonomy of Viruses. Academic Press, UT, USA (2000).
9. Gauntt CJ, Paque RE, Trousdale MD et al. Temperature-sensitive mutant of coxsackievirus B3 establishes resistance in neonatal mice that protects them during adolescence against coxsackievirus B3-induced myocarditis. Infect. Immun. 39(2), 851-864 (1983).
10. Brown BA, Oberste MS, Alexander JP, Kennett ML, Pallansch MA. Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J. Virol. 73(12), 9969-9975 (1999).
11. Mcintyre CL, Knowles NJ, Simmonds P. Proposals for the classification of human rhinovirus species A, B and C into genotypically assigned types. J. Gen. Virol. 94(Pt 8), 1791-1806 (2013).
12. Evans AS, Kaslow RA. Viral Infections of Humans: Epidemiology and Control. Springer, NY, USA (1997).
13. Rueckert RR. Picornaviridae: the viruses and their replication. Fields Virol. 1, 609-654 (1996).
14. Huber SA, Gauntt CJ, Sakkinen P. Enteroviruses and myocarditis: viral pathogenesis through replication, cytokine induction, and immunopathogenicity. Adv. Virus Res. 51, 35-80 (1998).
15. Flanegan JB, Petterson RF, Ambros V, Hewlett NJ, Baltimore D. Covalent linkage of a protein to a defined nucleotide sequence at the 5'-terminus of virion and replicative intermediate RNAs of poliovirus. Proc. Natl Acad. Sci. USA 74(3), 961-965 (1977).
16. Selinka HC, Wolde A, Sauter M, Kandolf R, Klingel K. Virus-receptor interactions of coxsackie B viruses and their putative influence on cardiotropism. Med. Microbiol. Immunol. 193(2-3), 127-131 (2004).
17. Carson SD, Chapman NM, Hafenstein S, Tracy S. Variations of coxsackievirus B3 capsid primary structure, ligands, and stability are selected for in a coxsackievirus and adenovirus receptor-limited environment. J. Virol. 85(7), 3306-3314 (2011).
18. Zautner A, Körner U, Henke A, Badorff C, Schmidtke M. Heparan sulfates and coxsackievirus-Adenovirus receptor: each one mediates coxsackievirus B3 PD infection. J. Virol. 77(18), 10071-10077 (2003).
19. Badorff C, Lee GH, Lamphear BJ et al. Enteroviral protease 2A cleaves dystrophin. evidence of cytoskeletal disruption in an acquired cardiomyopathy. Nat. Med. 5(3), 320-326 (1999).
20. Ehrenfeld E. Poliovirus-induced inhibition of host-cell protein synthesis. Cell 28(3), 435-436 (1982).
21. Mcbride AE, Schlegel A, Kirkegaard K. Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells. Proc. Natl Acad. Sci. USA 93(6), 2296-2301 (1996).
22. Bedard KM, Semler BL. Regulation of picornavirus gene expression. Microbes Infect. 6(7), 702-713 (2004).
23. Coyne CB, Bergelson JM. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124(1), 119-131 (2006).
24. Shaw CA, Holland PC, Sinnreich M et al. Isoform-specific expression of the Coxsackie and adenovirus receptor (CAR) in neuromuscular junction and cardiac intercalated discs. BMC 5(1), 42 (2004).
25. Zimmermann A, Gerber H, Nussenzweig V, Isliker H. Decay-Accelerating factor in the cardiomyocytes of normal individuals and patients with myocardial infarction. Virchows Arch. A Pathol. Anat. Histopathol. 417(4), 299-304 (1990).
26. Cheung PK, Yuan J, Zhang HM et al. Specific interactions of mouse organ proteins with the 5'untranslated region of coxsackievirus B3. potential determinants of viral tissue tropism. J. Med. Virol. 77(3), 414-424 (2005).
27. Harvala H, Kalimo H, Bergelson J, Stanway G, Hyypia T. Tissue tropism of recombinant coxsackieviruses in an adult mouse model. J. Gen Virol. 86(Pt 7), 1897-1907 (2005).
28. Crowell RL, Landau BJ, Siak J. Picornavirus receptors in pathogenesis. In: Virus Receptors, Part 2. Lonberg-Holm K, Philipson L (Eds). Chapman & Hall, London, UK, 169-184 (1981).
29. Wimmer E, Peutherer JF. Cellular Receptors for Animal Viruses. Cold Spring Harbor Laboratory Press, NY, USA (1994).
30. Rieder E, Wimmer E. Cellular receptors of picornaviruses: an overview. In: Molecular Biology of Picornaviruses. Semler BL, Wimmer E (Eds). ASM Press, Washington, DC, USA, 61-70 (2002).
31. Wessely R, Klingel K, Knowlton KU, Kandolf R. Cardioselective infection with coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication. Circulation 103(5), 756-761 (2001).
32. Anderson DR, Wilson JE, Carthy CM, Yang D, Kandolf R, Mcmanus BM. Direct interactions of coxsackievirus B3 with immune cells in the splenic compartment of mice susceptible or resistant to myocarditis. J. Virol. 70(7), 4632-4645 (1996).
33. Mena I, Fischer C, Gebhard JR, Perry CM, Harkins S, Whitton JL. Coxsackievirus infection of the pancreas: evaluation of receptor expression, pathogenesis, and immunopathology. Virology 271(2), 276-288 (2000).
34. Mena I, Perry CM, Harkins S, Rodriguez F, Gebhard J, Whitton JL. The role of B lymphocytes in coxsackievirus B3 infection. Am. J. Pathol. 155(4), 1205-1215 (1999).
35. Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat. Rev. Immunol. 8(9), 737-744 (2008).
