Matrix and envelope coevolution revealed in a patient monitored since primary infection with human immunodeficiency virus type 1

Journal of Virology

Volumn 83, Issue 19, 2009, Pages 9875-9889

  Beaumont, Elodie ^a,b   Vendrame, Daniela ^c   Verrier, Bernard ^d   Roch, Emmanuelle ^a,b   Biron, François ^e   Barin, Françis ^a,b   Mammano, Fabrizio ^c   Brand, Denys ^a,b  

^a UNIVERSITÉ DE TOURS   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE LYON   (France)

^e CROIX ROUSSE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; LAMIVUDINE PLUS ZIDOVUDINE; MATRIX PROTEIN; NEVIRAPINE; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CELL TRANSFER; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; PATIENT MONITORING; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS INFECTIVITY; VIRUS MUTANT; VIRUS PARTICLE; VIRUS REPLICATION;

AMINO ACID SEQUENCE; CYTOPLASM; FLOW CYTOMETRY; GENE PRODUCTS, ENV; HELA CELLS; HIV-1; HUMANS; KINETICS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL LOAD; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 70349281466     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01213-09     Document Type: Article

References (64)

1. Akari, H., T. Fukumori, and A. Adachi. 2000. Cell-dependent requirement of human immunodeficiency virus type 1 gp41 cytoplasmic tail for Env incorporation into virions. J. Virol. 74:4891-4893. (Pubitemid 30237919)
2. Alfadhli, A., R. L. Barklis, and E. Barklis. 2009. HIV-1 matrix organizes as a hexamer of trimers on membranes containing phosphatidylinositol-(4,5)- bisphosphate. Virology 387:466-472.
3. + T cell response against HIV-1. PLoS Med. 3:e403.
4. Amara, A., A. Vidy, G. Boulla, K. Mollier, J. Garcia-Perez, J. Alcami, C. Blanpain, M. Parmentier, J. L. Virelizier, P. Charneau, and F. Arenzana-Seisdedos. 2003. G protein-dependent CCR5 signaling is not required for efficient infection of primary T lymphocytes and macrophages by R5 human immunodeficiency virus type 1 isolates. J. Virol. 77:2550-2558. (Pubitemid 36222779)
5. Ataman-Onal, Y., C. Coiffier, A. Giraud, A. Babic-Erceg, F. Biron, and B. Verrier. 1999. Comparison of complete env gene sequences from individuals with symptomatic primary HIV type 1 infection. AIDS Res. Hum. Retrovir. 15:1035-1039.
6. Bergeron, L., N. Sullivan, and J. Sodroski. 1992. Target cell-specific determinants of membrane fusion within the human immunodeficiency virus type 1 gp120 third variable region and gp41 amino terminus. J. Virol. 66:2389-2397.
7. Berlioz-Torrent, C., B. L. Shacklett, L. Erdtmann, L. Delamarre, I. Bouchaert, P. Sonigo, M. C. Dokhelar, and R. Benarous. 1999. Interactions of the cytoplasmic domains of human and simian retroviral transmembrane proteins with components of the clathrin adaptor complexes modulate intracellular and cell surface expression of envelope glycoproteins. J. Virol. 73:1350-1361. (Pubitemid 29036790)
8. Blot, G., K. Janvier, S. Le Panse, R. Benarous, and C. Berlioz-Torrent. 2003. 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. 77:6931-6945. (Pubitemid 36666886)
9. Boge, M., S. Wyss, J. S. Bonifacino, and M. Thali. 1998. A membrane-proximal tyrosine-based signal mediates internalization of the HIV-1 envelope glycoprotein via interaction with the AP-2 clathrin adaptor. J. Biol. Chem. 273:15773-15778.
10. Byland, R., P. J. Vance, J. A. Hoxie, and M. Marsh. 2007. A conserved dileucine motif mediates clathrin and AP-2-dependent endocytosis of the HIV-1 envelope protein. Mol. Biol. Cell 18:414-425.
11. Chen, S. S., S. F. Lee, and C. T. Wang. 2001. Cellular membrane-binding ability of the C-terminal cytoplasmic domain of human immunodeficiency virus type 1 envelope transmembrane protein gp41. J. Virol. 75:9925-9938.
12. Clavel, F., M. D. Hoggan, R. L. Willey, K. Strebel, M. A. Martin, and R. Repaske. 1989. Genetic recombination of human immunodeficiency virus. J. Virol. 63:1455-1459. (Pubitemid 19061393)
13. Cosson, P. 1996. Direct interaction between the envelope and matrix proteins of HIV-1. EMBO J. 15:5783-5788. (Pubitemid 26375499)
