Mutation of critical serine residues in HIV-1 matrix result in an envelope incorporation defect which can be rescued by truncation of the gp41 cytoplasmic tail

Virology

Volumn 384, Issue 1, 2009, Pages 233-241

  Bhatia, Ajay K ^a   Kaushik, Rajnish ^a   Campbell, Nancy A ^a   Pontow, Suzanne E ^a   Ratner, Lee ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Envelope incorporation; Fusion; HIV 1 Matrix; Raft association

Indexed keywords

ALANINE; GLYCOPROTEIN GP 41; SERINE;

AMINO ACID SUBSTITUTION; ARTICLE; CELL BUDDING; CELL MEMBRANE; CYTOPLASM; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SUCROSE DENSITY GRADIENT CENTRIFUGATION; TRANSMISSION ELECTRON MICROSCOPY; VIRUS ASSEMBLY; VIRUS MUTATION; VIRUS REPLICATION; WESTERN BLOTTING; WILD TYPE;

ALANINE; AMINO ACID SUBSTITUTION; CELL MEMBRANE; DETERGENTS; HIV ENVELOPE PROTEIN GP41; HIV-1; MODELS, MOLECULAR; MUTATION; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; SEQUENCE DELETION; SERINE; VIRAL ENVELOPE PROTEINS; VIRAL MATRIX PROTEINS; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 58549092971     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.10.047     Document Type: Article

References (75)

