BST-2/tetherin-mediated restriction of chikungunya (CHIKV) VLP budding is counteracted by CHIKV non-structural protein 1 (nsP1)

Virology

Volumn 438, Issue 1, 2013, Pages 37-49

  Jones, Philip H ^a   Maric, Martina ^a,b   Madison, Marisa N ^a   Maury, Wendy ^a   Roller, Richard J ^a   Okeoma, Chioma M ^a  

^a UNIVERSITY OF IOWA   (United States)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

BST 2; CHIKV; E1; Nonstructural protein; NsP1; SEM; Tetherin; VLP

Indexed keywords

BONE MARROW STROMAL CELL ANTIGEN 2; GLYCOPROTEIN E1; NONSTRUCTURAL PROTEIN 1; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CHIKUNGUNYA ALPHAVIRUS; CONTROLLED STUDY; CYTOKINE RESPONSIVE ELEMENT; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; VIRUS LIKE AGENT; VIRUS RELEASE;

ANTIGENS, CD; CELL LINE; CHIKUNGUNYA VIRUS; GPI-LINKED PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS RELEASE;

ALPHAVIRUS; CHIKUNGUNYA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84875253993     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.01.010     Document Type: Article

References (70)

1. Ahola T., Kaariainen L. Reaction in alphavirus mRNA capping: formation of a covalent complex of nonstructural protein nsP1 with 7-methyl-GMP. Proc. Natl. Acad. Sci. USA 1995, 92:507-511.
2. Ahola T., Kujala P., Tuittila M., Blom T., Laakkonen P., Hinkkanen A., Auvinen P. Effects of palmitoylation of replicase protein nsP1 on alphavirus infection. J. Virol. 2000, 74:6725-6733.
3. Akahata W., Yang Z.Y., Andersen H., Sun S., Holdaway H.A., Kong W.P., Lewis M.G., Higgs S., Rossmann M.G., Rao S., Nabel G.J. A virus-like particle vaccine for epidemic chikungunya virus protects nonhuman primates against infection. Nat. Med. 2010, 16:334-338.
4. Bartee E., McCormack A., Fruh K. Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLoS Pathog. 2006, 2:e107.
5. Bishop K.N., Holmes R.K., Sheehy A.M., Davidson N.O., Cho S.J., Malim M.H. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 2004, 14:1392-1396.
6. Cho B., Jeon B.Y., Kim J., Noh J., Kim J., Park M., Park S. Expression and evaluation of chikungunya virus E1 and E2 envelope proteins for serodiagnosis of chikungunya virus infection. Yonsei Med. J. 2008, 49:828-835.
7. Couderc T., Chretien F., Schilte C., Disson O., Brigitte M., Guivel-Benhassine F., Touret Y., Barau G., Cayet N., Schuffenecker I., Despres P., Arenzana-Seisdedos F., Michault A., Albert M.L., Lecuit M. A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog. 2008, 4:e29.
8. Dube M., Bego M.G., Paquay C., Cohen E.A. Modulation of HIV-1-host interaction: role of the Vpu accessory protein. Retrovirology 2010, 7:114.
9. Dube M., Roy B.B., Guiot-Guillain P., Binette J., Mercier J., Chiasson A., Cohen E.A. Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathog. 2010, 6:e1000856.
10. Fitzpatrick K., Skasko M., Deerinck T.J., Crum J., Ellisman M.H., Guatelli J. Direct restriction of virus release and incorporation of the interferon-induced protein BST-2 into HIV-1 particles. PLoS Pathog. 2010, 6:e1000701.
11. Fros J.J., Liu W.J., Prow N.A., Geertsema C., Ligtenberg M., Vanlandingham D.L., Schnettler E., Vlak J.M., Suhrbier A., Khromykh A.A., Pijlman G.P. Chikungunya virus nonstructural protein 2 inhibits type I/II interferon-stimulated JAK-STAT signaling. J. Virol. 2010, 84:10877-10887.
12. Gerardin P., Barau G., Michault A., Bintner M., Randrianaivo H., Choker G., Lenglet Y., Touret Y., Bouveret A., Grivard P., Le Roux K., Blanc S., Schuffenecker I., Couderc T., Arenzana-Seisdedos F., Lecuit M., Robillard P.Y. Multidisciplinary prospective study of mother-to-child chikungunya virus infections on the island of La reunion. PLoS Med. 2008, 5:e60.
13. Goffinet C., Schmidt S., Kern C., Oberbremer L., Keppler O.T. Endogenous CD317/Tetherin limits replication of HIV-1 and murine leukemia virus in rodent cells and is resistant to antagonists from primate viruses. J. Virol. 2010, 84:11374-11384.
