Bmnpv-miR-3 facilitates BmNPV infection by modulating the expression of viral P6.9 and other late genes in Bombyx mori

Insect Biochemistry and Molecular Biology

Volumn 49, Issue 1, 2014, Pages 59-69

  Singh, C P ^a   Singh, J ^b   Nagaraju, J ^a  

^a CENTRE FOR DNA FINGERPRINTING AND DIAGNOSTICS   (India)

^b NATIONAL CENTRE FOR CELL SCIENCE   (India)

Author keywords

Baculovirus; BmNPV; Bombyx mori; MiRNA; P6.9

Indexed keywords

MICRORNA; VIRUS PROTEIN; VIRUS RNA;

ANIMAL; BACULOVIRIDAE; BOMBYX; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; VIROLOGY;

ANIMALS; BOMBYX; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; MICRORNAS; NUCLEOPOLYHEDROVIRUS; RNA, VIRAL; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

EID: 84898789147     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2014.03.008     Document Type: Article

References (67)

1. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
2. Asgari S. microRNA functions in insects. Insect Biochem. Mol. Biol. 2013, 43:388-397.
3. Bao Y.Y., Lv Z.Y., Liu Z.B., Xue J., Xu Y.P., Zhang C.X. Comparative analysis of Bombyx mori nucleopolyhedrovirus responsive genes in fat body and haemocyte of B. mori resistant and susceptible strains. Insect Mol. Biol. 2010, 19:347-358.
4. Bao Y.Y., Tang X.D., Lv Z.Y., Wang X.Y., Tian C.H., Xu Y.P., Zhang C.X. Gene expression profiling of resistant and susceptible Bombyx mori strains reveals nucleopolyhedrovirus-associated variations in host gene transcript levels. Genomics 2009, 94:138-145.
5. Barrett J.W., Brownwright A.J., Primavera M.J., Palli S.R. Studies of the nucleopolyhedrovirus infection process in insects by using the green fluorescence protein as a reporter. J.Virol. 1998, 72:3377-3382.
6. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
7. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
8. Borca M.V., Irusta P.M., Kutish G.F., Carillo C., Afonso C.L., Burrage A.T., Neilan J.G., Rock D.L. Astructural DNA binding protein of African swine fever virus with similarity to bacterial histone-like proteins. Arch. Virol. 1996, 141:301-313.
9. Cantalupo P., Doering A., Sullivan C.S., Pal A., Peden K.W., Lewis A.M., Pipas J.M. Complete nucleotide sequence of polyomavirus SA12. J.Virol. 2005, 79:13094-13104.
10. Chendrimada T.P., Gregory R.I., Kumaraswamy E., Norman J., Cooch N., Nishikura K., Shiekhattar R. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 2005, 436:740-744.
11. Choy E.Y., Siu K.L., Kok K.H., Lung R.W., Tsang C.M., To K.F., Kwong D.L., Tsao S.W., Jin D.Y. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J.Exp. Med. 2008, 205:2551-2560.
12. Cullen B.R. Transcription and processing of human microRNA precursors. Mol. Cell. 2004, 16:861-865.
13. Cullen B.R. MicroRNAs as mediators of viral evasion of the immune system. Nat. Immunol. 2013, 14:205-210.
14. Elbashir S.M., Lendeckel W., Tuschl T. RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes. Dev. 2001, 15:188-200.
15. Elbashir S.M., Martinez J., Patkaniowska A., Lendeckel W., Tuschl T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J. 2001, 20:6877-6888.
16. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6:259-269.
17. Gottwein E., Mukherjee N., Sachse C., Frenzel C., Majoros W.H., Chi J.T., Braich R., Manoharan M., Soutschek J., Ohler U., Cullen B.R. Aviral microRNA functions as an orthologue of cellular miR-155. Nature 2007, 450:1096-1099.
18. Grey F., Meyers H., White E.A., Spector D.H., Nelson J. Ahuman cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog. 2007, 3:e163.
19. Grishok A., Pasquinelli A.E., Conte D., Li N., Parrish S., Ha I., Baillie D.L., Fire A., Ruvkun G., Mello C.C. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 2001, 106:23-34.