36. Thom T, Haase N, Rosamond W et al. Heart disease and stroke statistics-2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 113(6), e85-e151 (2006).
37. Gauntt C, Huber S. Coxsackievirus experimental heart diseases. Front. Biosci. 8, e23-e35 (2003).
38. Lyden D, Olszewski J, Huber S. Variation in susceptibility of Balb/c mice to coxsackievirus group B type 3-induced myocarditis with age. Cell Immunol. 105(2), 332-339 (1987).
39. Klein SL. The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24(6), 627-638 (2000).
40. Ptak C, Petronis A. Epigenetics and complex disease: from etiology to new therapeutics. Ann. Rev. Pharmacol. Toxicol. 48, 257-276 (2008).
41. Mendelsohn ME, Karas RH. The protective effects of estrogen on the cardiovascular system. N. Engl. J. Med. 340(23), 1801-1811 (1999).
42. Rossouw JE, Anderson GL, Prentice RL et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women. principal results from the Women's Health Initiative randomized controlled trial. JAMA 288(3), 321-333 (2002).
43. Fairweather D, Frisancho-Kiss S, Yusung SA et al. Interferon-gamma protects against chronic viral myocarditis by reducing mast cell degranulation, fibrosis, and the profibrotic cytokines transforming growth factor-beta 1, interleukin-1 beta, and interleukin-4 in the heart. Am. J. Pathol. 165(6), 1883-1894 (2004).
44. Frisancho-Kiss S, Nyland JF, Davis SE et al. Sex differences in coxsackievirus B3-induced myocarditis. IL-12Rbeta1 signaling and IFN-gamma increase inflammation in males independent from STAT4. Brain Res. 1126(1), 139-147 (2006).
45. Bouman A, Heineman MJ, Faas MM. Sex hormones and the immune response in humans. Hum. Reprod. Update 11(4), 411-423 (2005).
46. Leslie KO, Schwarz J, Simpson K, Huber SA. Progressive interstitial collagen deposition in Coxsackievirus B3-induced murine myocarditis. Am. J. Pathol. 136(3), 683-693 (1990).
47. Mcmanus BM, Chow LH, Wilson JE et al. Direct myocardial injury by enterovirus. a central role in the evolution of murine myocarditis. Clin. Immunol. Immunopathol. 68(2), 159-169 (1993).
48. Narula J, Haider N, Virmani R et al. Apoptosis in myocytes in end-stage heart failure. N. Engl. J. Med. 335(16), 1182-1189 (1996).
49. Xiang W, Cuconati A, Hope D, Kirkegaard K, Wimmer E. Complete protein linkage map of poliovirus P3 proteins: interaction of polymerase 3Dpol with VPg and with genetic variants of 3AB. J. Virol. 72(8), 6732-6741 (1998).
50. Andino R, Rieckhof GE, Baltimore D. A functional ribonucleoprotein complex forms around the 5? end of poliovirus RNA. Cell 63(2), 369-380 (1990).
51. Zell R, Sidigi K, Bucci E, Stelzner A, Görlach M. Determinants of the recognition of enteroviral cloverleaf RNA by coxsackievirus B3 proteinase 3C. RNA 8(02), 188-201 (2002).
52. Hunziker IP, Cornell CT, Whitton JL. Deletions within the 5? UTR of coxsackievirus B3: consequences for virus translation and replication. Virology 360(1), 120-128 (2007).
53. Pilipenko EV, Maslova SV, Sinyakov AN, Agol VI. Towards identification of cis-Acting elements involved in the replication of enterovirus and rhinovirus RNAs: a proposal for the existence of tRNA-like terminal structures. Nucleic Acids Res. 20(7), 1739-1745 (1992).
54. Melchers W, Hoenderop J, Slot HB et al. Kissing of the two predominant hairpin loops in the coxsackie B virus 3'untranslated region is the essential structural feature of the origin of replication required for negative-strand RNA synthesis. J. Virol. 71(1), 686-696 (1997).
55. Pilipenko E, Poperechny K, Maslova S, Melchers W, Slot H, Agol V. Cis-element, oriR, involved in the initiation of (-) strand poliovirus RNA: a quasi-globular multidomain RNA structure maintained by tertiary ('kissing') interactions. EMBO J. 15(19), 5428 (1996).
56. Todd S, Towner JS, Brown DM, Semler BL. Replication-competent picornaviruses with complete genomic RNA 3'noncoding region deletions. J. Virol. 71(11), 8868-8874 (1997).
57. Harris KS, Hellen CUT, Wimmer E. Proteolytic processing in the replication of picornaviruses. Semin. Virol. 1, 323-333 (1990).
58. Hellen CU, Facke M, Krausslich HG, Lee CK, Wimmer E. Characterization of poliovirus 2A proteinase by mutational analysis: residues required for autocatalytic activity are essential for induction of cleavage of eukaryotic initiation factor 4F polypeptide p220. J. Virol. 65(8), 4226 (1991).
59. Bazan JF, Fletterick RJ. Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: structural and functional implications. Proc. Natl Acad. Sci. USA 85(21), 7872 (1988).
60. Gorbalenya AE, Donchenko AP, Blinov VM, Koonin EV. Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases: a distinct protein superfamily with a common structural fold. FEBS Lett. 243(2), 103-114 (1989).
61. Etchison D, Milburn SC, Edery I, Sonenberg N, Hershey JW. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J. Biol. Chem. 257(24), 14806 (1982).
62. Gingras A-C, Raught B, Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Ann. Rev. Biochem. 68(1), 913-963 (1999).
63. Kahvejian A, Svitkin YV, Sukarieh R, M'boutchou M-N, Sonenberg N. Mammalian poly (A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev. 19(1), 104-113 (2005).