14. Goila-Gaur R., Khan M.A., Miyagi E., Kao S., Strebel K. Targeting APOBEC3A to the viral nucleoprotein complex confers antiviral activity. Retrovirology 2007, 4:61.
15. Gomez de Cedron M., Ehsani N., Mikkola M.L., Garcia J.A., Kaariainen L. RNA helicase activity of Semliki Forest virus replicase protein NSP2. FEBS Lett. 1999, 448:19-22.
16. Hahn Y.S., Grakoui A., Rice C.M., Strauss E.G., Strauss J.H. Mapping of RNA-temperature-sensitive mutants of Sindbis virus: complementation group F mutants have lesions in nsP4. J. Virol. 1989, 63:1194-1202.
17. Hahn Y.S., Strauss E.G., Strauss J.H. Mapping of RNA-temperature-sensitive mutants of Sindbis virus: assignment of complementation groups A, B, and G to nonstructural proteins. J. Virol. 1989, 63:3142-3150.
18. Hammonds J., Wang J.J., Yi H., Spearman P. Immunoelectron microscopic evidence for Tetherin/BST2 as the physical bridge between HIV-1 virions and the plasma membrane. PLoS Pathog. 2010, 6:e1000749.
19. Hardy W.R., Strauss J.H. Processing the nonstructural polyproteins of sindbis virus: nonstructural proteinase is in the C-terminal half of nsP2 and functions both in cis and in trans. J. Virol. 1989, 63:4653-4664.
20. Hauser H., Lopez L.A., Yang S.J., Oldenburg J.E., Exline C.M., Guatelli J.C., Cannon P.M. HIV-1 Vpu and HIV-2 Env counteract BST-2/tetherin by sequestration in a perinuclear compartment. Retrovirology 2010, 7:51.
21. Her Z., Malleret B., Chan M., Ong E.K., Wong S.C., Kwek D.J., Tolou H., Lin R.T., Tambyah P.A., Renia L., Ng L.F. Active infection of human blood monocytes by Chikungunya virus triggers an innate immune response. J. Immunol. (Baltimore, Md. : 1950) 2010, 184:5903-5913.
22. Jolly C., Booth N.J., Neil S.J. Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells. J. Virol. 2010, 84:12185-12199.
23. Jones P.H., Mehta H.V., Maric M., Roller R.J., Okeoma C.M. Bone marrow stromal cell antigen 2 (BST-2) restricts mouse mammary tumor virus (MMTV) replication in vivo. Retrovirology 2012, 9:10.
24. Jones P.H., Mehta H.V., Okeoma C.M. A novel role for APOBEC3: susceptibility to sexual transmission of murine acquired immunodeficiency virus (mAIDS) is aggravated in APOBEC3 deficient mice. Retrovirology 2012, 9:50.
25. Kaletsky R.L., Francica J.R., Agrawal-Gamse C., Bates P. Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc. Natl. Acad. Sci. USA 2009, 106:2886-2891.
26. Kiiver K., Tagen I., Zusinaite E., Tamberg N., Fazakerley J.K., Merits A. Properties of non-structural protein 1 of Semliki Forest virus and its interference with virus replication. J. Gen. Virol. 2008, 89:1457-1466.
27. King P., Goodbourn S. The beta-interferon promoter responds to priming through multiple independent regulatory elements. J. Biol. Chem. 1994, 269:30609-30615.
28. Laakkonen P., Ahola T., Kaariainen L. The effects of palmitoylation on membrane association of Semliki forest virus RNA capping enzyme. J. Biol. Chem. 1996, 271:28567-28571.
29. Laakkonen P., Auvinen P., Kujala P., Kaariainen L. Alphavirus replicase protein NSP1 induces filopodia and rearrangement of actin filaments. J. Virol. 1998, 72:10265-10269.
30. Lahariya C., Pradhan S.K. Emergence of chikungunya virus in Indian subcontinent after 32 years: a review. J. Vector Borne Dis. 2006, 43:151-160.
31. Lam S., Chen K.C., Ng M.M., Chu J.J. Expression of Plasmid-based shRNA against the E1 and nsP1 genes effectively silenced chikungunya virus replication. PLoS One 2012, 7:e46396.
32. Le Tortorec A., Willey S., Neil S.J. Antiviral inhibition of enveloped virus release by tetherin/BST-2: action and counteraction. Viruses 2011, 3:520-540.
33. Leung J.Y., Ng M.M., Chu J.J. Replication of alphaviruses: a review on the entry process of alphaviruses into cells. Adv. Virol. 2011, 2011:249640.
