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References

  1. Badorff C, Berkely N, Mehrotra S, Talhouk JW, Rhoads RE, Knowlton KU. 2000. Enteroviral protease 2A directly cleaves dystrophin and is inhibited by a dystrophin-based substrate analogue. J. Biol. Chem. 275: 11191-11197.
    Pubmed CrossRef
  2. Chen TC, Weng KF, Chang SC, Lin JY, Huang PN, Shih SR. 2008. Development of antiviral agents for enteroviruses. J. Antimicrob. Chemother. 62: 1169-1173.
    Pubmed CrossRef
  3. Choi HG, Je IG, Kim GJ, Choi H, Kim SH, Kim JA, Lee KS. 2015. Anti-allergic inflammatory activities of compounds of amomi fructus. Nat. Prod. Commun. 10: 631-632.
    Pubmed
  4. Esfandiarei M, Luo H, Yanagawa B, Suarez A, Dabiri D, Zhang J, McManus BM. 2004. Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J. Virol. 78: 4289-4298.
    Pubmed PMC CrossRef
  5. Feldman AM, McNamara D. 2000. Myocarditis. N. Engl. J. Med. 343: 1388-1398.
    Pubmed CrossRef
  6. Herskowitz A, Beisel KW, Wolfgram LJ, Rose NR. 1985. Coxsackievirus B3 murine myocarditis: wide pathologic spectrum in genetically defined inbred strains. Hum. Pathol. 16: 671-673.
    CrossRef
  7. Kearney MT, Cotton JM, Richardson PJ, Shah AM. 2001. Viral myocarditis and dilated cardiomyopathy: mechanisms, manifestations, and management. Postgrad. Med. J. 77: 4-10.
    Pubmed PMC CrossRef
  8. Kim JM, Lim BK, Ho SH, Yun SH, Shin JO, Park EM, et al. 2006. TNFR-Fc fusion protein expressed by in vivo electroporation improves survival rates and myocardial injury in coxsackievirus induced murine myocarditis. Biochem. Biophys. Res. Commun. 344: 765-771.
    Pubmed CrossRef
  9. Knowlton KU, Badorff C. 1999. The immune system in viral myocarditis: maintaining the balance. Circ. Res. 85: 559-561.
    Pubmed CrossRef
  10. Knowlton KU, Jeon ES, Berkley N, Wessely R, Huber S. 1996. A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3. J. Virol. 70: 7811-7818.
    Pubmed PMC
  11. Kumar S, Pandey AK. 2013. Chemistry and biological activities of flavonoids: an overview. Scientific World Journal 2013: 162750.
    Pubmed PMC CrossRef
  12. Lim BK, Choe SC, Shin JO, Ho SH, Kim JM, Yu SS, et al. 2002. Local expression of interleukin-1 receptor antagonist by plasmid DNA improves mortality and decreases myocardial inflammation in experimental coxsackieviral myocarditis. Circulation 105: 1278-1281.
    Pubmed
  13. Lim BK, Choi JH, Nam JH, Gil CO, Shin JO, Yun SH, et al. 2006. Virus receptor trap neutralizes coxsackievirus in experimental murine viral myocarditis. Cardiovasc. Res. 71:517-526.
    Pubmed CrossRef
  14. Lim BK, Kim JH. 2014. ORI2 inhibits coxsackievirus replication and myocardial inflammation in experimental murine myocarditis. Biol. Pharm. Bull. 37: 1650-1654.
    Pubmed CrossRef
  15. Lim BK, Nam JH, Gil CO, Yun SH, Choi JH, Kim DK, Jeon ES. 2005. Coxsackievirus B3 replication is related to activation of the late extracellular signal-regulated kinase (ERK) signal. Virus Res. 113: 153-157.
    Pubmed CrossRef
  16. Lim BK, Xiong D, Dorner A, Youn TJ, Yung A, Liu TI, et al. 2008. Coxsackievirus and adenovirus receptor (CAR) mediates atrioventricular-node function and connexin 45 localization in the murine heart. J. Clin. Invest. 118: 2758-2770.
    Pubmed PMC CrossRef
  17. Lim BK, Yun SH, Gil CO, Ju ES, Choi JO, Kim DK, Jeon ES. 2012. Foreign gene transfer to cardiomyocyte using a replication-defective recombinant coxsackievirus B3 without cytotoxicity. Intervirology 55: 201-209.
    Pubmed CrossRef
  18. Lim BK, Yun SH, Ju ES, Gil CO, Kim DK, Jeon ES. 2012. Role of the myristoylation site in expressing exogenous functional proteins in coxsackieviral vector. Biosci. Biotechnol. Biochem. 76: 1173-1176.
    Pubmed CrossRef
  19. Liu P, Martino T, Opavsky MA, Penninger J. 1996. Viral myocarditis: balance between viral infection and immune response. Can. J. Cardiol. 12: 935-943.
    Pubmed
  20. Martino TA, Liu P, Sole MJ. 1994. Viral infection and the pathogenesis of dilated cardiomyopathy. Circ. Res. 74: 182188.
    CrossRef
  21. Schnitzler P, Neuner A, Nolkemper S, Zundel C, Nowack H, Sensch KH, Reichling J. 2010. Antiviral activity and mode of action of propolis extracts and selected compounds. Phytother. Res. 24 Suppl 1: S20-S28.
    Pubmed CrossRef
  22. Song JH, Kwon BE, Jang H, Kang H, Cho S, Park K, et al. 2015. Antiviral activity of chrysin derivatives against coxsackievirus B3 in vitro and in vivo. Biomol. Ther. (Seoul) 23: 465-470.
    Pubmed PMC CrossRef
  23. Sun F, Li Y, Jia T, Ling Y, Liang L, Liu G, et al. 2012. Differential expression of coxsackievirus and adenovirus receptor on alveolar epithelial cells between fetal and adult mice determines their different susceptibility to coxsackievirus B infection. Arch. Virol. 157: 1101-1111.
    Pubmed CrossRef
  24. Wang SM, Liu CC. 2014. Update of enterovirus 71 infection:epidemiology, pathogenesis and vaccine. Expert Rev. Anti Infect. Ther. 12: 447-456.
    Pubmed CrossRef
  25. Wong J, Zhang J, Yanagawa B, Luo Z, Yang X, Chang J, et al. 2012. Cleavage of serum response factor mediated by enteroviral protease 2A contributes to impaired cardiac function. Cell Res. 22: 360-371.
    Pubmed PMC CrossRef
  26. Woodruff JF. 1980. Viral myocarditis. A review. Am. J. Pathol. 101: 425-484.
    Pubmed PMC
  27. Xiong D, Lee GH, Badorff C, Dorner A, Lee S, Wolf P, Knowlton KU. 2002. Dystrophin deficiency markedly increases enterovirus-induced cardiomyopathy: a genetic predisposition to viral heart disease. Nat. Med. 8: 872-877.
    CrossRef
  28. Xiong D, Yajima T, Lim BK, Stenbit A, Dublin A, Dalton ND, et al. 2007. Inducible cardiac-restricted expression of enteroviral protease 2A is sufficient to induce dilated cardiomyopathy. Circulation 115: 94-102.
    Pubmed CrossRef
  29. Yu J, Sun L, Zhou L, Luo X, Guo J, Liu C, Cong P. 1997. [Chemical constituents of fructus Amomi]. Zhongguo Zhong Yao Za Zhi 22: 231-232, 255.
  30. Yun SH, Lee WG, Kim YC, Ju ES, Lim BK, Choi JO, et al. 2012. Antiviral activity of coxsackievirus B3 3C protease inhibitor in experimental murine myocarditis. J. Infect. Dis. 205: 491-497.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(11): 2012-2018

