Inhibition of hepatitis E virus replication by peptide-conjugated morpholino oligomers

Antiviral Research

Volumn 120, Issue , 2015, Pages 134-139

  Nan, Yuchen ^a   Ma, Zexu ^a   Kannan, Harilakshmi ^a,e   Stein, David A ^c   Iversen, Patrick I ^c   Meng, Xiang Jin ^d   Zhang, Yan Jin ^a,b  

^a UNIVERSITY OF MARYLAND   (United States)

^b University of Maryland   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^e MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Antisense; Antiviral; Hepatitis E virus; Morpholino oligomers; PPMO

Indexed keywords

ANTIVIRUS AGENT; CAPSID PROTEIN; OLIGOMER; PEPTIDE CONJUGATED MORPHOLINO OLIGOMER; PEPTIDE CONJUGATED MORPHOLINO OLIGOMER HP1; PEPTIDE CONJUGATED MORPHOLINO OLIGOMER HP3U; PEPTIDE CONJUGATED MORPHOLINO OLIGOMER HPN3; UNCLASSIFIED DRUG; ANTISENSE OLIGONUCLEOTIDE; DRUG CARRIER; MORPHOLINO OLIGONUCLEOTIDE; PEPTIDE; VIRUS RNA;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DRUG POTENCY; HEPATITIS B; HEPATITIS E VIRUS; HUMAN; HUMAN CELL; LIVER CELL; PRIORITY JOURNAL; RNA TRANSLATION; VIRUS GENOME; VIRUS INHIBITION; VIRUS ISOLATION; VIRUS REPLICATION; CELL LINE; DRUG EFFECTS; METABOLISM; MICROBIAL SENSITIVITY TEST; PHYSIOLOGY; VIROLOGY; VIRUS LOAD;

HEPATITIS E VIRUS; MIRIDAE;

ANTIVIRAL AGENTS; CAPSID PROTEINS; CELL LINE; DRUG CARRIERS; HEPATITIS E VIRUS; HEPATOCYTES; HUMANS; MICROBIAL SENSITIVITY TESTS; MORPHOLINOS; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDES; RNA, VIRAL; VIRAL LOAD; VIRUS REPLICATION;

EID: 84934943447     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2015.06.006     Document Type: Article

References (41)