1. Alfadhli A., Huseby D., Kapit E., Colman D., and Barklis E. The HIV-1 matrix protein assembles on the membranes as a hexamer. J. Virol. 81 (2007) 1472-1478
2. Batonick M., Favre M., Boge M., Spearman P., Honing S., and Thali M. Interaction of HIV-1 Gag with the clathrin-associated adaptor AP-2. Virology 342 (2005) 190-200
3. Beer C., Pedersen L., and Wirth M. Amphotropic murine leukaemia virus envelope protein is associated with cholesterol-rich microdomains. Virol. J. 2 (2005) 36-44
4. Bhattacharya J., Peters P.J., and Clapham P.R. Human immunodeficiency virus type 1 envelope glycoproteins that lack cytoplasmic domain cysteines: impact on association with membrane lipid rafts and incorporation onto budding virus particles. J. Virol. 78 (2004) 5500-5506
5. Bhattacharya J., Repik A., and Clapham P.R. Gag regulates association of human immunodeficiency virus type 1 envelope with detergent-resistant membranes. J. Virol. 80 (2006) 5292-5300
6. Blot G., Janvier K., Le Panse S., Benarous R., and Berlioz-Torrent C. Targeting of the human immunodeficiency virus type 1 envelope to the trans-Golgi network through binding to TIP47 is required for Env incorporation into virions and infectivity. J. Virol. 77 (2003) 6931-6945
7. Brody B.A., Rhee S.S., and Hunter E. Post-assembly cleavage of a retroviral glycoprotein cytoplasmic domain removes a necessary incorporation signal and activates fusion activity. J. Virol. 68 (1994) 4620-4627
8. Bryant M., and Ratner L. Myristoylation-dependent replication and assembly of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 523-527
9. Bukrinsky M.I., Haggerty S., Dempsey M.P., Sharova N., Adzhubei A., Spitz L., Lewis P., Goldfarb D., Emerman M., and Stevenson M. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature 365 (1993) 666-669
10. Byland R., Vance P.J., Hoxie J.A., and Marsh M. A conserved dileucine motif mediates clathrin and AP-2-dependent endocytosis of the HIV-1 envelope protein. Mol. Biol. Cell 18 (2007) 414-425
11. Cathomen T., Naim H.Y., and Cattaneo R. Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J. Virol. 72 (1998) 1224-1234
12. Cosson P. Direct interaction between the envelope and matrix proteins of HIV-1. EMBO J. 15 (1996) 5783-5788
13. Davis M.R., Jiang J., Zhou J., Freed E.O., and Aiken C. A mutation in the human immunodeficiency virus type 1 gag protein destabilizes the interaction of the envelope protein subunits gp120 and gp41. J. Virol. 80 (2006) 2405-2417
14. Dong X., Li H., Derdowski A., Ding L., Burnett A., Chen X., Peters T.R., Dermody T.S., Woodruff E., Wang J.-J., and Spearman P. AP-3 directs the intracellular trafficking of HIV-1 gag and plays a key role in particle assembly. Cell 120 (2005) 663-674
15. Dorfman T., Mammano F., Haseltine W.A., and Gottlinger H.G. Role of the matrix protein in the virion association of the human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 68 (1994) 1689-1696
16. Dubay J.W., Roberts S.J., Hahn B.H., and Hunter E. Truncation of the human immunodeficiency virus type 1 transmembrane glycoprotein cytoplasmic domain blocks virus infectivity. J. Virol. 66 (1992) 6616-6625
17. Dupont S., Sharova N., DeHoratius C., Virbasius C.M., Zhu X., Bukrinskaya A.G., Stevenson M., and Green M.R. A novel nuclear export activity in HIV-1 matrix protein required for viral replication. Nature 402 (1999) 681-685
18. Egan M., Carruth L., Rowell J., Yu X., and Siliciano R. Human immunodeficiency virus type 1 envelope protein endocytosis mediated by a highly conserved intrinsic internalization signal in the cytoplasmic domain of gp41 is suppressed in the presence of the Pr55gag precursor protein. J. Virol. 70 (1996) 6547-6556
19. Feng X., Vander Heyden N., and Ratner L. Alpha interferon inhibits human T-cell leukemia virus type 1 assembly by preventing Gag interaction with rafts. J. Virol. 77 (2003) 13389-13395
20. Forshey B.M., von Schwedler U., Sundquist W.I., and Aiken C. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76 (2002) 5667-5677
21. Freed E.O. HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 251 (1998) 1-15
22. Freed E.O., and Martin M.A. Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific single amino acid substitutions in the human immunodeficiency virus type 1 matrix. J. Virol. 69 (1995) 1984-1989
23. Freed E., and Martin M. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 70 (1996) 341-351
24. Gallay P., Swingler S., Song J., Bushman F., and Trono D. HIV nuclear import is governed by the phosphotyrosine-mediated binding of matrix to the core domain of integrase. Cell 83 (1995) 569-576
25. Guern M., and Levy J. Human immunodeficiency virus (HIV) type 1 can superinfect HIV-2-infected cells: pseudotyped virions produced with expanded cellular host range. Proc. Natl. Acad. Sci. 89 (1992) 363-367