64. Jang SK, Wimmer E. Cap-independent translation of encephalomyocarditis virus RNA: structural elements of the internal ribosomal entry site and involvement of a cellular 57-kD RNA-binding protein. Genes Dev. 4(9), 1560 (1990).
65. Pestova TV, Shatsky IN, Hellen C. Functional dissection of eukaryotic initiation factor 4F: the 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes. Mol. Cell. Biol. 16(12), 6870-6878 (1996).
66. Kerekatte V, Keiper BD, Badorff C, Cai A, Knowlton KU, Rhoads RE. Cleavage of poly (A)-binding protein by coxsackievirus 2A protease in vitro and in vivo : another mechanism for host protein synthesis shutoff? J. Virol. 73(1), 709-717 (1999).
67. Ehrenfeld E. Picornavirus Inhibition of Host Cell Protein Synthesis. Plenum Press, NY, USA (1984).
68. Lim B-K, Peter AK, Xiong D et al. Inhibition of Coxsackievirus-Associated dystrophin cleavage prevents cardiomyopathy. J. Clin. Invest. 123(123 (12)), 5146-5151 (2013).
69. Carthy CM, Yanagawa B, Luo H et al. Bcl-2 and Bcl-xL overexpression inhibits cytochrome c release, activation of multiple caspases, and virus release following coxsackievirus B3 infection. Virology 313(1), 147-157 (2003).
70. Carthy CM, Granville DJ, Watson KA et al. Caspase activation and specific cleavage of substrates after coxsackievirus B3-induced cytopathic effect in HeLa cells. J. Virol. 72(9), 7669-7675 (1998).
71. Agol VI. Cytopathic effects: virus-modulated manifestations of innate immunity Trends Microbiol. 20(12), 570-576 (2012).
72. Mikitas OV, Ivin YY, Golyshev SA et al. Suppression of injuries caused by a lytic RNA virus (mengovirus) and their uncoupling from viral reproduction by mutual cell/virus disarmament. J. Virol. 86(10), 5574-5583 (2012).
73. Fuse K, Chan G, Liu Y et al. Myeloid differentiation factor-88 plays a crucial role in the pathogenesis of coxsackievirus B3-induced myocarditis and influences type I interferon production. Circulation 112(15), 2276-2285 (2005).
74. Fairweather D, Yusung S, Frisancho S et al. IL-12 receptor ?1 and Toll-like receptor 4 increase IL-1?-And IL-18-Associated myocarditis and coxsackievirus replication. J. Immunol. 170(9), 4731-4737 (2003).
75. Kato H, Takeuchi O, Sato S et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441(7089), 101-105 (2006).
76. Kawai T, Akira S. Antiviral signaling through pattern recognition receptors. J. Biochem. 141(2), 137-145 (2007).
77. Fairweather D, Rose NR. Inflammatory heart disease: a role for cytokines. Lupus 14(9), 646-651 (2005).
78. Lane JR, Neumann DA, Lafond-Walker A, Herskowitz A, Rose NR. Interleukin 1 or tumor necrosis factor can promote Coxsackie B3-induced myocarditis in resistant B10.A mice. J. Exp. Med. 175(4), 1123-1129 (1992).
79. Lundgren M, Darnerud PO, Blomberg J, Friman G, Ilback NG. Sequential changes in serum cytokines reflect viral RNA kinetics in target organs of a coxsackievirus B infection in mice. J. Clin. Immunol. 29(5), 611-619 (2009).
80. Henke A, Mohr C, Sprenger H et al. Coxsackievirus B3-induced production of tumor necrosis factor-Alpha, IL-1 beta, and IL-6 in human monocytes. J. Immunol. 148(7), 2270-2277 (1992).
81. Althof N, Harkins S, Kemball CC, Flynn CT, Alirezaei M, Whitton JL. In vivo ablation of type I interferon receptor from cardiomyocytes delays coxsackieviral clearance and accelerates myocardial disease. J. Virol. 88(9), 5087-5099 (2014).
82. Klingel K, Kandolf R. The role of enterovirus replication in the development of acute and chronic heart muscle disease in different immunocompetent mouse strains. Scand. J. Infect. Dis. 88(Suppl.), 79-85 (1993).
83. Cohen P, Tcherpakov M. Will the ubiquitin system furnish as many drug targets as protein kinases Cell 143(5), 686-693 (2010).
84. Ribet D, Cossart P. Pathogen-mediated posttranslational modifications: a re-emerging field. Cell 143(5), 694-702 (2010).
85. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 298(5600), 1912-1934 (2002).
86. Papin JA, Hunter T, Palsson BO, Subramaniam S. Reconstruction of cellular signalling networks and analysis of their properties. Nat. Rev. Mol. Cell. Biol. 6(2), 99-111 (2005).
87. Dhanasekaran N, Premkumar Reddy E. Signaling by dual specificity kinases. Oncogene 17(11 Reviews), 1447-1455 (1998).
88. Huber M, Selinka HC, Kandolf R. Tyrosine phosphorylation events during coxsackievirus B3 replication. J. Virol. 71(1), 595-600 (1997).
89. Warny M, Keates AC, Keates S et al. p38 MAP kinase activation by Clostridium difficile toxin A mediates monocyte necrosis, IL-8 production, and enteritis. J. Clin. Invest. 105(8), 1147-1156 (2000).
90. Frame S, Cohen P, Biondi RM. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Molecular Cell 7(6), 1321-1327 (2001).
91. Cole A, Frame S, Cohen P. Further evidence that the tyrosine phosphorylation of glycogen synthase kinase-3 (GSK3) in mammalian cells is an autophosphorylation event. Biochem. J. 377(Pt 1), 249-255 (2004).
