Inhibition of porcine reproductive and respiratory syndrome virus infection in piglets by a peptide-conjugated morpholino oligomer

Antiviral Research

Volumn 91, Issue 1, 2011, Pages 36-42

  Opriessnig, Tanja ^a   Patel, Deendayal ^b   Wang, Rong ^b   Halbur, Patrick G ^a   Meng, Xiang Jin ^c   Stein, David A ^d   Zhang, Yan Jin ^b,e  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c CENTER FOR MOLECULAR MEDICINE AND INFECTIOUS DISEASES   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e Bldg 142   (United States)

Author keywords

Antisense; Antiviral; Morpholino; Porcine reproductive and respiratory syndrome virus; PPMO; PRRSV

Indexed keywords

ANTIVIRUS AGENT; OLIGOMER; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL MODEL; ARTICLE; AUTOPSY; BLOOD SAMPLING; CONTROLLED STUDY; INTERSTITIAL PNEUMONIA; LUNG ALVEOLUS MACROPHAGE; NONHUMAN; PIGLET; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PRIORITY JOURNAL; VIRUS INHIBITION; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; ANTIVIRAL AGENTS; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; MACROPHAGES, ALVEOLAR; MORPHOLINOS; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SWINE; TREATMENT OUTCOME; VIRUS REPLICATION;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS;

EID: 79957445457     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2011.04.012     Document Type: Article

References (42)