26. Haffar O.K., Popov S., Dubrovsky L., Agostini I., Tang H., Pushkarsky T., Nadler S.G., and Bukrinsky M. Two nuclear localization signals in the HIV-1 matrix protein regulate nuclear import of the HIV-1 pre-integration complex. J. Mol. Biol. 299 (2000) 359-368
27. Halwani R., Khorchid A., Cen S., and Kleiman L. Rapid localization of Gag/GagPol complexes to detergent-resistant membrane during the assembly of human immunodeficiency virus type 1. J. Virol. 77 (2003) 3973-3984
28. Henderson G., Murray J., and Yeo R.P. Sorting of the respiratory syncytial virus matrix protein into detergent-resistant structures is dependent on cell-surface expression of the glycoproteins. Virology 300 (2002) 244-254
29. Hill C.P., Worthylake D., Bancroft D.P., Christensen A.M., and Sundquist W.I. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. 93 (1996) 3099-3104
30. Johnston P.B., Dubay J.W., and Hunter E. Truncations of the simian immunodeficiency virus transmembrane protein confer expanded virus host range by removing a block to virus entry into cells. J. Virol. 67 (1993) 3077-3086
31. Kaushik R., and Ratner L. Role of human immunodeficiency virus type 1 matrix phosphorylation in an early postentry step of virus replication. J. Virol. 78 (2004) 2319-2326
32. Kim F.J., Manel N., Boublik Y., Battini J.L., and Sitbon M. Human T-cell leukemia virus type 1 envelope-mediated syncytium formation can be activated in resistant mammalian cell lines by a carboxy-terminal truncation of the envelope cytoplasmic domain. J. Virol. 77 (2003) 963-969
33. Landau N.R., Page K.A., and Littman D.R. Pseudotyping with human T-cell leukemia virus type I broadens the human immunodeficiency virus host range. J. Virol. 65 (1991) 162-169
34. Leitner T., Foley B., Hahn B., Marx P., McCutchan F., Mellors J., Wolinsky S., and Korber B. HIV Sequence Compendium 2006/2007 (2007), Los Alamos National Laboratory, Los Alamos, New Mexico
35. Lopez-Verges S., Camus G., Blot G., Beauvoir R., Benarous R., and Berlioz-Torrent C. Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions. Proc. Natl. Acad. Sci. U. S. A. 40 (2006) 14947-14952
36. Mammano F., Kondo E., Sodroski J., Bukovsky A., and Gottlinger H. Rescue of human immunodeficiency virus type 1 matrix protein mutants by envelope glycoproteins with short cytoplasmic domains. J. Virol. 69 6 (1995) 3824-3830
37. Massiah M.A., Worthylake D., Christensen A.M., Sundquist W.I., Hill C.P., and Summers M.F. Comparison of the NMR and X-ray structures of the HIV-1 matrix protein: evidence for conformational changes during viral assembly. Protein Sci. 5 (1996) 2391-2398
38. McClure M.O., Sommerfelt M.A., Marsh M., and Weiss R.A. The pH independence of mammalian retrovirus infection. J. Gen. Virol. 71 (1990) 767-773
39. Mebatsion T., Weiland F., and Conzelmann K.-K. Matrix protein of rabies virus is responsible for the assembly and budding of bullet-shaped particles and interacts with the transmembrane spike glycoprotein G. J. Virol. 73 (1999) 242-250
40. Murakami T., and Freed E.O. Genetic evidence for an interaction between human immunodeficiency virus type 1 matrix and alpha-helix 2 of the gp41 cytoplasmic tail. J. Virol. 74 (2000) 3548-3554
41. Murakami T., and Freed E.O. The long cytoplasmic tail of gp41 is required in a cell type-dependent manner of rHIV-1 envelope glycoprotein incorporation into virions. Proc. Natl. Acad. Sci. 97 (2000) 343-348
42. Murakami T., Ablan S., Freed E.O., and Tanaka Y. Regulation of human immunodeficiency virus type 1 Env-mediated membrane fusion by viral protease activity. J. Virol. 78 (2004) 1026-1031
43. Murray J.L., Mavrakis M., McDonald N.J., Yilla M., Sheng J., Bellini W.J., Zhao L., Le Doux J.M., Shaw M.W., Luo C.-C., Lippincott-Schwartz J., Sanchez A., Rubin D.H., and Hodge T.W. Rab9 GTPase is required for replication of human immunodeficiency virus type 1, filoviruses, and measles virus. J. Virol. 79 (2005) 11742-11751
44. Nayak D.P., Hui E.K.-W., and Barman S. Assembly and budding of influenza virus. Virus Res. 12 (2004) 147-165
45. Noble B., Abada P., Nunez-Iglesias J., and Cannon P.M. Recruitment of the adaptor protein 2 complex by the human immunodeficiency virus type 2 envelope protein is necessary for high levels of virus release. J. Virol. 80 (2006) 2924-2932
46. Ohno H., Aguilar R.C., Fournier M.-C., Hennecke S., Cosson P., and Bonifacino J.S. Interaction of endocytic signals from the HIV-1 envelope glycoprotein complex with members of the adaptor medium chain family. Virology 238 (1997) 305-315
47. Ono A., and Freed E.O. Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J. Virol. 73 (1999) 4136-4144
48. Ono A., and Freed E.O. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 13925-13930
49. Ono A., and Freed E.O. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J. Virol. 78 (2004) 1552-1563