92. Sugden PH, Fuller SJ, Weiss SC, Clerk A. Glycogen synthase kinase 3 (GSK3) in the heart: a point of integration in hypertrophic signalling and a therapeutic target? A critical analysis. Br. J. Pharmacol. 153(Suppl. 1), S137-S153 (2008).
93. Thornton TM, Pedraza-Alva G, Deng B et al. Phosphorylation by p38 MAPK as an alternative pathway for GSK3beta inactivation. Science (New York) 320(5876), 667-670 (2008).
94. Yuan J, Zhang J, Wong BW et al. Inhibition of glycogen synthase kinase 3beta suppresses coxsackievirus-induced cytopathic effect and apoptosis via stabilization of betacatenin. Cell Death Differ. 12(8), 1097-1106 (2005).
95. Cunningham KA, Chapman NM, Carson SD. Caspase-3 activation and ERK phosphorylation during CVB3 infection of cells: influence of the coxsackievirus and adenovirus receptor and engineered variants. Virus Res. 92(2), 179-186 (2003).
96. Mcmanus BM, Yanagawa B, Rezai N et al. Genetic determinants of coxsackievirus B3 pathogenesis. Ann. NY Acad. Sci. 975, 169-179 (2002).
97. Opavsky MA, Martino T, Rabinovitch M et al. Enhanced ERK-1/2 activation in mice susceptible to coxsackievirus-induced myocarditis. J. Clin. Invest. 109(12), 1561-1569 (2002).
98. Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature 410(6824), 37-40 (2001).
99. Reichenspurner H. Overview of tacrolimusbased immunosuppression after heart or lung transplantation. J. Heart Lung Transplant. 24(2), 119-130 (2005).
100. Luo H, Yanagawa B, Zhang J et al. Coxsackievirus B3 replication is reduced by inhibition of the extracellular signal-regulated kinase (ERK) signaling pathway. J. Virol. 76(7), 3365-3373 (2002).
101. Nishimoto S, Nishida E. MAPK signalling: ERK5 versus ERK1/2. EMBO Rep. 7(8), 782-786 (2006).
102. Zhou G, Bao ZQ, Dixon JE. Components of a new human protein kinase signal transduction pathway. J. Biol. Chem? 270(21), 12665-12669 (1995).
103. Kato Y, Kravchenko VV, Tapping RI, Han J, Ulevitch RJ, Lee JD. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16(23), 7054-7066 (1997).
104. Abe J, Kusuhara M, Ulevitch RJ, Berk BC, Lee JD. Big mitogen-Activated protein kinase 1 (BMK1) is a redox-sensitive kinase. J. Biol. Chem. 271(28), 16586-16590 (1996).
105. Luo H, Reidy MA. Activation of big mitogen-Activated protein kinase-1 regulates smooth muscle cell replication. Arterioscler. Thromb. Vasc. Biol. 22(3), 394-399 (2002).
106. Kamakura S, Moriguchi T, Nishida E. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J. Biol. Chem. 274(37), 26563-26571 (1999).
107. Jensen KJ, Garmaroudi FS, Zhang J et al. An ERK-p38 subnetwork coordinates host cell apoptosis and necrosis during coxsackievirus B3 infection. Cell Host Microbe 13(1), 67-76 (2013).
108. Mody N, Leitch J, Armstrong C, Dixon J, Cohen P. Effects of MAP kinase cascade inhibitors on the MKK5/ERK5 pathway. FEBS Lett. 502(1-2), 21-24 (2001).
109. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351(Pt 1), 95-105 (2000).
110. Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N. Engl J. Med. 355(3), 251-259 (2006).
111. Johnson GL, Lapadat R. Mitogen-Activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science (New York) 298(5600), 1911-1912 (2002).
112. Manning AM, Davis RJ. Targeting JNK for therapeutic benefit: from junk to gold Nat. Rev. Drug Discov. 2(7), 554-565 (2003).
113. Garmaroudi FS, Marchant D, Si X et al. Pairwise network mechanisms in the host signaling response to coxsackievirus B3 infection. Proc. Natl Acad. Sci. USA 107(39), 17053-17058 (2010).
114. Gupta S, Campbell D, Derijard B, Davis RJ. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267(5196), 389-393 (1995).
115. Raingeaud J, Gupta S, Rogers JS et al. Pro-inflammatory cytokines and environmental stress cause p38 mitogenactivated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270(13), 7420-7426 (1995).
116. Ouwens DM, De Ruiter ND, Van Der Zon GC et al. Growth factors can activate ATF2 via a two-step mechanism. phosphorylation of Thr71 through the Ras-MEK-ERK pathway and of Thr69 through RalGDS-Src-p38. EMBO J. 21(14), 3782-3793 (2002).
117. Gonzalez GA, Montminy MR. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59(4), 675-680 (1989).
118. Xing J, Ginty DD, Greenberg ME. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273(5277), 959-963 (1996).
119. Deak M, Clifton AD, Lucocq LM, Alessi DR. Mitogen-And stress-Activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 17(15), 4426-4441 (1998).
120. Ashwell JD. The many paths to p38 mitogen-Activated protein kinase activation in the immune system. Nat. Rev. Immunol. 6(7), 532-540 (2006).
121. Holloway G, Coulson BS. Rotavirus activates JNK and p38 signaling pathways in intestinal cells, leading to AP-1-driven transcriptional responses and enhanced virus replication. J. Virol. 80(21), 10624-10633 (2006).
122. Mizutani T, Fukushi S, Saijo M, Kurane I, Morikawa S. Phosphorylation of p38 MAPK and its downstream targets in SARS coronavirus-infected cells. Biochem. Biophys. Res. Commun. 319(4), 1228-1234 (2004).
