Transfer of the amino-terminal nuclear envelope targeting domain of human MX2 converts MX1 into an HIV-1 resistance factor

Journal of Virology

Volumn 88, Issue 16, 2014, Pages 9017-9026

  Goujon, Caroline ^a   Moncorgé, Olivier ^b   Bauby, Hélène ^a   Doyle, Tomas ^a   Barclay, Wendy S ^b   Malim, Michael H ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; DYNAMIN; GUANOSINE TRIPHOSPHATASE; MYXOVIRUS RESISTANCE 1 PROTEIN; MYXOVIRUS RESISTANCE 2 PROTEIN; NUCLEOPORIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANTIVIRAL ACTIVITY; ARTICLE; CELL NUCLEUS MEMBRANE; CHIMERA; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFLUENZA A; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RETROVIRUS INFECTION; REVERSE TRANSCRIPTION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; VIRUS ENVELOPE; VIRUS INHIBITION; VIRUS PARTICLE; VIRUS RESISTANCE;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; CELL LINE; CELL LINE, TUMOR; GTP PHOSPHOHYDROLASES; HEK293 CELLS; HELA CELLS; HIV-1; HUMANS; INTERFERONS; MOLECULAR SEQUENCE DATA; MYXOVIRUS RESISTANCE PROTEINS; NUCLEAR ENVELOPE; R FACTORS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84904861293     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01269-14     Document Type: Article

References (59)

1. Ivashkiv LB, Donlin LT. 2014. Regulation of type I interferon responses. Nat. Rev. Immunol. 14:36-49. http://dx.doi.org/10.1038/nri3581.
2. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47. http://dx.doi.org/10.1099/vir.0.83391-0.
3. Samuel CE. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809. http://dx.doi.org/10.1128/CMR.14.4.778-809.2001.
4. Schoggins JW. 2014. Interferon-stimulated genes: roles in viral pathogenesis. Curr. Opin. Virol. 6:40-46. http://dx.doi.org/10.1016/j.coviro.2014.03.006.
5. Ho DD, Hartshorn KL, Rota TR, Andrews CA, Kaplan JC, Schooley RT, Hirsch MS. 1985. Recombinant human interferon alfa-A suppresses HTLV-III replication in vitro. Lancet i:602-604.
6. Poli G, Orenstein JM, Kinter A, Folks TM, Fauci AS. 1989. Interferonalpha but not AZT suppresses HIV expression in chronically infected cell lines. Science 244:575-577. http://dx.doi.org/10.1126/science.2470148.
7. Gendelman HE, Baca LM, Turpin J, Kalter DC, Hansen B, Orenstein JM, Dieffenbach CW, Friedman RM, Meltzer MS. 1990. Regulation of HIV replication in infected monocytes by IFN-alpha. Mechanisms for viral restriction. J. Immunol. 145:2669-2676.
8. Meylan PR, Guatelli JC, Munis JR, Richman DD, Kornbluth RS. 1993. Mechanisms for the inhibition of HIV replication by interferons-alpha,-beta, and-gamma in primary human macrophages. Virology 193:138-148. http://dx.doi.org/10.1006/viro.1993.1110.
9. Goujon C, Malim MH. 2010. Characterization of the alpha interferoninduced postentry block to HIV-1 infection in primary human macrophages and T cells. J. Virol. 84:9254-9266. http://dx.doi.org/10.1128/JVI.00854-10.
10. Cheney KM, McKnight A. 2010. Interferon-alpha mediates restriction of human immunodeficiency virus type-1 replication in primary human macrophages at an early stage of replication. PLoS One 5:e13521. http://dx.doi.org/10.1371/journal.pone.0013521.
11. Fraietta JA, Mueller YM, Yang G, Boesteanu AC, Gracias DT, Do DH, Hope JL, Kathuria N, McGettigan SE, Lewis MG, Giavedoni LD, Jacobson JM, Katsikis PD. 2013. Type I interferon upregulates Bak and contributes to T cell loss during human immunodeficiency virus (HIV) infection. PLoS Pathog. 9:e1003658. http://dx.doi.org/10.1371/journal.ppat.1003658.
12. Goujon C, Moncorgé O, Bauby H, Doyle T, Ward CC, Schaller T, Hué S, Barclay WS, Schulz R, Malim MH. 2013. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502:559-562. http://dx.doi.org/10.1038/nature12542.