1. S. Abes, H.M. Moulton, P. Clair, P. Prevot, D.S. Youngblood, R.P. Wu, P.L. Iversen, and B. Lebleu Vectorization of morpholino oligomers by the (R-Ahx-R)4 peptide allows efficient splicing correction in the absence of endosomolytic agents J. Control. Release 116 2006 304 313
2. I. Ahmad, R.P. Holla, and S. Jameel Molecular virology of hepatitis E virus Virus Res. 161 2011 47 58
3. A. Amantana, H.M. Moulton, M.L. Cate, M.T. Reddy, T. Whitehead, J.N. Hassinger, D.S. Youngblood, and P.L. Iversen Pharmacokinetics, biodistribution, stability and toxicity of a cell-penetrating peptide-morpholino oligomer conjugate Bioconjug. Chem. 18 2007 1325 1331
4. K. Anthony, L. Feng, V. Arechavala-Gomeza, M. Guglieri, V. Straub, K. Bushby, S. Cirak, J. Morgan, and F. Muntoni Exon skipping quantification by quantitative reverse-transcription polymerase chain reaction in Duchenne muscular dystrophy patients treated with the antisense oligomer eteplirsen Hum. Gene Ther. Methods 23 2012 336 345
5. R. Burrer, B.W. Neuman, J.P. Ting, D.A. Stein, H.M. Moulton, P.L. Iversen, P. Kuhn, and M.J. Buchmeier Antiviral effects of antisense morpholino oligomers in murine coronavirus infection models J. Virol. 81 2007 5637 5648
6. S. Emerson, D. Anderson, V.A. Arankalle, X.-J. Meng, M. Purdy, G.G. Schlauder, and S. Tsarev Hepevirus C.M. Fauquest, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball, Virus Taxonomy, VIIIth Report of the ICTV 2004 Elseiver/Academic Press London, UK
7. R. Gerolami, P. Borentain, F. Raissouni, A. Motte, C. Solas, and P. Colson Treatment of severe acute hepatitis E by ribavirin J. Clin. Virol. 52 2011 60 62
8. J. Graff, H. Nguyen, C. Yu, W.R. Elkins, M. St Claire, R.H. Purcell, and S.U. Emerson The open reading frame 3 gene of hepatitis E virus contains a cis-reactive element and encodes a protein required for infection of macaques J. Virol. 79 2005 6680 6689
9. J. Graff, U. Torian, H. Nguyen, and S.U. Emerson A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus J. Virol. 80 2006 5919 5926
10. G. Haqshenas, H.L. Shivaprasad, P.R. Woolcock, D.H. Read, and X.J. Meng Genetic identification and characterization of a novel virus related to human hepatitis E virus from chickens with hepatitis-splenomegaly syndrome in the United States J. Gen. Virol. 82 2001 2449 2462
11. Y.W. Huang, T. Opriessnig, P.G. Halbur, and X.J. Meng Initiation at the third in-frame AUG codon of open reading frame 3 of the hepatitis E virus is essential for viral infectivity in vivo J. Virol. 81 2007 3018 3026
12. S. Jameel Molecular biology and pathogenesis of hepatitis E virus Expert Rev. Mol. Med. 1999 1999 1 16
13. N. Kamar, H.R. Dalton, F. Abravanel, and J. Izopet Hepatitis E virus infection Clin. Microbiol. Rev. 27 2014 116 138
14. N. Kamar, J. Izopet, S. Tripon, M. Bismuth, S. Hillaire, J. Dumortier, S. Radenne, A. Coilly, V. Garrigue, L. D'Alteroche, M. Buchler, L. Couzi, P. Lebray, S. Dharancy, A. Minello, M. Hourmant, A.M. Roque-Afonso, F. Abravanel, S. Pol, L. Rostaing, and V. Mallet Ribavirin for chronic hepatitis E virus infection in transplant recipients N. Engl. J. Med. 370 2014 1111 1120
15. N. Kamar, L. Rostaing, F. Abravanel, C. Garrouste, S. Lhomme, L. Esposito, G. Basse, O. Cointault, D. Ribes, M.B. Nogier, L. Alric, J.M. Peron, and J. Izopet Ribavirin therapy inhibits viral replication on patients with chronic hepatitis e virus infection Gastroenterology 139 2010 1612 1618
16. S. Kumar, S. Subhadra, B. Singh, and B.K. Panda Hepatitis E virus: the current scenario Int. J. Infect. Dis. 17 2013 e228 e233
17. T.C. Li, K. Chijiwa, N. Sera, T. Ishibashi, Y. Etoh, Y. Shinohara, Y. Kurata, M. Ishida, S. Sakamoto, N. Takeda, and T. Miyamura Hepatitis E virus transmission from wild boar meat Emerg. Infect. Dis. 11 2005 1958 1960
18. L. Lu, C. Li, and C.H. Hagedorn Phylogenetic analysis of global hepatitis E virus sequences: genetic diversity, subtypes and zoonosis Rev. Med. Virol. 16 2006 5 36
19. V. Mallet, E. Nicand, P. Sultanik, C. Chakvetadze, S. Tesse, E. Thervet, L. Mouthon, P. Sogni, and S. Pol Brief communication: case reports of ribavirin treatment for chronic hepatitis E Ann. Intern. Med. 153 2010 85 89