123. Rahaus M, Desloges N, Wolff MH. Replication of varicella-zoster virus is influenced by the levels of JNK/SAPK and p38/MAPK activation. J. Gen. Virol. 85(Pt 12), 3529-3540 (2004).
124. Si X, Luo H, Morgan A et al. Stress-Activated protein kinases are involved in coxsackievirus B3 viral progeny release. J. Virol. 79(22), 13875-13881 (2005).
125. Marchant D, Dou Y, Luo H et al. Bosentan enhances viral load via endothelin-1 receptor type-A-mediated p38 mitogen-Activated protein kinase activation while improving cardiac function during coxsackievirusinduced myocarditis. Circ. Res. 104(6), 813-821 (2009).
126. Ghosh S, Hayden MS. New regulators of NF-kappaB in inflammation. Nat. Rev. Immunol. 8(11), 837-848 (2008).
127. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell 132(3), 344-362 (2008).
128. Hayden MS, West AP, Ghosh S. SnapShot: NF-kappaB signaling pathways. Cell 127(6), 1286-1287 (2006).
129. Waelchli R, Bollbuck B, Bruns C et al. Design and preparation of 2-benzamido-pyrimidines as inhibitors of IKK. Bioorg. Med. Chem. Lett. 16(1), 108-112 (2006).
130. Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl.), S81-S96 (2002).
131. Chen ZJ, Parent L, Maniatis T. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity. Cell 84(6), 853-862 (1996).
132. Baeuerle PA. Pro-inflammatory signaling: last pieces in the NF-kappaB puzzle Curr. Biol. 8(1), R19-R22 (1998).
133. Baeuerle PA, Baltimore D. NF-kappa B: ten years after. Cell 87(1), 13-20 (1996).
134. Siebenlist U, Franzoso G, Brown K. Structure, regulation and function of NF-kappa B. Ann. Rev. Cell Biol. 10, 405-455 (1994).
135. Barnes PJ, Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 336(15), 1066-1071 (1997).
136. Didonato J, Mercurio F, Rosette C et al. Mapping of the inducible IkappaB phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol. 16(4), 1295-1304 (1996).
137. Didonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388(6642), 548-554 (1997).
138. Foo SY, Nolan GP. NF-kappaB to the rescue: RELs, apoptosis and cellular transformation. Trends Genet. 15(6), 229-235 (1999).
139. Ryan KM, Ernst MK, Rice NR, Vousden KH. Role of NF-kappaB in p53-mediated programmed cell death. Nature 404(6780), 892-897 (2000).
140. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nature Immunol. 3(3), 221-227 (2002).
141. Esfandiarei M, Boroomand S, Suarez A, Si X, Rahmani M, Mcmanus B. Coxsackievirus B3 activates nuclear factor kappa B transcription factor via a phosphatidylinositol-3 kinase/protein kinase B-dependent pathway to improve host cell viability. Cell. Microbiol. 9(10), 2358-2371 (2007).
142. Esfandiarei M, Luo H, Yanagawa B et al. Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J. Virol. 78(8), 4289-4298 (2004).
143. Esfandiarei M, Suarez A, Amaral A et al. Novel role for integrin-linked kinase in modulation of coxsackievirus B3 replication and virus-induced cardiomyocyte injury. Circulation Res. 99(4), 354-361 (2006).
144. Wong J, Zhang J, Gao G et al. Liposomemediated transient transfection reduces cholesterol-dependent coxsackievirus infectivity. J. Virol. Methods 133(2), 211-218 (2006).
145. Nowak M, May RM. Virus Dynamics: Mathematical Principles of Immunology and Virology. Oxford University Press, Oxford, UK (2000).
146. Perelson AS. Modelling viral and immune system dynamics. Nat. Rev. Immunol. 2(1), 28-36 (2002).
147. Neumann AU, Lam NP, Dahari H et al. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-? therapy. Science 282(5386), 103-107 (1998).
148. Lifson JD, Rossio JL, Piatak M et al. Role of CD8+ lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J. Virol. 75(21), 10187-10199 (2001).
149. Rouzine IM, Rodrigo A, Coffin J. Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol. Mol. Biol. Rev. 65(1), 151-185 (2001).
150. Weinberger LS, Burnett JC, Toettcher JE, Arkin AP, Schaffer DV. Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell 122(2), 169-182 (2005).
151. Tam PE. Coxsackievirus myocarditis: interplay between virus and host in the pathogenesis of heart disease. Viral Immunol. 19(2), 133-146 (2006).
152. Odum EP, . Fundamentals of Ecology. W.B. Saunders, PA, USA (1971).
153. Aderem A. Systems biology: its practice and challenges. Cell 121(4), 511-513 (2005).
154. Weinberger LS, Dar RD, Simpson ML. Transient-mediated fate determination in a transcriptional circuit of HIV. Nat. Genet. 40(4), 466-470 (2008).
155. Kitano H. Systems biology: a brief overview. Science 295(5560), 1662-1664 (2002).
156. Kitano H. Biological robustness. Nat. Rev. Genet. 5(11), 826-837 (2004).
157. Kawai C. From myocarditis to cardiomyopathy: mechanisms of inflammation and cell death: learning from the past for the future. Circulation 99(8), 1091-1100 (1999).
158. Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Ann. Rev. Physiol. 60, 619-642 (1998).
159. Degterev A, Huang Z, Boyce M et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1(2), 112-119 (2005).
160. Jacobson MD, Weil M, Raff MC. Programmed cell death in animal development. Cell 88(3), 347-354 (1997).
161. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science (New York) 267(5203), 1456-1462 (1995).
162. Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol. Cell 9(3), 459-470 (2002).
163. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol. 5(11), 897-907 (2004).
164. Thornberry NA, Bull HG, Calaycay JR et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356(6372), 768-774 (1992).
165. Martinon F, Tschopp J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117(5), 561-574 (2004).
166. Pasinelli P, Houseweart MK, Brown RH Jr., Cleveland DW. Caspase-1 and-3 are sequentially activated in motor neuron death in Cu, Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 97(25), 13901-13906 (2000).
167. Peter ME, Krammer PH. The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ. 10(1), 26-35 (2003).
168. Galluzzi L, Kroemer G. Necroptosis: a specialized pathway of programmed necrosis. Cell 135(7), 1161-1163 (2008).
169. Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N. Engl. J. Med. 368(7), 651-662 (2013).
170. Massey AC, Zhang C, Cuervo AM. Chaperone-mediated autophagy in aging and disease. Curr. Top. Dev. Biol. 73, 205-235 (2006).
171. Mijaljica D, Prescott M, Devenish RJ. Microautophagy in mammalian cells: revisting a 40-year-old conundrum. Autophagy 7(7), 673-682 (2011).
172. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 290(5497), 1717-1721 (2000).
173. Orvedahl A, Alexander D, Talloczy Z et al. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1(1), 23-35 (2007).
174. Orvedahl A, Macpherson S, Sumpter R Jr., Talloczy Z, Zou Z, Levine B. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7(2), 115-127 (2010).
175. Shi J, Luo H. Interplay between the cellular autophagy machinery and positive-stranded RNA viruses. Acta Biochim. Biophys. Sin. (Shanghai) 44(5), 375-384 (2012).
176. Alirezaei M, Flynn CT, Wood MR, Whitton JL. Pancreatic acinar cell-specific autophagy disruption reduces coxsackievirus replication and pathogenesis in vivo. Cell Host Microbe 11(3), 298-305 (2012).
177. Kemball CC, Alirezaei M, Flynn CT et al. Coxsackievirus infection induces autophagylike vesicles and megaphagosomes in pancreatic acinar cells in vivo. J. Virol. 84(23), 12110-12124 (2010).
178. Tabor-Godwin JM, Tsueng G, Sayen MR, Gottlieb RA, Feuer R. The role of autophagy during coxsackievirus infection of neural progenitor and stem cells. Autophagy 8(6), 938-953 (2012).
179. Wong J, Zhang J, Si X et al. Autophagosome supports coxsackievirus B3 replication in host cells. J. Virol. 82(18), 9143-9153 (2008).
180. Salonen A, Ahola T, Kaariainen L. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285, 139-173 (2005).
181. Jackson WT, Giddings TH Jr., Taylor MP et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3(5), e156 (2005).
182. Suhy DA, Giddings TH Jr., Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J. Virol. 74(19), 8953-8965 (2000).
183. Kirkegaard K, Taylor MP, Jackson WT. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat. Rev. Microbiol. 2(4), 301-314 (2004).
184. Robinson SM, Tsueng G, Sin J et al. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLoS Pathog. 10(4), e1004045 (2014).
185. Fujita N, Yoshimori T. Ubiquitinationmediated autophagy against invading bacteria. Curr. Opin. Cell. Biol. 23(4), 492-497 (2011).
186. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 7(3), 279-296 (2011).
187. Komatsu M, Ichimura Y. Selective autophagy regulates various cellular functions. Genes Cells 15(9), 923-933 (2010).
188. Gao G, Zhang J, Si X et al. Proteasome inhibition attenuates coxsackievirus-induced myocardial damage in mice. American Journal of Physiology. Heart Circ. Physiol. 295(1), H401-H408 (2008).
189. Luo H, Wong J, Wong B. Protein degradation systems in viral myocarditis leading to dilated cardiomyopathy. Cardiovasc. Res. 85(2), 347-356 (2010).
190. Si X, Gao G, Wong J, Wang Y, Zhang J, Luo H. Ubiquitination is required for effective replication of coxsackievirus B3. PLoS ONE 3(7), e2585 (2008).
191. Ichimura Y, Komatsu M. Selective degradation of p62 by autophagy. Semin. Immunopathol. 32(4), 431-436 (2010).
192. Shi J, Fung G, Piesik P, Zhang J, Luo H. Dominant-negative function of the C-terminal fragments of NBR1 and SQSTM1 generated during enteroviral infection. Cell Death Differ.21, 1432-1441 (2014).
193. Shi J, Wong J, Piesik P et al. Cleavage of sequestosome 1/p62 by an enteroviral protease results in disrupted selective autophagy and impaired NFKB signaling. Autophagy 9(10), 1591-1603 (2013).
194. Mcquibban GA, Gong J-H, Tam EM, Mcculloch CA, Clark-Lewis I, Overall CM. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289(5482), 1202-1206 (2000).
195. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111(5), 635-646 (2002).
196. Mcquibban GA, Gong JH, Wong JP, Wallace JL, Clark-Lewis I, Overall CM. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 100(4), 1160-1167 (2002).
197. Dean RA, Cox JH, Bellac CL, Doucet A, Starr AE, Overall CM. Macrophage-specific metalloelastase (MMP-12) truncates and inactivates ELR+ CXC chemokines and generates CCL2,-7,-8, and-13 antagonists: potential role of the macrophage in terminating polymorphonuclear leukocyte influx. Blood 112(8), 3455-3464 (2008).
198. Kandasamy AD, Chow AK, Ali MA, Schulz R. Matrix metalloproteinase-2 and myocardial oxidative stress injury: beyond the matrix. Cardiovasc. Res. 85(3), 413-423 (2010).
199. Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JR, Sawicki G, Schulz R. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 106(12), 1543-1549 (2002).
200. Marchant DJ, Bellac CL, Moraes TJ et al. A new transcriptional role for matrix metalloproteinase-12 in antiviral immunity. Nat. Med. 20(5), 493-502 (2014).
201. Zuo X, Pan W, Feng T, Shi X, Dai J. Matrix metalloproteinase 3 promotes cellular anti-dengue virus response via interaction with transcription factor NF?B in cell nucleus. PLoS ONE 9(1), e84748 (2014).
202. Cheung C, Luo H, Yanagawa B et al. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in coxsackievirus-induced myocarditis. Cardiovasc. Pathol. 15(2), 63-74 (2006).
203. Cheung CT, Deisher TA, Luo H et al. Neutralizing anti-4-1BBL treatment improves cardiac function in viral myocarditis. Lab. Invest. 87(7), 651-661 (2007).
204. Rutschow S, Leschka S, Westermann D et al. Left ventricular enlargement in coxsackievirus-B3 induced chronic myocarditis-ongoing inflammation and an imbalance of the matrix degrading system. Eur. J. Pharmacol. 630(1-3), 145-151 (2010).
205. Heymans S, Pauschinger M, De Palma A et al. Inhibition of urokinase-type plasminogen activator or matrix metalloproteinases prevents cardiac injury and dysfunction during viral myocarditis. Circulation 114(6), 565-573 (2006).
206. Cheung C, Marchant D, Walker EK et al. Ablation of matrix metalloproteinase-9 increases severity of viral myocarditis in mice. Circulation 117(12), 1574-1582 (2008).
207. Westermann D, Savvatis K, Lindner D et al. Reduced degradation of the chemokine MCP-3 by matrix metalloproteinase-2 exacerbates myocardial inflammation in experimental viral cardiomyopathy. Circulation 124(19), 2082-2093 (2011).
208. Nelissen I, Martens E, Van Den Steen PE, Proost P, Ronsse I, Opdenakker G. Gelatinase B/matrix metalloproteinase9 cleaves interferon and is a target for immunotherapy. Brain 126(6), 1371-1381 (2003).
209. Pauschinger M, Chandrasekharan K, Schultheiss HP. Myocardial remodeling in viral heart disease: possible interactions between inflammatory mediators and MMP-TIMP system. Heart Fail. Rev. 9(1), 21-31 (2004).
210. Crocker SJ, Frausto RF, Whitmire JK, Benning N, Milner R, Whitton JL. Amelioration of coxsackievirus B3-mediated myocarditis by inhibition of tissue inhibitors of matrix metalloproteinase-1. Am. J. Pathol. 171(6), 1762-1773 (2007).
211. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5), 843-854 (1993).
212. Cullen BR. Viruses and microRNAs. Nat. Genet. 38(Suppl.), S25-S30 (2006).
213. Pillai RS. MicroRNA function: multiple mechanisms for a tiny RNA? RNA 11(12), 1753-1761 (2005).
214. Vasudevan S. Posttranscriptional upregulation by microRNAs. Wiley Interdiscip. Rev. RNA 3(3), 311-330 (2012).
215. Cullen BR. Transcription and processing of human microRNA precursors. Molecular Cell 16(6), 861-865 (2004).
216. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11(9), 597-610 (2010).
217. Plaisance-Bonstaff K, Renne R. Viral miRNAs. Methods Mol. Biol. 721, 43-66 (2011).
218. Kim Do N, Lee SK. Biogenesis of Epstein-Barr virus microRNAs. Mol. Cell. Biochem. 365(1-2), 203-210 (2012).
219. Libri V, Miesen P, Van Rij RP, Buck AH. Regulation of microRNA biogenesis and turnover by animals and their viruses. Cell. Mol. Life Sci. (2013).
220. Thornburg NJ, Hayward SL, Crowe JE. Respiratory syncytial virus regulates human microRNAs by using mechanisms involving beta interferon and NF-kappa B. mBio 3(6), (2012).
221. Cameron JE, Yin QY, Fewell C et al. Epstein-Barr virus latent membrane protein induces cellular microRNA miR-146a, a modulator of lymphocyte signaling pathways. J. Virol. 82(4), 1946-1958 (2008).
222. Sun GH, Li HT, Wu XW et al. Interplay between HIV-1 infection and host microRNAs. Nucleic Acids Res. 40(5), 2181-2196 (2012).
223. Li Y, Chan EY, Li JN et al. MicroRNA expression and virulence in pandemic influenza virus-infected mice. J. Virol. 84(6), 3023-3032 (2010).
224. Braconi C, Valeri N, Gasparini P et al. Hepatitis C virus proteins modulate microRNA expression and chemosensitivity in malignant hepatocytes. Clin. Cancer Res. 16(3), 957-966 (2010).
225. Motsch N, Alles J, Imig J et al. MicroRNA profiling of Epstein-Barr virus-Associated NK/T-cell lymphomas by deep sequencing. PLoS ONE 7(8), (2012).
226. Kaczkowski B, Morevati M, Rossing M, Cilius F, Norrild B. A decade of global mRNA and miRNA profiling of HPVpositive cell lines and clinical specimens. Open Virol. J. 6, 216-231 (2012).
227. Stewart CR, Marsh GA, Jenkins KA et al. Promotion of Hendra virus replication by microRNA 146a. J. Virol. 87(7), 3782-3791 (2013).
228. Triboulet R, Mari B, Lin YL et al. Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315(5818), 1579-1582 (2007).
229. Yin Q, Mcbride J, Fewell C et al. MicroRNA-155 is an Epstein-Barr virusinduced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J. Virol. 82(11), 5295-5306 (2008).