13. Kane M, Yadav SS, Bitzegeio J, Kutluay SB, Zang T, Wilson SJ, Schoggins JW, Rice CM, Yamashita M, Hatziioannou T, Bieniasz PD. 2013. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 502: 563-566. http://dx.doi.org/10.1038/nature12653.
14. Liu Z, Pan Q, Ding S, Qian J, Xu F, Zhou J, Cen S, Guo F, Liang C. 2013. The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 14:398-410. http://dx.doi.org/10.1016/j.chom.2013.08.015.
15. Braaten D, Aberham C, Franke EK, Yin L, Phares W, Luban J. 1996. Cyclosporine A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J. Virol. 70:5170-5176.
16. Koh Y, Wu X, Ferris AL, Matreyek KA, Smith SJ, Lee K, Kewal Ramani VN, Hughes SH, Engelman A. 2013. Differential effects of human immunodeficiency virus type 1 capsid and cellular factors nucleoporin 153 and LEDGF/p75 on the efficiency and specificity of viral DNA integration. J. Virol. 87:648-658. http://dx.doi.org/10.1128/JVI.01148-12.
17. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, Julias JG, Vandegraaff N, Baumann JG, Wang R, Yuen W, Takemura T, Shelton K, Taniuchi I, Li Y, Sodroski J, Littman DR, Coffin JM, Hughes SH, Unutmaz D, Engelman A, Kewal Ramani VN. 2010. Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 7:221-233. http://dx.doi.org/10.1016/j.chom.2010.02.007.
18. Matreyek KA, Yucel SS, Li X, Engelman A. 2013. Nucleoporin NUP153 phenylalanine-glycine motifs engage a common binding pocket within the HIV-1 capsid protein to mediate lentiviral infectivity. PLoS Pathog. 9:e1003693. http://dx.doi.org/10.1371/journal.ppat.1003693.
19. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, Hue S, Fletcher AJ, Lee K, Kewal Ramani VN, Noursadeghi M, Jenner RG, James LC, Bushman FD, Towers GJ. 2011. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog. 7:e1002439. http://dx.doi.org/10.1371/journal.ppat.1002439.
20. Shah VB, Shi J, Hout DR, Oztop I, Krishnan L, Ahn J, Shotwell MS, Engelman A, Aiken C. 2013. The host proteins transportin SR2/TNPO3 and cyclophilin A exert opposing effects on HIV-1 uncoating. J. Virol. 87:422-432. http://dx.doi.org/10.1128/JVI.07177-11.
21. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848-853. http://dx.doi.org/10.1038/nature02343.
22. Matreyek KA, Engelman A. 2013. Viral and cellular requirements for the nuclear entry of retroviral preintegration nucleoprotein complexes. Viruses 5:2483-2511. http://dx.doi.org/10.3390/v5102483.
23. Haller O, Kochs G. 2011. Human MxA protein: an interferon-induced dynamin-like GTPase with broad antiviral activity. J. Interferon Cytokine Res. 31:79-87. http://dx.doi.org/10.1089/jir.2010.0076.
24. Kim BH, Shenoy AR, Kumar P, Bradfield CJ, MacMicking JD. 2012. IFN-inducible GTPases in host cell defense. Cell Host Microbe 12:432-444. http://dx.doi.org/10.1016/j.chom.2012.09.007.
25. Frese M, Kochs G, Feldmann H, Hertkorn C, Haller O. 1996. Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein. J. Virol. 70:915-923.
26. Gordien E, Rosmorduc O, Peltekian C, Garreau F, Brechot C, Kremsdorf D. 2001. Inhibition of hepatitis B virus replication by the interferoninducible MxA protein. J. Virol. 75:2684-2691. http://dx.doi.org/10.1128/JVI.75.6.2684-2691.2001.
27. Kochs G, Janzen C, Hohenberg H, Haller O. 2002. Antivirally active MxA protein sequesters La Crosse virus nucleocapsid protein into perinuclear complexes. Proc. Natl. Acad. Sci. U. S. A. 99:3153-3158. http://dx.doi.org/10.1073/pnas.052430399.
28. Pavlovic J, Zürcher T, Haller O, Staeheli P. 1990. Resistance to influenza virus and vesicular stomatitis virus conferred by expression of human MxA protein. J. Virol. 64:3370-3375.
