Increasing expression of microrna 181 inhibits porcine reproductive and respiratory syndrome virus replication and has implications for controlling virus infection

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 1159-1171

  Guo, Xue kun ^a   Zhang, Qiong ^a   Gao, Li ^a   Li, Ning ^a   Chen, Xin xin ^a   Feng, Wen Hai ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; MESSENGER RNA; MICRORNA; MICRORNA 181; MICRORNA 181C; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL THERAPY; ARTERIVIRUS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; MOLECULAR THERAPY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; RNA ANALYSIS; RNA BINDING; RNA INTERFERENCE; SWINE; VIRUS GENOME; VIRUS INFECTION; VIRUS INHIBITION; VIRUS LOAD; VIRUS PATHOGENESIS; VIRUS REPLICATION;

ANIMALS; CELL LINE; MICRORNAS; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RNA, VIRAL; SWINE; VIRUS REPLICATION;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE;

EID: 84872001370     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02386-12     Document Type: Article

References (60)

1. Tian K, Yu X, Zhao T, Feng Y, Cao Z, Wang C, Hu Y, Chen X, Hu D, Tian X, Liu D, Zhang S, Deng X, Ding Y, Yang L, Zhang Y, Xiao H, Qiao M, Wang B, Hou L, Wang X, Yang X, Kang L, Sun M, Jin P, Wang S, Kitamura Y, Yan J, Gao GF. 2007. Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One 2:e526. doi:10.1371/ journal.pone.0000526.
2. Thiel HJ, Meyers G, Stark R, Tautz N, Rumenapf T, Unger G, Conzelmann KK. 1993. Molecular characterization of positive-strand RNA viruses: pestiviruses and the porcine reproductive and respiratory syndrome virus (PRRSV). Arch. Virol. Suppl. 7:41-52.
3. Lecellier CH, Dunoyer P, Arar K, Lehmann-Che J, Eyquem S, Himber C, Saib A, Voinnet O. 2005. A cellular microRNA mediates antiviral defense in human cells. Science 308:557-560.
4. Li HW, Ding SW. 2005. Antiviral silencing in animals. FEBS Lett. 579: 5965-5973.
5. Nathans R, Chu CY, Serquina AK, Lu CC, Cao H, Rana TM. 2009. Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol. Cell 34:696-709.
6. Otsuka M, Jing Q, Georgel P, New L, Chen JM, Mols J, Kang YJ, Jiang ZF, Du X, Cook R, Das SC, Pattnaik AK, Beutler B, Han JH. 2007. Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 27:123-134.
7. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M. 2007. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449:919-922.
8. Song L, Liu H, Gao S, Jiang W, Huang W. 2010. Cellular microRNAs inhibit replication of the H1N1 influenza A virus in infected cells. J. Virol. 84:8849-8860.
9. Chen Y, Shen A, Rider PJ, Yu Y, Wu K, Mu Y, Hao Q, Liu Y, Gong H, Zhu Y, Liu F, Wu J. 2011. A liver-specific microRNA binds to a highly conserved RNA sequence of hepatitis B virus and negatively regulates viral gene expression and replication. FASEB J. 25:4511-4521.
10. Gottwein E, Cullen BR. 2008. Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3:375-387.
11. Huang J, Wang F, Argyris E, Chen K, Liang Z, Tian H, Huang W, Squires K, Verlinghieri G, Zhang H. 2007. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat. Med. 13:1241-1247.
12. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T. 2004. Identification of virusencoded microRNAs. Science 304:734-736.
13. Umbach JL, Kramer MF, Jurak I, Karnowski HW, Coen DM, Cullen BR. 2008. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454:780-783.
14. Lu CC, Li Z, Chu CY, Feng J, Sun R, Rana TM. 2010. MicroRNAs encoded by Kaposi's sarcoma-associated herpesvirus regulate viral life cycle. EMBO Rep. 11:784-790.
15. Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, Kim YK, Kim YE, Ahn JH, Riddell SR, Stratikos E, Kim VN, Ahn K. 2011. Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat. Immunol. 12:984-991.