20. Grundhoff A., Sullivan C.S. Virus-encoded microRNAs. Virology 2011, 411:325-343.
21. Guarino L.A., Xu B., Jin J., Dong W. Avirus-encoded RNA polymerase purified from baculovirus-infected cells. J.Virol. 1998, 72:7985-7991.
22. Hussain M., Taft R.J., Asgari S. An insect virus-encoded microRNA regulates viral replication. J.Virol. 2008, 82:9164-9170.
23. Hutvagner G., McLachlan J., Pasquinelli A.E., Balint E., Tuschl T., Zamore P.D. Acellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293:834-838.
24. Katsuma S., Mita K., Shimada T. ERK- and JNK-dependent signaling pathways contribute to Bombyx mori nucleopolyhedrovirus infection. J.Virol. 2007, 81:13700-13709.
25. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., Plasterk R.H. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes. Dev. 2001, 15:2654-2659.
26. Kincaid R.P., Sullivan C.S. Virus-encoded microRNAs: an overview and a look to the future. PLoS Pathog. 2012, 8:e1003018.
27. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
28. Liu X., Zhao H., Fang Z., Yuan M., Yang K., Pang Y. Distribution and phosphorylation of the basic protein P6.9 of Autographa californica nucleopolyhedrovirus. J.Virol. 2012, 86:12217-12227.
29. Lo A.K., To K.F., Lo K.W., Lung R.W., Hui J.W., Liao G., Hayward S.D. Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc. Natl. Acad. Sci. U S A 2007, 104:16164-16169.
30. Lu A., Miller L.K. Identification of three late expression factor genes within the 33.8- to 43.4-map-unit region of Autographa californica nuclear polyhedrosis virus. J.Virol. 1994, 68:6710-6718.
31. Maeda S., Kamita S.G., Kataoka H. The basic DNA-binding protein of Bombyx mori nuclear polyhedrosis virus: the existence of an additional arginine repeat. Virology 1991, 180:807-810.
32. Marques J.T., Carthew R.W. Acall to arms: coevolution of animal viruses and host innate immune responses. Trends Genet. 2007, 23:359-364.
33. Mehrabadi M., Hussain M., Asgari S. MicroRNAome of Spodoptera frugiperda cells (Sf9) and its alteration following baculovirus infection. J.Gen. Virol. 2013, 94:1385-1397.
34. Meister G., Landthaler M., Patkaniowska A., Dorsett Y., Teng G., Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell. 2004, 15:185-197.
35. Mirza M.A., Weber J. Structure of adenovirus chromatin. Biochim. Biophys. Acta 1982, 696:76-86.
36. Moreno-Habel D.A., Biglang-awa I.M., Dulce A., Luu D.D., Garcia P., Weers P.M., Haas-Stapleton E.J. Inactivation of the budded virus of Autographa californica M nucleopolyhedrovirus by gloverin. J.Invertebr. Pathol. 2012, 110:92-101.
37. Murphy E., Vanicek J., Robins H., Shenk T., Levine A.J. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc. Natl. Acad. Sci. U S A 2008, 105:5453-5458.
38. Nachmani D., Stern-Ginossar N., Sarid R., Mandelboim O. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell. Host Microbe 2009, 5:376-385.
39. Pfeffer S., Sewer A., Lagos-Quintana M., Sheridan R., Sander C., Grasser F.A., van Dyk L.F., Ho C.K., Shuman S., Chien M., Russo J.J., Ju J., Randall G., Lindenbach B.D., Rice C.M., Simon V., Ho D.D., Zavolan M., Tuschl T. Identification of microRNAs of the herpesvirus family. Nat. Meth. 2005, 2:269-276.
40. Pfeffer S., Zavolan M., Grasser F.A., Chien M., Russo J.J., Ju J., John B., Enright A.J., Marks D., Sander C., Tuschl T. Identification of virus-encoded microRNAs. Science 2004, 304:734-736.
41. Rahman M.M., Gopinathan K.P. Systemic and invitro infection process of Bombyx mori nucleopolyhedrovirus. Virus Res. 2004, 101:109-118.
42. Rehmsmeier M., Steffen P., Hochsmann M., Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA 2004, 10:1507-1517.
43. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
44. Rohrmann G.F. Baculovirus Molecular Biology 2011, National Center for Biotechnology Information (US).