Published online November 28, 2016 https://doi.org/10.4014/jmb.1605.05056

Copyright © The Korean Society for Microbiology and Biotechnology.

Fructus Amomi Cardamomi Extract Inhibits Coxsackievirus-B3 Induced Myocarditis in a Murine Myocarditis Model

Yun-Gyeong Lee 1, Jung-Ho Park 3, Eun-Seok Jeon 4, Jin-Hee Kim 2 and Byung-Kwan Lim 1*

1Department of Biomedical Science, Jungwon University, Goesan 28024, Republic of Korea, 2College of Herbal Bio-Industry, Daegu Haany University, Gyeongsan 38610, Republic of Korea, 3Bio-Evaluation Center, Korea Research Institute of Bioscience and Biotechnology, Cheonju 28116, Republic of Korea, 4Cardiac and Vascular Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 06351, Republic of Korea

Received: May 18, 2016; Accepted: August 17, 2016

Abstract

Coxsackievirus B3 (CVB3) is the main cause of acute myocarditis and dilated cardiomyopathy. Plant extract is considered as useful materials to develop new antiviral drug. We select the candidate plant extract, which showed anti-inflammatory effect previously. We examined the antiviral effects by using a HeLa cell survival assay. Among these extracts, we chose the Amomi Cardamomi (Amomi) extract, which showed strong antiviral effect and preserved cell survival in CVB3 infection. We investigated the mechanisms underlying the ability of Amomi extract to inhibit CVB3 infection and replication. HeLa cells infected by CVB3 with or without Amomi extract. Erk and Akt activity, and its correlation with virus replication was observed. Live virus titer in cell supernatants and viral positive- and negative-strand RNA amplification were measured. Amomi extract significantly increased HeLa cell survival in different concentrations (100–10㎍/㎖). Production of the viral capsid protein VP1 (76%) and viral protease 2A–induced eIF4G1 cleavage (70%) were significantly decreased in Amomi extract (100㎍/㎖) treated cells. The levels of positive- (20%) and negative-strand (80%) RNA were dramatically decreased compared to control, as revealed by reverse transcription–PCR. In addition, Amomi extract improved mice survival (51% vs 26%) and dramatically reduced heart inflammation in CVB3-induced myocarditis mouse model. These results suggested that Amomi extract was significantly inhibited Enterovirus replication and myocarditis damage. Amomi may be develop therapeutic drug for Enterovirus.

Keywords: Coxsackievirus B3, Myocarditis, Plant extract, Antiviral effect, Enterovirus

