Host and viral determinants for MxB restriction of HIV-1 infection

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Matreyek, Kenneth A ^a,c   Wang, Weifeng ^a   Serrao, Erik ^a   Singh, Kumar P ^b   Levin, Henry L ^b   Engelman, Alan ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

HIV 1; Innate immunity; Mx2; MxB; Restriction factor

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MYXOVIRUS RESISTANCE PROTEIN; MYXOVIRUS RESISTANCE PROTEIN B; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; MX2 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INNATE IMMUNITY; LONG TERMINAL REPEAT; NONHUMAN; NUCLEAR IMPORT; OLIGOMERIZATION; OSTEOSARCOMA CELL; PEPTIDE MAPPING; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS DNA CELL DNA INTERACTION; ACTIVE TRANSPORT; CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANTIVIRAL AGENTS; CELL LINE; HIV-1; HUMANS; MYXOVIRUS RESISTANCE PROTEINS; VIRUS INTEGRATION;

EID: 84934977725     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0090-z     Document Type: Article

References (65)

1. Sheehy AM, Gaddis NC, Choi JD, Malim MH: Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418:646-650.
2. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J: The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in old world monkeys. Nature 2004, 427:848-853.
3. Sayah DM, Sokolskaja E, Berthoux L, Luban J: Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 2004, 430:569-573.
4. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, Yatim A, Emiliani S, Schwartz O, Benkirane M: SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 2011, 474:654-657.
5. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J: Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011, 474:658-661.
6. Neil SJ, Zang T, Bieniasz PD: Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
7. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, 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.
8. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM: A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
9. Goujon C, Moncorge O, Bauby H, Doyle T, Ward CC, Schaller T, Hue S, Barclay WS, Schulz R, Malim MH: Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 2013, 502:559-562.
10. Liu Z, Pan Q, Ding S, Qian J, Xu F, Zhou J, Cen S, Guo F, Liang C: The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 2013, 14:398-410.
11. Kane M, Yadav SS, Bitzegeio J, Kutluay SB, Zang T, Wilson SJ, Schoggins JW, Rice CM, Yamashita M, Hatziioannou T, Bieniasz PD: MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 2013, 502:563-566.
12. Verhelst J, Hulpiau P, Saelens X: Mx proteins: antiviral gatekeepers that restrain the uninvited. Microbiol Mol Biol Rev 2013, 77:551-566.
13. Gao S, von der Malsburg A, Dick A, Faelber K, Schroder GF, Haller O, Kochs G, Daumke O: Structure of myxovirus resistance protein a reveals intra- and intermolecular domain interactions required for the antiviral function. Immunity 2011, 35:514-525.
14. Accola MA, Huang B, Al Masri A, McNiven MA: The antiviral dynamin family member, MxA, tubulates lipids and localizes to the smooth endoplasmic reticulum. J Biol Chem 2002, 277:21829-21835.
15. von der Malsburg A, Abutbul-Ionita I, Haller O, Kochs G, Danino D: Stalk domain of the dynamin-like MxA GTPase protein mediates membrane binding and liposome tubulation via the unstructured L4 loop. J Biol Chem 2011, 286:37858-37865.
16. Mitchell PS, Emerman M, Malik HS: An evolutionary perspective on the broad antiviral specificity of MxA. Curr Opin Microbiol 2013, 16:493-499.
17. King MC, Raposo G, Lemmon MA: Inhibition of nuclear import and cell-cycle progression by mutated forms of the dynamin-like GTPase MxB. Proc Natl Acad Sci U S A 2004, 101:8957-8962.
18. Melen K, Keskinen P, Ronni T, Sareneva T, Lounatmaa K, Julkunen I: 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 1996, 271:23478-23486.
19. Fassati A, Goff SP: Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J Virol 2001, 75:3626-3635.
20. McDonald D, Vodicka MA, Lucero G, Svitkina TM, Borisy GG, Emerman M, Hope TJ: Visualization of the intracellular behavior of HIV in living cells. J Cell Biol 2002, 159:441-452.
21. Craigie R, Bushman FD: HIV DNA integration. Cold Spring Harb Perspect Med 2012, 2:a006890.