50. Ono A., Waheed A.A., and Freed E.O. Depletion of cellular cholesterol inhibits membrane binding and higher-order multimerization of human immunodeficiency virus type 1 Gag. Virology 360 (2007) 27-35
51. Oomens A.G.P., Bevis K.P., and Wertz G.W. The cytoplasmic tail of the human respiratory syncytial virus F protein plays critical roles in cellular localization of the F protein and infectious progeny production. J. Virol. 80 (2006) 465-477
52. Owens R.J., Dubay J.W., Hunter E., and Compans R.W. Human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells. Proc. Natl. Acad. Sci. 88 (1991) 3987-3991
53. Pickl W.F., Pimental-Muinos F.X., and Seed B. Lipid rafts and pseudotyping. J. Virol. 75 (2001) 7175-7183
54. Pirounaki M., Vander Heyden N.A., Arens M., and Ratner L. Rapid phenotypic drug susceptibility assay for HIV-1 with a CCR5 expressing indicator cell line. J. Virol. Methods 85 (2000) 151-162
55. Pontow S.E., Heyden N.V., Wei S., and Ratner L. Actin cytoskeletal reorganizations and coreceptor-mediated activation of Rac during human immunodeficiency virus-induced cell fusion. J. Virol. 78 (2004) 7138-7147
56. Rein A., Mirro J., Haynes J.G., Ernst S.M., and Nagashima K. Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J. Virol. 68 (1994) 1773-1781
57. Saad J.S., Miller J., Tai J., Kim A., Ghanam R.H., and Summers M.F. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11364-11369
58. Saad J.S., Kim A., Ghanam R.H., Dalton A.K., Vogt V.M., Wu Z., Lu W., and Summers M.F. Mutations that mimic phosphorylation of the HIV-1 matrix protein do not perturb the myristyl switch. Protein Sci. 16 (2007) 1793-1797
59. Salzwedel K., Johnston P.B., Roberts S.J., Dubay J.W., and Hunter E. Expression and characterization of glycophospholipid-anchored human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 67 (1993) 5279-5288
60. Sauter M., Pelchen-Matthews A., Bron R., Marsh M., LaBranche C., Vance P., Romano J., Haggarty B., Hart T., Lee W., and Hoxie J. An internalization signal in the simian immunodeficiency virus transmembrane protein cytoplasmic domain modulates expression of envelope glycoproteins on the cell surface. J. Cell Biol. 132 (1996) 795-811
61. Scarlatta S., and Carter C. The role of HIV Gag domains in viral assembly. Biochim. Biophys. Acta 1614 (2003) 62-72
62. Shkriabai N., Datta S.A.K., Zhao Z., Hess S., Rein A., and Kvaratskhelia M. Interactions of HIV-1 Gag with assembly cofactors. Biochemistry 45 (2006) 4077-4083
63. Spearman P., Wang J.J., Vander Heyden N., and Ratner L. Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J. Virol. 68 (1994) 3232-3242
64. Spearman P., Horton R., Ratner L., and Kuli-Zade I. Membrane binding of HIV-1 matrix protein in vivo supports a conformation switch mechanism. J. Virol. 71 (1997) 6582-6592
65. Spector D.H., Wade E., Wright D.A., Koval V., Clark C., Jaquish D., and Spector S.A. Human immunodeficiency virus pseudotypes with expanded cellular and species tropism. J. Virol. 64 (1990) 2298-2308
66. Spies C.P., and Compans R.W. Effects of cytoplasmic domain length on cell surface expression and syncytium-forming capacity of the simian immunodeficiency virus envelope glycoprotein. Virology 203 (1994) 8-19
67. Tang C., Loeliger E., Luncsford P., Kinde I., Beckett D., and Summers M.F. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 517-522
68. Tang S., Murakami T., Cheng N., Steven A.C., Freed E.O., and Levin J.G. Human immunodeficiency virus type 1 N-terminal capsid mutants containing cores with abnormally high levels of capsid protein and virtually no reverse transcriptase. J. Virol. 77 (2003) 12592-12602
69. West J.T., Weldon S.K., Wyss S., Lin X., Yu Q., Thali M., and Hunter E. Mutation of the dominant endocytosis motif in human immunodeficiency virus type 1 gp41 can complement matrix mutations without increasing Env incorporation. J. Virol. 76 (2002) 3338-3349
70. Wills J.W., and Craven R.C. Form, function, and use of retroviral gag proteins. AIDS 5 (1991) 639-654
71. Wyma D.J., Kotov A., and Aiken C. Evidence for a stable interaction of gp41 with Pr55Gag in immature human immunodeficiency virus type 1 particles. J. Virol. 74 (2000) 9381-9387
72. Wyma D.J., Jiang J., Shi J., Zhou J., Lineberger J.E., Miller M.D., and Aiken C. Coupling of human immunodeficiency virus type 1 fusion to virion maturation: a novel role of the gp41 cytoplasmic tail. J. Virol. 78 (2004) 3429-3435
73. Yu X., Yuan X., Matsuda Z., Lee T.H., and Essex M. The matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions. J. Virol. 66 8 (1992) 4966-4971
74. Zeilfelder U., and Bosch V. Properties of wild-type, C-terminally truncated, and chimeric Maedi-Visna virus glycoprotein and putative pseudotyping of retroviral vector particles. J. Virol. 75 1 (2001) 548-555
75. Zhou W., and Resh M.D. Differential membrane binding of the human immunodeficiency virus type 1 matrix protein. J. Virol. 70 (1996) 8540-8548