References

  1. Badorff C, Berkely N, Mehrotra S, Talhouk JW, Rhoads RE, Knowlton KU. 2000. Enteroviral protease 2A directly cleaves dystrophin and is inhibited by a dystrophin-based substrate analogue. J. Biol. Chem. 275: 11191-11197.
    Pubmed CrossRef
  2. Chen TC, Weng KF, Chang SC, Lin JY, Huang PN, Shih SR. 2008. Development of antiviral agents for enteroviruses. J. Antimicrob. Chemother. 62: 1169-1173.
    Pubmed CrossRef
  3. Choi HG, Je IG, Kim GJ, Choi H, Kim SH, Kim JA, Lee KS. 2015. Anti-allergic inflammatory activities of compounds of amomi fructus. Nat. Prod. Commun. 10: 631-632.
    Pubmed
  4. Esfandiarei M, Luo H, Yanagawa B, Suarez A, Dabiri D, Zhang J, McManus BM. 2004. Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J. Virol. 78: 4289-4298.
    Pubmed KoreaMed CrossRef
  5. Feldman AM, McNamara D. 2000. Myocarditis. N. Engl. J. Med. 343: 1388-1398.
    Pubmed CrossRef
  6. Herskowitz A, Beisel KW, Wolfgram LJ, Rose NR. 1985. Coxsackievirus B3 murine myocarditis: wide pathologic spectrum in genetically defined inbred strains. Hum. Pathol. 16: 671-673.
    CrossRef
  7. Kearney MT, Cotton JM, Richardson PJ, Shah AM. 2001. Viral myocarditis and dilated cardiomyopathy: mechanisms, manifestations, and management. Postgrad. Med. J. 77: 4-10.
    Pubmed KoreaMed CrossRef
  8. Kim JM, Lim BK, Ho SH, Yun SH, Shin JO, Park EM, et al. 2006. TNFR-Fc fusion protein expressed by in vivo electroporation improves survival rates and myocardial injury in coxsackievirus induced murine myocarditis. Biochem. Biophys. Res. Commun. 344: 765-771.
    Pubmed CrossRef
  9. Knowlton KU, Badorff C. 1999. The immune system in viral myocarditis: maintaining the balance. Circ. Res. 85: 559-561.
    Pubmed CrossRef
  10. Knowlton KU, Jeon ES, Berkley N, Wessely R, Huber S. 1996. A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3. J. Virol. 70: 7811-7818.
    Pubmed KoreaMed
  11. Kumar S, Pandey AK. 2013. Chemistry and biological activities of flavonoids: an overview. Scientific World Journal 2013: 162750.
    Pubmed KoreaMed CrossRef
  12. Lim BK, Choe SC, Shin JO, Ho SH, Kim JM, Yu SS, et al. 2002. Local expression of interleukin-1 receptor antagonist by plasmid DNA improves mortality and decreases myocardial inflammation in experimental coxsackieviral myocarditis. Circulation 105: 1278-1281.
    Pubmed
  13. Lim BK, Choi JH, Nam JH, Gil CO, Shin JO, Yun SH, et al. 2006. Virus receptor trap neutralizes coxsackievirus in experimental murine viral myocarditis. Cardiovasc. Res. 71:517-526.
    Pubmed CrossRef
  14. Lim BK, Kim JH. 2014. ORI2 inhibits coxsackievirus replication and myocardial inflammation in experimental murine myocarditis. Biol. Pharm. Bull. 37: 1650-1654.
    Pubmed CrossRef
  15. Lim BK, Nam JH, Gil CO, Yun SH, Choi JH, Kim DK, Jeon ES. 2005. Coxsackievirus B3 replication is related to activation of the late extracellular signal-regulated kinase (ERK) signal. Virus Res. 113: 153-157.
    Pubmed CrossRef