22. Munir S, Thierry S, Subra F, Deprez E, Delelis O: Quantitative analysis of the time-course of viral DNA forms during the HIV-1 life cycle. Retrovirology 2013, 10:87.
23. Melen K, Julkunen I: Nuclear cotransport mechanism of cytoplasmic human MxB protein. J Biol Chem 1997, 272:32353-32359.
24. Yamashita M, Emerman M: Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J Virol 2004, 78:5670-5678.
25. Matreyek KA, Engelman A: The requirement for nucleoporin NUP153 during human immunodeficiency virus type 1 infection is determined by the viral capsid. J Virol 2011, 85:7818-7827.
26. Matreyek KA, Yucel SS, Li X, Engelman A: Nucleoporin NUP153 phenylalanine-glycine motifs engage a common binding pocket within the HIV-1 capsid protein to mediate lentiviral infectivity. PLoS Pathog 2013, 9:e1003693.
27. Lu R, Nakajima N, Hofmann W, Benkirane M, Teh-Jeang K, Sodroski J, Engelman A: Simian virus 40-based replication of catalytically inactive human immunodeficiency virus type 1 integrase mutants in nonpermissive T cells and monocyte-derived macrophages. J Virol 2004, 78:658-668.
28. Li X, Koh Y, Engelman A: Correlation of recombinant integrase activity and functional preintegration complex formation during acute infection by replication-defective integrase mutant human immunodeficiency virus. J Virol 2012, 86:3861-3879.
29. Buckman JS, Bosche WJ, Gorelick RJ: Human immunodeficiency virus type 1 nucleocapsid Zn2+ fingers are required for efficient reverse transcription, initial integration processes, and protection of newly synthesized viral DNA. J Virol 2003, 77:1469-1480.
30. Diamond TL, Roshal M, Jamburuthugoda VK, Reynolds HM, Merriam AR, Lee KY, Balakrishnan M, Bambara RA, Planelles V, Dewhurst S, Kim B: Macrophage tropism of HIV-1 depends on efficient cellular dNTP utilization by reverse transcriptase. J Biol Chem 2004, 279:51545-51553.
31. Butler SL, Hansen MS, Bushman FD: A quantitative assay for HIV DNA integration in vivo . Nat Med 2001, 7:631-634.
32. Brussel A, Sonigo P: Analysis of early human immunodeficiency virus type 1 DNA synthesis by use of a new sensitive assay for quantifying integrated provirus. J Virol 2003, 77:10119-10124.
33. Swanstrom R, DeLorbe WJ, Bishop JM, Varmus HE: Nucleotide sequence of cloned unintegrated avian sarcoma virus DNA: viral DNA contains direct and inverted repeats similar to those in transposable elements. Proc Natl Acad Sci U S A 1981, 78:124-128.
34. Li L, Olvera JM, Yoder KE, Mitchell RS, Butler SL, Lieber M, Martin SL, Bushman FD: Role of the non-homologous DNA end joining pathway in the early steps of retroviral infection. EMBO J 2001, 20:3272-3281.
35. Li Y, Kappes JC, Conway JA, Price RW, Shaw GM, Hahn BH: Molecular characterization of human immunodeficiency virus type 1 cloned directly from uncultured human brain tissue: identification of replication-competent and -defective viral genomes. J Virol 1991, 65:3973-3985.
36. Yan N, Cherepanov P, Daigle JE, Engelman A, Lieberman J: The SET complex acts as a barrier to autointegration of HIV-1. PLoS Pathog 2009, 5:e1000327.
37. De Iaco A, Santoni F, Vannier A, Guipponi M, Antonarakis S, Luban J: TNPO3 protects HIV-1 replication from CPSF6-mediated capsid stabilization in the host cell cytoplasm. Retrovirology 2013, 10:20.
38. Ansari-Lari MA, Donehower LA, Gibbs RA: Analysis of human immunodeficiency virus type 1 integrase mutants. Virology 1995, 211:332-335.
39. Engelman A, Englund G, Orenstein JM, Martin MA, Craigie R: Multiple effects of mutations in human immunodeficiency virus type 1 integrase on viral replication. J Virol 1995, 69:2729-2736.
40. Wiskerchen M, Muesing MA: Human immunodeficiency virus type 1 integrase: effects of mutations on viral ability to integrate, direct viral gene expression from unintegrated viral DNA templates, and sustain viral propagation in primary cells. J Virol 1995, 69:376-386.
41. Schröder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F: HIV-1 integration in the human genome favors active genes and local hotspots. Cell 2002, 110:521-529.
42. Koh Y, Wu X, Ferris AL, Matreyek KA, Smith SJ, Lee K, KewalRamani VN, Hughes SH, Engelman A: 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 2013, 87:648-658.
43. Ferris AL, Wu X, Hughes CM, Stewart C, Smith SJ, Milne TA, Wang GG, Shun M-C, Allis CD, Engelman A, Hughes SH: Lens epithelium-derived growth factor fusion proteins redirect HIV-1 DNA integration. Proc Natl Acad Sci U S A 2010, 107:3135-3140.