45. Samols M.A., Skalsky R.L., Maldonado A.M., Riva A., Lopez M.C., Baker H.V., Renne R. Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog. 2007, 3:e65.
46. Seo G.J., Chen C.J., Sullivan C.S. Merkel cell polyomavirus encodes a microRNA with the ability to autoregulate viral gene expression. Virology 2009, 383:183-187.
47. Singh C.P., Singh J., Nagaraju J. Abaculovirus-encoded MicroRNA (miRNA) suppresses its host miRNA biogenesis by regulating the exportin-5 cofactor Ran. J.Virol. 2012, 86:7867-7879.
48. Singh J., Singh C.P., Bhavani A., Nagaraju J. Discovering microRNAs from Bombyx mori nucleopolyhedrosis virus. Virology 2010, 407:120-128.
49. Skalsky R.L., Cullen B.R. Viruses, microRNAs, and host interactions. Annu Rev. Microbiol. 2010, 64:123-141.
50. Skalsky R.L., Samols M.A., Plaisance K.B., Boss I.W., Riva A., Lopez M.C., Baker H.V., Renne R. Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J.Virol. 2007, 81:12836-12845.
51. Stern-Ginossar N., Elefant N., Zimmermann A., Wolf D.G., Saleh N., Biton M., Horwitz E., Prokocimer Z., Prichard M., Hahn G., Goldman-Wohl D., Greenfield C., Yagel S., Hengel H., Altuvia Y., Margalit H., Mandelboim O. Host immune system gene targeting by a viral miRNA. Science 2007, 317:376-381.
52. Sullivan C.S. New roles for large and small viral RNAs in evading host defences. Nat. Rev. Genet. 2008, 9:503-507.
53. Sullivan C.S., Grundhoff A.T., Tevethia S., Pipas J.M., Ganem D. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 2005, 435:682-686.
54. Sullivan C.S., Sung C.K., Pack C.D., Grundhoff A., Lukacher A.E., Benjamin T.L., Ganem D. Murine Polyomavirus encodes a microRNA that cleaves early RNA transcripts but is not essential for experimental infection. Virology 2009, 387:157-167.
55. Tomari Y., Du T., Zamore P.D. Sorting of Drosophila small silencing RNAs. Cell 2007, 130:299-308.
56. Umbach J.L., Kramer M.F., Jurak I., Karnowski H.W., Coen D.M., Cullen B.R. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008, 454:780-783.
57. van Oers M.M., Vlak J.M. Baculovirus genomics. Curr. Drug. Targets 2007, 8:1051-1068.
58. Wang M., Tuladhar E., Shen S., Wang H., van Oers M.M., Vlak J.M., Westenberg M. Specificity of baculovirus P6.9 basic DNA-binding proteins and critical role of the C terminus in virion formation. J.Virol. 2010, 84:8821-8828.
59. Wang Q., Liu Y., He H.J., Zhao X.F., Wang J.X. Immune responses of Helicoverpa armigera to different kinds of pathogens. BMC Immunol. 2010, 11:9.
60. Watanabe H. Resistance of the silkworm, Bombyx mori, to viral infections. Agri. Ecosyst. Environ. 1986, 15:131-139.
61. Watanabe H. Genetic resistance of the silkworm, Bombyx mori to viral diseases. Curr. Sci. 2002, 83:439-446.
62. Wu P., Han S., Chen T., Qin G., Li L., Guo X. Involvement of microRNAs in infection of silkworm with bombyx mori cytoplasmic polyhedrosis virus (BmCPV). PLoS One 2013, 8:e68209.
63. Wu Y.L., Wu C.P., Liu C.Y., Hsu P.W., Wu E.C., Chao Y.C. Anon-coding RNA of insect HzNV-1 virus establishes latent viral infection through microRNA. Sci. Rep. 2011, 1:60.
64. Xia T., O'Hara A., Araujo I., Barreto J., Carvalho E., Sapucaia J.B., Ramos J.C., Luz E., Pedroso C., Manrique M., Toomey N.L., Brites C., Dittmer D.P., Harrington W.J. EBV microRNAs in primary lymphomas and targeting of CXCL-11 by ebv-mir-BHRF1-3. Cancer Res. 2008, 68:1436-1442.
65. Xiao C., Rajewsky K. MicroRNA control in the immune system: basic principles. Cell 2009, 136:26-36.
66. Yi R., Qin Y., Macara I.G., Cullen B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes. Dev. 2003, 17:3011-3016.
67. Zeng Y., Cullen B.R. Efficient processing of primary microRNA hairpins by Drosha requires flanking nonstructured RNA sequences. J.Biol. Chem. 2005, 280:27595-27603.