  16. Lim BK, Xiong D, Dorner A, Youn TJ, Yung A, Liu TI, et al. 2008. Coxsackievirus and adenovirus receptor (CAR) mediates atrioventricular-node function and connexin 45 localization in the murine heart. J. Clin. Invest. 118: 2758-2770.
    Pubmed KoreaMed CrossRef
  17. Lim BK, Yun SH, Gil CO, Ju ES, Choi JO, Kim DK, Jeon ES. 2012. Foreign gene transfer to cardiomyocyte using a replication-defective recombinant coxsackievirus B3 without cytotoxicity. Intervirology 55: 201-209.
    Pubmed CrossRef
  18. Lim BK, Yun SH, Ju ES, Gil CO, Kim DK, Jeon ES. 2012. Role of the myristoylation site in expressing exogenous functional proteins in coxsackieviral vector. Biosci. Biotechnol. Biochem. 76: 1173-1176.
    Pubmed CrossRef
  19. Liu P, Martino T, Opavsky MA, Penninger J. 1996. Viral myocarditis: balance between viral infection and immune response. Can. J. Cardiol. 12: 935-943.
    Pubmed
  20. Martino TA, Liu P, Sole MJ. 1994. Viral infection and the pathogenesis of dilated cardiomyopathy. Circ. Res. 74: 182188.
    CrossRef
  21. Schnitzler P, Neuner A, Nolkemper S, Zundel C, Nowack H, Sensch KH, Reichling J. 2010. Antiviral activity and mode of action of propolis extracts and selected compounds. Phytother. Res. 24 Suppl 1: S20-S28.
    Pubmed CrossRef
  22. Song JH, Kwon BE, Jang H, Kang H, Cho S, Park K, et al. 2015. Antiviral activity of chrysin derivatives against coxsackievirus B3 in vitro and in vivo. Biomol. Ther. (Seoul) 23: 465-470.
    Pubmed KoreaMed CrossRef
  23. Sun F, Li Y, Jia T, Ling Y, Liang L, Liu G, et al. 2012. Differential expression of coxsackievirus and adenovirus receptor on alveolar epithelial cells between fetal and adult mice determines their different susceptibility to coxsackievirus B infection. Arch. Virol. 157: 1101-1111.
    Pubmed CrossRef
  24. Wang SM, Liu CC. 2014. Update of enterovirus 71 infection:epidemiology, pathogenesis and vaccine. Expert Rev. Anti Infect. Ther. 12: 447-456.
    Pubmed CrossRef
  25. Wong J, Zhang J, Yanagawa B, Luo Z, Yang X, Chang J, et al. 2012. Cleavage of serum response factor mediated by enteroviral protease 2A contributes to impaired cardiac function. Cell Res. 22: 360-371.
    Pubmed KoreaMed CrossRef
  26. Woodruff JF. 1980. Viral myocarditis. A review. Am. J. Pathol. 101: 425-484.
    Pubmed KoreaMed
  27. Xiong D, Lee GH, Badorff C, Dorner A, Lee S, Wolf P, Knowlton KU. 2002. Dystrophin deficiency markedly increases enterovirus-induced cardiomyopathy: a genetic predisposition to viral heart disease. Nat. Med. 8: 872-877.
    CrossRef
  28. Xiong D, Yajima T, Lim BK, Stenbit A, Dublin A, Dalton ND, et al. 2007. Inducible cardiac-restricted expression of enteroviral protease 2A is sufficient to induce dilated cardiomyopathy. Circulation 115: 94-102.
    Pubmed CrossRef
  29. Yu J, Sun L, Zhou L, Luo X, Guo J, Liu C, Cong P. 1997. [Chemical constituents of fructus Amomi]. Zhongguo Zhong Yao Za Zhi 22: 231-232, 255.
  30. Yun SH, Lee WG, Kim YC, Ju ES, Lim BK, Choi JO, et al. 2012. Antiviral activity of coxsackievirus B3 3C protease inhibitor in experimental murine myocarditis. J. Infect. Dis. 205: 491-497.
    Pubmed CrossRef