29. Gao S, von der Malsburg A, Dick A, Faelber K, Schroder GF, Haller O, Kochs G, Daumke O. 2011. Structure of myxovirus resistance protein a reveals intra-and intermolecular domain interactions required for the antiviral function. Immunity 35:514-525. http://dx.doi.org/10.1016/j.immuni.2011.07.012.
30. Pitossi F, Blank A, Schroder A, Schwarz A, Hussi P, Schwemmle M, Pavlovic J, Staeheli P. 1993. A functional GTP-binding motif is necessary for antiviral activity of Mx proteins. J. Virol. 67:6726-6732.
31. Ponten A, Sick C, Weeber M, Haller O, Kochs G. 1997. Dominantnegative mutants of human MxA protein: domains in the carboxyterminal moiety are important for oligomerization and antiviral activity. J. Virol. 71:2591-2599.
32. Kochs G, Haener M, Aebi U, Haller O. 2002. Self-assembly of human MxA GTPase into highly ordered dynamin-like oligomers. J. Biol. Chem. 277:14172-14176. http://dx.doi.org/10.1074/jbc.M200244200.
33. von der Malsburg A, Abutbul-Ionita I, Haller O, Kochs G, Danino D. 2011. Stalk domain of the dynamin-like MxA GTPase protein mediates membrane binding and liposome tubulation via the unstructured L4 loop. J. Biol. Chem. 286:37858-37865. http://dx.doi.org/10.1074/jbc.M111.249037.
34. Mänz B, Dornfeld D, Götz V, Zell R, Zimmerman P, Haller O, Kochs G, Schwemmle M. 2013. Pandemic influenza A viruses escape from restriction by human MxA through adaptive mutations in the nucleoprotein. PLoS Pathog. 9:e1003279. http://dx.doi.org/10.1371/journal.ppat.1003279.
35. Mitchell PS, Patzina C, Emerman M, Haller O, Malik HS, Kochs G. 2012. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12:598-604. http://dx.doi.org/10.1016/j.chom.2012.09.005.
36. Zimmermann P, Mänz B, Haller O, Schwemmle M, Kochs G. 2011. The viral nucleoprotein determines Mx sensitivity of influenza A viruses. J. Virol. 85:8133-8140. http://dx.doi.org/10.1128/JVI.00712-11.
37. Turan K, Mibayashi M, Sugiyama K, Saito S, Numajiri A, Nagata K. 2004. Nuclear MxA proteins form a complex with influenza virus NP and inhibit the transcription of the engineered influenza virus genome. Nucleic Acids Res. 32:643-652. http://dx.doi.org/10.1093/nar/gkh192.
38. Kochs G, Haller O. 1999. GTP-bound human MxA protein interacts with the nucleocapsids of Thogoto virus (Orthomyxoviridae). J. Biol. Chem. 274:4370-4376. http://dx.doi.org/10.1074/jbc.274.7.4370.
39. Patzina C, Haller O, Kochs G. 2014. Structural requirements for the antiviral activity of the human MxA protein against Thogoto and influenzaAvirus. J. Biol. Chem. 289:6020-6027. http://dx.doi.org/10.1074/jbc.M113.543892.
40. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267. http://dx.doi.org/10.1126/science.272.5259.263.
41. Saenz DT, Teo W, Olsen JC, Poeschla EM. 2005. Restriction of feline immunodeficiency virus by Ref1, Lv1, and primate TRIM5alpha proteins. J. Virol. 79:15175-15188. http://dx.doi.org/10.1128/JVI.79.24.15175-15188.2005.
42. O'Rourke JP, Newbound GC, Kohn DB, Olsen JC, Bunnell BA. 2002. Comparison of gene transfer efficiencies and gene expression levels achieved with equine infectious anemia virus-and human immunodeficiency virus type 1-derived lentivirus vectors. J. Virol. 76:1510-1515. http://dx.doi.org/10.1128/JVI.76.3.1510-1515.2002.
43. Jarrosson-Wuilleme L, Goujon C, Bernaud J, Rigal D, Darlix JL, Cimarelli A. 2006. Transduction of nondividing human macrophages with gammaretrovirus-derived vectors. J. Virol. 80:1152-1159. http://dx.doi.org/10.1128/JVI.80.3.1152-1159.2006.
44. Simon JH, Southerling TE, Peterson JC, Meyer BE, Malim MH. 1995. Complementation of vif-defective human immunodeficiency virus type 1 by primate, but not nonprimate, lentivirus vif genes. J. Virol. 69:4166-4172.