44. Sandelin A, Carninci P, Lenhard B, Ponjavic J, Hayashizaki Y, Hume DA: Mammalian RNA polymerase II core promoters: insights from genome-wide studies. Nat Rev Genet 2007, 8:424-436.
45. Ocwieja KE, Brady TL, Ronen K, Huegel A, Roth SL, Schaller T, James LC, Towers GJ, Young JA, Chanda SK, Konig R, Malani N, Berry CC, Bushman FD: HIV integration targeting: a pathway involving transportin-3 and the nuclear pore protein RanBP2. PLoS Pathog 2011, 7:e1001313.
46. Lewinski MK, Yamashita M, Emerman M, Ciuffi A, Marshall H, Crawford G, Collins F, Shinn P, Leipzig J, Hannenhalli S, Berry CC, Ecker JR, Bushman FD: Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog 2006, 2:e60.
47. Mitchell PS, Patzina C, Emerman M, Haller O, Malik HS, Kochs G: Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 2012, 12:598-604.
48. Gao S, von der Malsburg A, Paeschke S, Behlke J, Haller O, Kochs G, Daumke O: Structural basis of oligomerization in the stalk region of dynamin-like MxA. Nature 2010, 465:502-506.
49. Ingerman E, Perkins EM, Marino M, Mears JA, McCaffery JM, Hinshaw JE, Nunnari J: Dnm1 forms spirals that are structurally tailored to fit mitochondria. J Cell Biol 2005, 170:1021-1027.
50. Busnadiego I, Kane M, Rihn SJ, Preugschas HF, Hughes J, Blanco-Melo D, Strouvelle VP, Zang TM, Willett BJ, Boutell C, Bieniasz PD, Wilson SJ: Host and viral determinants of Mx2 antiretroviral activity. J Virol 2014, 88:7738-7752.
51. Langelier CR, Sandrin V, Eckert DM, Christensen DE, Chandrasekaran V, Alam SL, Aiken C, Olsen JC, Kar AK, Sodroski JG, Sundquist WI: Biochemical characterization of a recombinant TRIM5α protein that restricts human immunodeficiency virus type 1 replication. J Virol 2008, 82:11682-11694.
52. Li X, Yeung DF, Fiegen AM, Sodroski J: Determinants of the higher order association of the restriction factor TRIM5α and other tripartite motif (TRIM) proteins. J Biol Chem 2011, 286:27959-27970.
53. Fricke T, White TE, Schulte B, de Souza Aranha Vieira DA, Dharan A, Campbell EM, Brandariz-Nuñez A, Diaz-Griffero F: MxB binds to the HIV-1 core and prevents the uncoating process of HIV-1. Retrovirology 2014, 11:68.
54. Fribourgh JL, Nguyen HC, Matreyek KA, Alvarez FJD, Summers BJ, Dewdney TG, Aiken C, Zhang P, Engelman A, Xiong Y: Strucutral insight into HIV-1 restriction by MxB. Cell Host Microbe 2014, 16:. in press.
55. Goujon C, Moncorgé O, Bauby H, Doyle T, Barclay WS, Malim MH: Transfer of the amino-terminal nuclear envelope targeting domain of human MX2 converts MX1 into an HIV-1 resistance factor. J Virol 2014, 88:9017-9026.
56. Di Nunzio F, Fricke T, Miccio A, Valle-Casuso JC, Perez P, Souque P, Rizzi E, Severgnini M, Mavilio F, Charneau P, Diaz-Griffero F: Nup153 and Nup98 bind the HIV-1 core and contribute to the early steps of HIV-1 replication. Virology 2013, 440:8-18.
57. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, Hue S, Fletcher AJ, Lee K, KewalRamani VN, Noursadeghi M, Jenner RG, James LC, Bushman FD, Towers GJ: HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog 2011, 7:e1002439.
58. Di Primio C, Quercioli V, Allouch A, Gijsbers R, Christ F, Debyser Z, Arosio D, Cereseto A: Single-cell imaging of HIV-1 provirus (SCIP). Proc Natl Acad Sci U S A 2013, 110:5636-5641.
59. Chang LJ, Urlacher V, Iwakuma T, Cui Y, Zucali J: Efficacy and safety analyses of a recombinant human immunodeficiency virus type 1 derived vector system. Gene Ther 1999, 6:715-728.
60. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D: The human genome browser at UCSC. Genome Res 2002, 12:996-1006.
61. Kent WJ: BLAT-the BLAST-like alignment tool. Genome Res 2002, 12:656-664.
62. Quinlan AR, Hall IM: BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
63. Engelman A, Oztop I, Vandegraaff N, Raghavendra NK: Quantitative analysis of HIV-1 preintegration complexes. Methods 2009, 47:283-290.
64. Wang H, Jurado KA, Wu X, Shun M-C, Li X, Ferris AL, Smith SJ, Patel PA, Fuchs JR, Cherepanov P, Kvaratskhelia M, Hughes SH, Engelman A: HRP2 determines the efficiency and specificity of HIV-1 integration in LEDGF/p75 knockout cells but does not contribute to the antiviral activity of a potent LEDGF/p75-binding site integrase inhibitor. Nucleic Acids Res 2012, 40:11518-11530.
65. R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2011.