34. Lopez L.A., Yang S.J., Hauser H., Exline C.M., Haworth K.G., Oldenburg J., Cannon P.M. Ebola virus glycoprotein counteracts BST-2/Tetherin restriction in a sequence-independent manner that does not require tetherin surface removal. J. Virol. 2010, 84:7243-7255.
35. Low A., Okeoma C.M., Lovsin N., de las Heras M., Taylor T.H., Peterlin B.M., Ross S.R., Fan H. Enhanced replication and pathogenesis of Moloney murine leukemia virus in mice defective in the murine APOBEC3 gene. Virology 2009, 385:455-463.
36. Lumsden W.H. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. II. General description and epidemiology. Trans. R. Soc. Trop. Med. Hyg. 1955, 49:33-57.
37. Malet H., Coutard B., Jamal S., Dutartre H., Papageorgiou N., Neuvonen M., Ahola T., Forrester N., Gould E.A., Lafitte D., Ferron F., Lescar J., Gorbalenya A.E., de Lamballerie X., Canard B. The crystal structures of chikungunya and Venezuelan equine encephalitis virus nsP3 macro domains define a conserved adenosine binding pocket. J. Virol. 2009, 83:6534-6545.
38. Mangeat B., Cavagliotti L., Lehmann M., Gers-Huber G., Kaur I., Thomas Y., Kaiser L., Piguet V. Influenza virus partially counteracts restriction imposed by Tetherin/BST-2. J. Biol. Chem. 2012, 287:22015-22029.
39. Mangeat B., Gers-Huber G., Lehmann M., Zufferey M., Luban J., Piguet V. HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog. 2009, 5:e1000574.
40. Mehta H.V., Jones P.H., Weiss J.P., Okeoma C.M. IFN-alpha and lipopolysaccharide upregulate APOBEC3 mRNA through different signaling pathways. J. Immunol. (Baltimore, Md. : 1950) 2012, 189:4088-4103.
41. Mi S., Durbin R., Huang H.V., Rice C.M., Stollar V. Association of the Sindbis virus RNA methyltransferase activity with the nonstructural protein nsP1. Virology 1989, 170:385-391.
42. Morrison T.E., Oko L., Montgomery S.A., Whitmore A.C., Lotstein A.R., Gunn B.M., Elmore S.A., Heise M.T. A mouse model of chikungunya virus-induced musculoskeletal inflammatory disease: evidence of arthritis, tenosynovitis, myositis, and persistence. Am. J. Pathol. 2011, 178:32-40.
43. Neil S., Bieniasz P. Human immunodeficiency virus, restriction factors, and interferon. J. Interferon Cytokine Res. 2009, 29:569-580.
44. Neil S.J., Zang T., Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
45. Okeoma C.M., Huegel A.L., Lingappa J., Feldman M.D., Ross S.R. APOBEC3 proteins expressed in mammary epithelial cells are packaged into retroviruses and can restrict transmission of milk-borne virions. Cell Host Microbe 2010, 8:534-543.
46. Okeoma C.M., Lovsin N., Peterlin B.M., Ross S.R. APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 2007, 445:927-930.
47. Okeoma C.M., Low A., Bailis W., Fan H.Y., Peterlin B.M., Ross S.R. Induction of APOBEC3 in vivo causes increased restriction of retrovirus infection. J. Virol. 2009, 83:3486-3495.
48. Okeoma C.M., Petersen J., Ross S.R. Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection. J. Virol. 2009, 83:3029-3038.
49. Okeoma C.M., Shen M., Ross S.R. A novel block to mouse mammary tumor virus infection of lymphocytes in B10.BR mice. J. Virol. 2008, 82:1314-1322.
50. Park E., Griffin D.E. The nsP3 macro domain is important for Sindbis virus replication in neurons and neurovirulence in mice. Virology 2009, 388:305-314.
51. Pease L.F., Lipin D.I., Tsai D.H., Zachariah M.R., Lua L.H., Tarlov M.J., Middelberg A.P. Quantitative characterization of virus-like particles by asymmetrical flow field flow fractionation, electrospray differential mobility analysis, and transmission electron microscopy. Biotechnol. Bioeng. 2009, 102:845-855.
52. Pellet J., Tafforeau L., Lucas-Hourani M., Navratil V., Meyniel L., Achaz G., Guironnet-Paquet A., Aublin-Gex A., Caignard G., Cassonnet P., Chaboud A., Chantier T., Deloire A., Demeret C., Le Breton M., Neveu G., Jacotot L., Vaglio P., Delmotte S., Gautier C., Combet C., Deleage G., Favre M., Tangy F., Jacob Y., Andre P., Lotteau V., Rabourdin-Combe C., Vidalain P.O. ViralORFeome: an integrated database to generate a versatile collection of viral ORFs. Nucleic Acids Res. 2010, 38:D371-D378.