20. J.R. Mendell, L.R. Rodino-Klapac, Z. Sahenk, K. Roush, L. Bird, L.P. Lowes, L. Alfano, A.M. Gomez, S. Lewis, J. Kota, V. Malik, K. Shontz, C.M. Walker, K.M. Flanigan, M. Corridore, J.R. Kean, H.D. Allen, C. Shilling, K.R. Melia, P. Sazani, J.B. Saoud, and E.M. Kaye Eteplirsen for the treatment of Duchenne muscular dystrophy Ann. Neurol. 74 2013 637 647
21. X.J. Meng Recent advances in hepatitis E virus J. Viral Hepatitis 17 2010 153 161
22. X.J. Meng From barnyard to food table: the omnipresence of hepatitis E virus and risk for zoonotic infection and food safety Virus Res. 161 2011 23 30
23. X.J. Meng, P.G. Halbur, M.S. Shapiro, S. Govindarajan, J.D. Bruna, I.K. Mushahwar, R.H. Purcell, and S.U. Emerson Genetic and experimental evidence for cross-species infection by swine hepatitis E virus J. Virol. 72 1998 9714 9721
24. X.J. Meng, R.H. Purcell, P.G. Halbur, J.R. Lehman, D.M. Webb, T.S. Tsareva, J.S. Haynes, B.J. Thacker, and S.U. Emerson A novel virus in swine is closely related to the human hepatitis E virus Proc. Natl. Acad. Sci. USA 94 1997 9860 9865
25. H.M. Moulton In vivo delivery of morpholino oligos by cell-penetrating peptides Curr. Pharm. Des. 19 2013 2963 2969
26. Y. Nan, Z. Ma, R. Wang, Y. Yu, H. Kannan, B. Fredericksen, and Y.J. Zhang Enhancement of interferon induction by ORF3 product of hepatitis E Virus J. Virol. 88 2014 8696 8705
27. Y. Nan, R. Wang, M. Shen, K.S. Faaberg, S.K. Samal, and Y.J. Zhang Induction of type I interferons by a novel porcine reproductive and respiratory syndrome virus isolate Virology 432 2012 261 270
28. Y. Nan, Y. Yu, Z. Ma, S.K. Khattar, B. Fredericksen, and Y.J. Zhang Hepatitis E virus inhibits type I interferon induction by ORF1 product J. Virol. 88 2014 11924 11932
29. S. Paessler, R. Rijnbrand, D.A. Stein, H. Ni, N.E. Yun, N. Dziuba, V. Borisevich, A. Seregin, Y. Ma, R. Blouch, P.L. Iversen, and M.A. Zacks Inhibition of alphavirus infection in cell culture and in mice with antisense morpholino oligomers Virology 376 2008 357 370
30. D. Patel, Y. Nan, M. Shen, K. Ritthipichai, X. Zhu, and Y.J. Zhang Porcine reproductive and respiratory syndrome virus inhibits type I interferon signaling by blocking STAT1/STAT2 nuclear translocation J. Virol. 84 2010 11045 11055
31. S. Pischke, S. Hardtke, U. Bode, S. Birkner, C. Chatzikyrkou, W. Kauffmann, C.L. Bara, J. Gottlieb, J. Wenzel, M.P. Manns, and H. Wedemeyer Ribavirin treatment of acute and chronic hepatitis E: a single-centre experience Liver Int. 33 2013 722 726
32. M.A. Riddell, F. Li, and D.A. Anderson Identification of immunodominant and conformational epitopes in the capsid protein of hepatitis E virus by using monoclonal antibodies J. Virol. 74 2000 8011 8017
33. P. Shukla, H.T. Nguyen, U. Torian, R.E. Engle, K. Faulk, H.R. Dalton, R.P. Bendall, F.E. Keane, R.H. Purcell, and S.U. Emerson Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant Proc. Natl. Acad. Sci. USA 108 2011 2438 2443
34. D.B. Smith, P. Simmonds, S. Jameel, S.U. Emerson, T.J. Harrison, X.J. Meng, H. Okamoto, W.H. Van der Poel, and M.A. Purdy Consensus proposals for classification of the family Hepeviridae J. Gen. Virol. 95 2014 2223 2232
35. D.A. Stein Inhibition of RNA virus infections with peptide-conjugated morpholino oligomers Curr. Pharm. Des. 14 2008 2619 2634
36. J. Summerton Morpholino antisense oligomers: the case for an RNase H-independent structural type Biochim. Biophys. Acta 1489 1999 141 158
37. A.W. Tam, M.M. Smith, M.E. Guerra, C.C. Huang, D.W. Bradley, K.E. Fry, and G.R. Reyes Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome Virology 185 1991 120 131
38. H. Wedemeyer, S. Pischke, and M.P. Manns Pathogenesis and treatment of hepatitis E virus infection Gastroenterology 142 1388-1397 2012 e1381
39. Y.J. Zhang, R.S. Bonaparte, D. Patel, D.A. Stein, and P.L. Iversen Blockade of viral interleukin-6 expression of Kaposi's sarcoma-associated herpesvirus Mol. Cancer Ther. 7 2008 712 720
40. Y.J. Zhang, D.A. Stein, S.M. Fan, K.Y. Wang, A.D. Kroeker, X.J. Meng, P.L. Iversen, and D.O. Matson Suppression of porcine reproductive and respiratory syndrome virus replication by morpholino antisense oligomers Vet. Microbiol. 117 2006 117 129
41. Y.J. Zhang, K.Y. Wang, D.A. Stein, D. Patel, R. Watkins, H.M. Moulton, P.L. Iversen, and D.O. Matson Inhibition of replication and transcription activator and latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus by morpholino oligomers Antiviral Res. 73 2007 12 23