230. Lecellier CH, Dunoyer P, Arar K et al. A cellular microRNA mediates antiviral defense in human cells. Science 308(5721), 557-560 (2005).
231. Otsuka M, Jing Q, Georgel P et al. Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 27(1), 123-134 (2007).
232. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309(5740), 1577-1581 (2005).
233. Linial ML. Foamy viruses are unconventional retroviruses. J. Virol. 73(3), 1747-1755 (1999).
234. Park NJ, Zhou H, Elashoff D et al. Salivary microRNA. discovery, characterization, and clinical utility for oral cancer detection. Clin. Cancer Res. 15(17), 5473-5477 (2009).
235. Sullivan CS, Grundhoff AT, Tevethia S, Pipas JM, Ganem D. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435(7042), 682-686 (2005).
236. Pfeffer S, Sewer A, Lagos-Quintana M et al. Identification of microRNAs of the herpesvirus family. Nat. Methods 2(4), 269-276 (2005).
237. Barth S, Pfuhl T, Mamiani A et al. Epstein-Barr virus-encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res. 36(2), 666-675 (2008).
238. Tang S, Bertke AS, Patel A, Wang K, Cohen JI, Krause PR. An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc. Natl Acad. Sci. USA 105(31), 10931-10936 (2008).
239. Tang S, Patel A, Krause PR. Novel lessabundant viral microRNAs encoded by herpes simplex virus 2 latency-Associated transcript and their roles in regulating ICP34.5 and ICP0 mRNAs. J. Virol. 83(3), 1433-1442 (2009).
240. Lo AK, To KF, Lo KW et al. Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc. Natl Acad. Sci. USA 104(41), 16164-16169 (2007).
241. Samols MA, Skalsky RL, Maldonado AM et al. Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog. 3(5), e65 (2007).
242. Ziegelbauer JM, Sullivan CS, Ganem D. Tandem array-based expression screens identify host mRNA targets of virus-encoded microRNAs. Nat. Genet. 41(1), 130-134 (2009).
243. Hansen A, Henderson S, Lagos D et al. KSHV-encoded miRNAs target MAF to induce endothelial cell reprogramming. Genes Dev. 24(2), 195-205 (2010).
244. Choy EY, Siu KL, Kok KH et al. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J. Exp. Med. 205(11), 2551-2560 (2008).
245. Xia T, O'Hara A, Araujo I et al. EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res. 68(5), 1436-1442 (2008).
246. Ho BC, Yu SL, Chen JJ et al. Enterovirusinduced miR-141 contributes to shutoff of host protein translation by targeting the translation initiation factor eIF4E. Cell Host Microbe 9(1), 58-69 (2011).
247. Corsten MF, Papageorgiou A, Verhesen W et al. MicroRNA profiling identifies microRNA-155 as an adverse mediator of cardiac injury and dysfunction during acute viral myocarditis. Circulation Res. 111(4), 415-425 (2012).
248. Hemida MG, Ye X, Zhang HM et al. MicroRNA-203 enhances coxsackievirus B3 replication through targeting zinc finger protein-148. Cell. Mol. Life Sci. 70(2), 277-291 (2013).
249. Ye X, Hemida MG, Qiu Y, Hanson PJ, Zhang HM, Yang D. MiR-126 promotes coxsackievirus replication by mediating cross-talk of ERK1/2 and Wnt/beta-catenin signal pathways. Cell. Mol. Life Sci. 70(23), 4631-4644 (2013).
250. Xu HF, Ding YJ, Shen YW et al. MicroRNA-represses Cx43 expression in viral myocarditis. Mol. Cell. Biochem. 362(1-2), 141-148 (2012).
251. Guerrier A, Fonlupt P, Morand I et al. Gap junctions and cell polarity. connexin32 and connexin43 expressed in polarized thyroid epithelial cells assemble into separate gap junctions, which are located in distinct regions of the lateral plasma membrane domain. J. Cell Sci. 108(Pt 7), 2609-2617 (1995).
252. He J, Yue Y, Dong C, Xiong S. MiR-21 confers resistance against CVB3-induced myocarditis by inhibiting PDCD4-mediated apoptosis. Clinical and investigative medicine. Clin. Invest. Med. 36(2), E103-E111 (2013).
253. Liu YL, Wu W, Xue Y et al. MicroRNA-21 and-146b are involved in the pathogenesis of murine viral myocarditis by regulating TH-17 differentiation. Arch. Virol.158(9), 1953-1963 (2013).
254. Ye X, Zhang HM, Qiu Y et al. Coxsackievirusinduced miR-21 disrupts cardiomyocyte interactions via the downregulation of intercalated disk components. PLoS Pathog. 10(4), e1004070 (2014).
255. Ikeda S, He A, Kong SW et al. MicroRNA-1 negatively regulates expression of the hypertrophy-Associated calmodulin and Mef2a genes. Mol. Cell. Biol. 29(8), 2193-2204 (2009).
256. Tong L, Lin L, Wu S et al. MiR-10a up-regulates coxsackievirus B3 biosynthesis by targeting the 3D-coding sequence. Nucleic Acids Res. 41(6), 3760-3771 (2013).
257. Wang L, Qin Y, Tong L et al. MiR-342-5p suppresses coxsackievirus B3 biosynthesis by targeting the 2C-coding region. Antiviral Res. 93(2), 270-279 (2012).
258. Ye X, Liu Z, Hemida MG, Yang D. Targeted delivery of mutant tolerant anticoxsackievirus artificial microRNAs using folate conjugated bacteriophage Phi29 pRNA. PLoS ONE 6(6), e21215 (2011).
259. Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol. 11(8), R90 (2010).