16. Nachmani D, Lankry D, Wolf DG, Mandelboim O. 2010. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat. Immunol. 11:806-813.
17. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577-1581.
18. Lodish HF, Zhou B, Liu G, Chen CZ. 2008. Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol. 8:120-130.
19. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. 2010. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10:111-122.
20. Davidson BL, McCray PB, Jr. 2011. Current prospects for RNA interference-based therapies. Nat. Rev. Genet. 12:329-340.
21. Bitko V, Musiyenko A, Shulyayeva O, Barik S. 2005. Inhibition of respiratory viruses by nasally administered siRNA. Nat. Med. 11:50-55.
22. Geisbert TW, Lee AC, Robbins M, Geisbert JB, Honko AN, Sood V, Johnson JC, de Jong S, Tavakoli I, Judge A, Hensley LE, Maclachlan I. 2010. Postexposure protection of non-human primates against a lethal Ebola virus challenge with RNA interference: a proof-of-concept study. Lancet 375:1896-1905.
23. Li BJ, Tang Q, Cheng D, Qin C, Xie FY, Wei Q, Xu J, Liu Y, Zheng BJ, Woodle MC, Zhong N, Lu PY. 2005. Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque. Nat. Med. 11:944-951.
24. Palliser D, Chowdhury D, Wang QY, Lee SJ, Bronson RT, Knipe DM, Lieberman J. 2006. An siRNA-based microbicide protects mice from lethal herpes simplex virus 2 infection. Nature 439:89-94.
25. Tompkins SM, Lo CY, Tumpey TM, Epstein SL. 2004. Protection against lethal influenza virus challenge by RNA interference in vivo. Proc. Natl. Acad. Sci. U. S. A. 101:8682-8686.
26. Wu Y, Navarro F, Lal A, Basar E, Pandey RK, Manoharan M, Feng Y, Lee SJ, Lieberman J, Palliser D. 2009. Durable protection from herpes simplex virus-2 transmission following intravaginal application of siRNAs targeting both a viral and host gene. Cell Host Microbe 5:84-94.
27. Zhang W, Yang H, Kong X, Mohapatra S, San Juan-Vergara H, Hellermann G, Behera S, Singam R, Lockey RF, Mohapatra SS. 2005. Inhibition of respiratory syncytial virus infection with intranasal siRNA nanoparticles targeting the viral NS1 gene. Nat. Med. 11:56-62.
28. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, Kauppinen S, Orum H. 2010. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327:198-201.
29. Pasternak AO, Spaan WJ, Snijder EJ. 2006. Nidovirus transcription: how to make sense.? J. Gen. Virol. 87:1403-1421.
30. Hu S, Chao CC, Khanna KV, Gekker G, Peterson PK, Molitor TW. 1996. Cytokine and free radical production by porcine microglia. Clin. Immunol. Immunopathol. 78:93-96.
31. Zhou L, Zhang J, Zeng J, Yin S, Li Y, Zheng L, Guo X, Ge X, Yang H. 2009. The 30-amino-acid deletion in the Nsp2 of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China is not related to its virulence. J. Virol. 83:5156-5167.
32. Huang HY, Chien CH, Jen KH, Huang HD. 2006. RegRNA: an integrated web server for identifying regulatory RNA motifs and elements. Nucleic Acids Res. 34:W429-W434.
33. Hsu PW, Lin LZ, Hsu SD, Hsu JB, Huang HD. 2007. ViTa: prediction of host microRNAs targets on viruses. Nucleic Acids Res. 35:D381-D385.
34. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233.
35. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
36. Yang CH, Yue J, Fan M, Pfeffer LM. 2010. IFN induces miR-21 through a signal transducer and activator of transcription 3-dependent pathway as a suppressive negative feedback on IFN-induced apoptosis. Cancer Res. 70:8108-8116.
37. Bookout AL, Cummins CL, Mangelsdorf DJ, Pesola JM, Kramer MF. 2006. High-throughput real-time quantitative reverse transcription PCR. Curr. Protoc. Mol. Biol. 73:15.8.1-15.8.28.
38. Moreno JL, Zuniga S, Enjuanes L, Sola I. 2008. Identification of a coronavirus transcription enhancer. J. Virol. 82:3882-3893.
39. Fu Y, Quan R, Zhang H, Hou J, Tang J, Feng WH. 2012. Porcine reproductive and respiratory syndrome virus induces interleukin-15 through the NF-κB signaling pathway. J. Virol. 86:7625-7636.