1. Abes S., Moulton H.M., Clair P., Prevot P., Youngblood D.S., Wu R.P., Iversen P.L., Lebleu B. Vectorization of morpholino oligomers by the (R-Ahx-R)4 peptide allows efficient splicing correction in the absence of endosomolytic agents. J. Control. Release 2006, 116:304-313.
2. Benfield D.A., Nelson E., Collins J.E., Harris L., Goyal S.M., Bobinson D., Christianson W.T., Morrison R.B., Gorcyca D., Chladek D. Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). J. Vet. Diagn. Invest. 1992, 4:127-133.
3. Carr M.W., Roth S.J., Luther E., Rose S.S., Springer T.A. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc.Natl. Acad. Sci. USA 1994, 91:3652-3656.
4. Conzelmann K.K., Visser N., Van Woensel P., Thiel H.J. Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology 1993, 193:329-339.
5. Eide K., Moerdyk-Schauwecker M., Stein D.A., Bildfell R., Koelle D.M., Jin L. Reduction of herpes simplex virus type-2 replication in cell cultures and in rodent models with peptide-conjugated morpholino oligomers. Antivir. Ther. 2010, 15:1141-1149.
6. Gabriel G., Nordmann A., Stein D.A., Iversen P.L., Klenk H.D. Morpholino oligomers targeting the PB1 and NP genes enhance the survival of mice infected with highly pathogenic influenza A H7N7 virus. J. Gen. Virol. 2008, 89:939-948.
7. Halbur P.G., Andrews J.J., Huffman E.L., Paul P.S., Meng X.J., Niyo Y. Development of a streptavidin-biotin immunoperoxidase procedure for the detection of porcine reproductive and respiratory syndrome virus antigen in porcine lung. J. Vet. Diagn. Invest. 1994, 6:254-257.
8. Halbur P.G., Paul P.S., Frey M.L., Landgraf J., Eernisse K., Meng X.J., Lum M.A., Andrews J.J., Rathje J.A. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet. Pathol. 1995, 32:648-660.
9. Halbur P.G., Paul P.S., Meng X.J., Lum M.A., Andrews J.J., Rathje J.A. Comparative pathogenicity of nine US porcine reproductive and respiratory syndrome virus (PRRSV) isolates in a five-week-old cesarean-derived, colostrum-deprived pig model. J. Vet. Diagn. Invest. 1996, 8:11-20.
10. Han X., Fan S., Patel D., Zhang Y.J. Enhanced inhibition of porcine reproductive and respiratory syndrome virus replication by combination of morpholino oligomers. Antiviral Res. 2009, 82:59-66.
11. Hudziak R.M., Barofsky E., Barofsky D.F., Weller D.L., Huang S.B., Weller D.D. Resistance of morpholino phosphorodiamidate oligomers to enzymatic degradation. Antisense Nucleic Acid Drug Dev. 1996, 6:267-272.
12. Keffaber K.K. Reproductive failure of unknown etiology. Am. Assoc. Swine Pract. Newsletter 1989, 1:1-9.
13. Kim H.S., Kwang J., Yoon I.J., Joo H.S., Frey M.L. Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch. Virol. 1993, 133:477-483.
14. Lai S.H., Stein D.A., Guerrero-Plata A., Liao S.L., Ivanciuc T., Hong C., Iversen P.L., Casola A., Garofalo R.P. Inhibition of respiratory syncytial virus infections with morpholino oligomers in cell cultures and in mice. Mol. Ther. 2008, 16:1120-1128.
15. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
16. Loula T. Mystery pig disease: an update for the practitioner. Agri-Practice 1991, 12:23-34.
17. Lupfer C., Stein D.A., Mourich D.V., Tepper S.E., Iversen P.L., Pastey M. Inhibition of influenza A H3N8 virus infections in mice by morpholino oligomers. Arch. Virol. 2008, 153:929-937.
18. Meng X.J., Paul P.S., Halbur P.G. Molecular cloning and nucleotide sequencing of the 3′ terminal genomic RNA of porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 1994, 75:1795-1801.
19. Meng X.J., Paul P.S., Halbur P.G., Lum M.A. Phylogenetic analyses of the putative M (ORF 6) and N (ORF 7) genes of porcine reproductive and respiratory syndrome virus (PRRSV): implication for the existence of two genotypes of PRRSV in the USA and Europe. Arch. Virol. 1995, 140:745-755.
20. Meulenberg J.J., Hulst M.M., de Meijer E.J., Moonen P.L., den Besten A., de Kluyver E.P., Wensvoort G., Moormann R.J. Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 1993, 192:62-72.
21. Meulenberg J.J., de Meijer E.J., Moormann R.J. Subgenomic RNAs of Lelystad virus contain a conserved leader-body junction sequence. J. Gen. Virol. 1993, 74:1697-1701.
22. Miller M.D., Krangel M.S. The human cytokine I-309 is a monocyte chemoattractant. Proc. Natl. Acad. Sci. USA 1992, 89:2950-2954.
23. Miller L.C., Laegreid W.W., Bono J.L., Chitko-McKown C.G., Fox J.M. Interferon type I response in porcine reproductive and respiratory syndrome virus-infected MARC-145 cells. Arch. Virol. 2004, 149:2453-2463.
24. Moerdyk-Schauwecker M., Stein D.A., Eide K., Blouch R.E., Bildfell R., Iversen P., Jin L. Inhibition of HSV-1 ocular infection with morpholino oligomers targeting ICP0 and ICP27. Antiviral Res. 2009, 84:131-141.
25. Moulton H.M., Nelson M.H., Hatlevig S.A., Reddy M.T., Iversen P.L. Cellular uptake of antisense morpholino oligomers conjugated to arginine-rich peptides. Bioconjug. Chem. 2004, 15:290-299.
26. Murtaugh M.P., Xiao Z., Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol. 2002, 15:533-547.
27. Nelson M.H., Stein D.A., Kroeker A.D., Hatlevig S.A., Iversen P.L., Moulton H.M. Arginine-rich peptide conjugation to morpholino oligomers: effects on antisense activity and specificity. Bioconjug. Chem. 2005, 16:959-966.
28. Neumann E.J., Kliebenstein J.B., Johnson C.D., Mabry J.W., Bush E.J., Seitzinger A.H., Green A.L., Zimmerman J.J. Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J. Am. Vet. Med. Assoc. 2005, 227:385-392.
29. Opriessnig T., Halbur P.G., Yoon K.J., Pogranichniy R.M., Harmon K.M., Evans R., Key K.F., Pallares F.J., Thomas P., Meng X.J. Comparison of molecular and biological characteristics of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine (ingelvac PRRS MLV), the parent strain of the vaccine (ATCC VR2332), ATCC VR2385, and two recent field isolates of PRRSV. J. Virol. 2002, 76:11837-11844.
30. Patel D., Opriessnig T., Stein D.A., Halbur P.G., Meng X.J., Iversen P.L., Zhang Y.J. Peptide-conjugated morpholino oligomers inhibit porcine reproductive and respiratory syndrome virus replication. Antiviral Res. 2008, 77:95-107.
31. Patel D., Stein D.A., Zhang Y.J. Morpholino oligomer-mediated protection of porcine pulmonary alveolar macrophages from arterivirus-induced cell death. Antivir. Ther. 2009, 14:899-909.
32. Silverman R.H. Viral encounters with 2′, 5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 2007, 81:12720-12729.
33. Stein D.A. Inhibition of RNA virus infections with peptide-conjugated morpholino oligomers. Curr. Pharm. Des. 2008, 14:2619-2634.
34. Summerton J. Morpholino antisense oligomers: the case for an RNase H-independent structural type. Biochim. Biophys. Acta 1999, 1489:141-158.
35. Summerton J., Weller D. Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 1997, 7:187-195.
36. Wensvoort G., Terpstra C., Pol J.M., ter Laak E.A., Bloemraad M., de Kluyver E.P., Kragten C., van Buiten L., den Besten A., Wagenaar F., et al. Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet. Q. 1991, 13:121-130.
37. Yoon I.J., Joo H.S., Christianson W.T., Kim H.S., Collins J.E., Carlson J.H., Dee S.A. Isolation of a cytopathic virus from weak pigs on farms with a history of swine infertility and respiratory syndrome. J. Vet. Diagn. Invest. 1992, 4:139-143.
38. Youngblood D.S., Hatlevig S.A., Hassinger J.N., Iversen P.L., Moulton H.M. Stability of cell-penetrating peptide-morpholino oligomer conjugates in human serum and in cells. Bioconjug. Chem. 2007, 18:50-60.
39. Zhang Y.J., Stein D.A., Fan S.M., Wang K.Y., Kroeker A.D., Meng X.J., Iversen P.L., Matson D.O. Suppression of porcine reproductive and respiratory syndrome virus replication by morpholino antisense oligomers. Vet. Microbiol. 2006, 117:117-129.
40. Zhang Y.J., Wang K.Y., Stein D.A., Patel D., Watkins R., Moulton H.M., Iversen P.L., Matson D.O. Inhibition of replication and transcription activator and latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus by morpholino oligomers. Antiviral Res. 2007, 73:12-23.
41. Zhang Y.J., Bonaparte R.S., Patel D., Stein D.A., Iversen P.L. Blockade of viral interleukin-6 expression of Kaposi's sarcoma-associated herpesvirus. Mol. Cancer Ther. 2008, 7:712-720.
42. Zurcher T., Pavlovic J., Staeheli P. Nuclear localization of mouse Mx1 protein is necessary for inhibition of influenza virus. J. Virol. 1992, 66:5059-5066.