45. Cordeil S, Nguyen XN, Berger G, Durand S, Ainouze M, Cimarelli A. 2013. Evidence for a different susceptibility of primate lentiviruses to type I interferons. J. Virol. 87:2587-2596. http://dx.doi.org/10.1128/JVI.02553-12.
46. Mangeot PE, Dollet S, Girard M, Ciancia C, Joly S, Peschanski M, Lotteau V. 2011. Protein transfer into human cells by VSV-G-induced nanovesicles. Mol. Ther. 19:1656-1666. http://dx.doi.org/10.1038/mt.2011.138.
47. Cauldwell AV, Moncorge O, Barclay WS. 2013. Unstable polymerasenucleoprotein interaction is not responsible for avian influenza virus polymerase restriction in human cells. J. Virol. 87:1278-1284. http://dx.doi.org/10.1128/JVI.02597-12.
48. Melén K, Keskinen P, Ronni T, Sareneva T, Lounatmaa K, Julkunen I. 1996. Human MxB protein, an interferon-alpha-inducible GTPase, contains a nuclear targeting signal and is localized in the heterochromatin region beneath the nuclear envelope. J. Biol. Chem. 271:23478-23486. http://dx.doi.org/10.1074/jbc.271.38.23478.
49. Aebi M, Fah J, Hurt N, Samuel CE, Thomis D, Bazzigher L, Pavlovic J, Haller O, Staeheli P. 1989. cDNA structures and regulation of two interferon-induced human Mx proteins. Mol. Cell. Biol. 9:5062-5072.
50. King MC, Raposo G, Lemmon MA. 2004. Inhibition of nuclear import and cell-cycle progression by mutated forms of the dynamin-like GTPase MxB. Proc. Natl. Acad. Sci. U. S. A. 101:8957-8962. http://dx.doi.org/10.1073/pnas.0403167101.
51. Zürcher T, Pavlovic J, Staeheli P. 1992. Mechanism of human MxA protein action: variants with changed antiviral properties. EMBO J. 11: 1657-1661.
52. Dreiding P, Staeheli P, Haller O. 1985. Interferon-induced protein Mx accumulates in nuclei of mouse cells expressing resistance to influenza viruses. Virology 140:192-196. http://dx.doi.org/10.1016/0042-6822(85) 90460-X.
53. Engelhardt OG, Ullrich E, Kochs G, Haller O. 2001. Interferon-induced antiviral Mx1 GTPase is associated with components of the SUMO-1 system and promyelocytic leukemia protein nuclear bodies. Exp. Cell Res. 271:286-295. http://dx.doi.org/10.1006/excr.2001.5380.
54. Zürcher T, Pavlovic J, Staeheli P. 1992. Mouse Mx2 protein inhibits vesicular stomatitis virus but not influenza virus. Virology 187:796-800. http://dx.doi.org/10.1016/0042-6822(92)90481-4.
55. Laguette N, Bregnard C, Hue P, Basbous J, Yatim A, Larroque M, Kirchhoff F, Constantinou A, Sobhian B, Benkirane M. 2014. Premature activation of the SLX4 complex by Vpr promotes G2/M arrest and escape from innate immune sensing. Cell 156:134-145. http://dx.doi.org/10.1016/j.cell.2013.12.011.
56. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J. 2010. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 11:1005-1013. http://dx.doi.org/10.1038/ni.1941.
57. Xiao H, Killip MJ, Staeheli P, Randall RE, Jackson D. 2013. The human interferon-induced MxA protein inhibits early stages of influenza A virus infection by retaining the incoming viral genome in the cytoplasm. J. Virol. 87:13053-13058. http://dx.doi.org/10.1128/JVI.02220-13.
58. Kochs G, Haller O. 1999. Interferon-induced human MxA GTPase blocks nuclear import of Thogoto virus nucleocapsids. Proc. Natl. Acad. Sci. U. S. A. 96:2082-2086. http://dx.doi.org/10.1073/pnas.96.5.2082.
59. Matzinger SR, Carroll TD, Dutra JC, Ma ZM, Miller CJ. 2013. Myxovirus resistance gene A (MxA) expression suppresses influenza A virus replication in alpha interferon-treated primate cells. J. Virol. 87:1150-1158. http://dx.doi.org/10.1128/JVI.02271-12.