40. Wang W-X, Wilfred BR, Hu Y, Stromberg AJ, Nelson PT. 2010. Anti-Argonaute RIP-Chip shows that miRNA transfections alter global patterns of mRNA recruitment to microribonucleoprotein complexes. RNA 16:394-404.
41. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. 2011. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146:353-358.
42. Van Breedam W, Delputte PL, Van Gorp H, Misinzo G, Vanderheijden N, Duan XB, Nauwynck HJ. 2010. Porcine reproductive and respiratory syndrome virus entry into the porcine macrophage. J. Gen. Virol. 91: 1659-1667.
43. Rossow KD, Shivers JL, Yeske PE, Polson DD, Rowland RRR, Lawson SR, Murtaugh MP, Nelson EA, Collins JE. 1999. Porcine reproductive and respiratory syndrome virus infection in neonatal pigs characterised by marked neurovirulence. Vet. Rec. 144:444-448.
44. Christopher-Hennings J, Holler LD, Benfield DA, Nelson EA. 2001. Detection and duration of porcine reproductive and respiratory syndrome virus in semen, serum, peripheral blood mononuclear cells, and tissues from Yorkshire, Hampshire, and Landrace boars. J. Vet. Diagn. Invest. 13:133-142.
45. Duan X, Nauwynck HJ, Pensaert MB. 1997. Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV). Arch. Virol. 142:2483-2497.
46. Ghanayem NS, Yee L, Nelson T, Wong S, Gordon JB, Marcdante K, Rice TB. 2001. Stability of dopamine and epinephrine solutions up to 84 hours. Pediatr. Crit. Care Med. 2:315-317.
47. Umbach JL, Cullen BR. 2009. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 23:1151-1164.
48. Cullen BR. 2006. Viruses and microRNAs. Nat. Genet. 38(Suppl):S25-S30.
49. Fukuhara T, Kambara H, Shiokawa M, Ono C, Katoh H, Morita E, Okuzaki D, Maehara Y, Koike K, Matsuura Y. 2012. Expression of microRNA miR-122 facilitates an efficient replication in nonhepatic cells upon infection with hepatitis C virus. J. Virol. 86:7918-7933.
50. Jackson AL, Linsley PS. 2010. Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat. Rev. Drug Discov. 9:57-67.
51. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-63.
52. Chen CZ, Li L, Lodish HF, Bartel DP. 2004. MicroRNAs modulate hematopoietic lineage differentiation. Science 303:83-86.
53. Cichocki F, Felices M, McCullar V, Presnell SR, Al-Attar A, Lutz CT, Miller JS. 2011. Cutting edge: microRNA-181 promotes human NK cell development by regulating Notch signaling. J. Immunol. 187:6171-6175.
54. Li QJ, Chau J, Ebert PJ, Sylvester G, Min H, Liu G, Braich R, Manoharan M, Soutschek J, Skare P, Klein LO, Davis MM, Chen CZ. 2007. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 129:147-161.
55. Neilson JR, Zheng GXY, Burge CB, Sharp PA. 2007. Dynamic regulation of miRNA expression in ordered stages of cellular development. Genes Dev. 21:578-589.
56. Boden D, Pusch O, Lee F, Tucker L, Ramratnam B. 2003. Human immunodeficiency virus type 1 escape from RNA interference. J. Virol. 77:11531-11535.
57. Das AT, Brummelkamp TR, Westerhout EM, Vink M, Madiredjo M, Bernards R, Berkhout B. 2004. Human immunodeficiency virus type 1 escapes from RNA interference-mediated inhibition. J. Virol. 78:2601-2605.
58. Prieto C, Vazquez A, Nunez JI, Alvarez E, Simarro I, Castro JM. 2009. Influence of time on the genetic heterogeneity of Spanish porcine reproductive and respiratory syndrome virus isolates. Vet. J. 180:363-370.
59. Heiss BL, Maximova OA, Thach DC, Speicher JM, Pletnev AG. 2012. MicroRNA targeting of neurotropic flavivirus: effective control of virus escape and reversion to neurovirulent phenotype. J. Virol. 86:5647-5659.
60. Kelly EJ, Nace R, Barber GN, Russell SJ. 2010. Attenuation of vesicular stomatitis virus encephalitis through microRNA targeting. J. Virol. 84: 1550-1562. miR-181 Inhibits PRRSV Replication January