53. Peranen J., Laakkonen P., Hyvonen M., Kaariainen L. The alphavirus replicase protein nsP1 is membrane-associated and has affinity to endocytic organelles. Virology 1995, 208:610-620.
54. Robinson M.C. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. I. Clinical features. Trans. R. Soc. Trop. Med. Hyg. 1955, 49:28-32.
55. Rollason R., Korolchuk V., Hamilton C., Jepson M., Banting G. A CD317/tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J. Cell Biol. 2009, 184:721-736.
56. Ruiz A., Lau D., Mitchell R.S., Hill M.S., Schmitt K., Guatelli J.C., Stephens E.B. BST-2 mediated restriction of simian-human immunodeficiency virus. Virology 2010, 406:312-321.
57. Salonen A., Vasiljeva L., Merits A., Magden J., Jokitalo E., Kaariainen L. Properly folded nonstructural polyprotein directs the semliki forest virus replication complex to the endosomal compartment. J. Virol. 2003, 77:1691-1702.
58. Schilte C., Couderc T., Chretien F., Sourisseau M., Gangneux N., Guivel-Benhassine F., Kraxner A., Tschopp J., Higgs S., Michault A., Arenzana-Seisdedos F., Colonna M., Peduto L., Schwartz O., Lecuit M., Albert M.L. Type I IFN controls chikungunya virus via its action on nonhematopoietic cells. J. Exp. Med. 2010, 207:429-442.
59. Schuffenecker I., Iteman I., Michault A., Murri S., Frangeul L., Vaney M.C., Lavenir R., Pardigon N., Reynes J.M., Pettinelli F., Biscornet L., Diancourt L., Michel S., Duquerroy S., Guigon G., Frenkiel M.P., Brehin A.C., Cubito N., Despres P., Kunst F., Rey F.A., Zeller H., Brisse S. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 2006, 3:e263.
60. Shirako Y., Strauss E.G., Strauss J.H. Suppressor mutations that allow sindbis virus RNA polymerase to function with nonaromatic amino acids at the N-terminus: evidence for interaction between nsP1 and nsP4 in minus-strand RNA synthesis. Virology 2000, 276:148-160.
61. Shirako Y., Strauss J.H. Regulation of Sindbis virus RNA replication: uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand RNA synthesis. J. Virol. 1994, 68:1874-1885.
62. Solignat M., Gay B., Higgs S., Briant L., Devaux C. Replication cycle of chikungunya: a re-emerging arbovirus. Virology 2009, 393:183-197.
63. Suspene R., Guetard D., Henry M., Sommer P., Wain-Hobson S., Vartanian J.P. Extensive editing of both hepatitis B virus DNA strands by APOBEC3 cytidine deaminases in vitro and in vivo. Proc. Natl. Acad. Sci. USA 2005, 102:8321-8326.
64. Tuittila M., Hinkkanen A.E. Amino acid mutations in the replicase protein nsP3 of Semliki Forest virus cumulatively affect neurovirulence. J. Gen. Virol. 2003, 84:1525-1533.
65. Van Damme N., Goff D., Katsura C., Jorgenson R.L., Mitchell R., Johnson M.C., Stephens E.B., Guatelli J. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3:245-252.
66. Vasiljeva L., Merits A., Auvinen P., Kaariainen L. Identification of a novel function of the alphavirus capping apparatus. RNA 5'-triphosphatase activity of Nsp2. J. Biol. Chem. 2000, 275:17281-17287.
67. Voss J.E., Vaney M.C., Duquerroy S., Vonrhein C., Girard-Blanc C., Crublet E., Thompson A., Bricogne G., Rey F.A. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 2010, 468:709-712.
68. Werneke S.W., Schilte C., Rohatgi A., Monte K.J., Michault A., Arenzana-Seisdedos F., Vanlandingham D.L., Higgs S., Fontanet A., Albert M.L., Lenschow D.J. ISG15 is critical in the control of chikungunya virus infection independent of UbE1L mediated conjugation. PLoS Pathog. 2011, 7:e1002322.
69. Yu Q., Chen D., Konig R., Mariani R., Unutmaz D., Landau N.R. APOBEC3B and APOBEC3C are potent inhibitors of simian immunodeficiency virus replication. J. Biol. Chem. 2004, 279:53379-53386.
70. Zhang J., Liang C. BST-2 diminishes HIV-1 infectivity. J. Virol. 2010, 84:12336-12343.