14. Dacheux, L., A. Moreau, Y. Ataman-Onal, F. Biron, B. Verrier, and F. Barin. 2004. Evolutionary dynamics of the glycan shield of the human immunodeficiency virus envelope during natural infection and implications for exposure of the 2G12 epitope. J. Virol. 78:12625-12637.
15. Deng, H., R. Liu, W. Ellmeier, S. Choe, D. Unutmaz, M. Burkhart, P. Di Marzio, S. Marmon, R. E. Sutton, C. M. Hill, C. B. Davis, S. C. Peiper, T. J. Schall, D. R. Littman, and N. R. Landau. 1996. Identification of a major coreceptor for primary isolates of HIV-1. Nature 381:661-666. (Pubitemid 26197679)
16. Dubay, J. W., S. J. Roberts, B. H. Hahn, and E. Hunter. 1992. Truncation of the human immunodeficiency virus type 1 transmembrane glycoprotein cytoplasmic domain blocks virus infectivity. J. Virol. 66:6616-6625.
17. Eisenberg, D., and M. Wesson. 1990. The most highly amphiphilic alpha-helices include two amino acid segments in human immunodeficiency virus glycoprotein 41. Biopolymers 29:171-177. (Pubitemid 20055813)
18. Feng, Y., C. C. Broder, P. E. Kennedy, and E. A. Berger. 1996. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877. (Pubitemid 26154590)
19. Freed, E. O., and M. A. Martin. 1996. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 70:341-351.
20. Freed, E. O., J. M. Orenstein, A. J. Buckler-White, and M. A. Martin. 1994. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol. 68:5311-5320.
21. Gabuzda, D. H., A. Lever, E. Terwilliger, and J. Sodroski. 1992. Effects of deletions in the cytoplasmic domain on biological functions of human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 66:3306-3315.
22. Gousset, K., S. D. Ablan, L. V. Coren, A. Ono, F. Soheilian, K. Nagashima, D. E. Ott, and E. O. Freed. 2008. Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLoS Pathog. 4:e1000015.
23. Grigorov, B., F. Arcanger, P. Roingeard, J. L. Darlix, and D. Muriaux. 2006. Assembly of infectious HIV-1 in human epithelial and T-lymphoblastic cell lines. J. Mol. Biol. 359:848-862.
24. Hermida-Matsumoto, L., and M. D. Resh. 2000. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J. Virol. 74:8670-8679. (Pubitemid 30666717)
25. Hill, C. P., D. Worthylake, D. P. Bancroft, A. M. Christensen, and W. I. Sundquist. 1996. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. USA 93:3099-3104.
26. Hourioux, C., D. Brand, P. Y. Sizaret, F. Lemiale, S. Lebigot, F. Barin, and P. Roingeard. 2000. Identification of the glycoprotein 41(TM) cytoplasmic tail domains of human immunodeficiency virus type 1 that interact with Pr55Gag particles. AIDS Res. Hum. Retrovir. 16:1141-1147.
27. Hunter, E., and R. Swanstrom. 1990. Retrovirus envelope glycoproteins. Curr. Top. Microbiol. Immunol. 157:187-253.
28. Jiang, J., and C. Aiken. 2007. Maturation-dependent human immunodeficiency virus type 1 particle fusion requires a carboxyl-terminal region of the gp41 cytoplasmic tail. J. Virol. 81:9999-10008. (Pubitemid 350067703)
29. Jones, P. L., T. Korte, and R. Blumenthal. 1998. Conformational changes in cell surface HIV-1 envelope glycoproteins are triggered by cooperation between cell surface CD4 and coreceptors. J. Biol. Chem. 273:404-409.
30. Jouve, M., N. Sol-Foulon, S. Watson, O. Schwartz, and P. Benaroch. 2007. HIV-1 buds and accumulates in "nonacidic" endosomes of macrophages. Cell Host Microbe 2:85-95.
31. Kalia, V., S. Sarkar, P. Gupta, and R. C. Montelaro. 2005. Antibody neutralization escape mediated by point mutations in the intracytoplasmic tail of human immunodeficiency virus type 1 gp41. J. Virol. 79:2097-2107. (Pubitemid 40204567)
32. Kalia, V., S. Sarkar, P. Gupta, and R. C. Montelaro. 2003. Rational site-directed mutations of the LLP-1 and LLP-2 lentivirus lytic peptide domains in the intracytoplasmic tail of human immunodeficiency virus type 1 gp41 indicate common functions in cell-cell fusion but distinct roles in virion envelope incorporation. J. Virol. 77:3634-3646. (Pubitemid 36297283)
33. Kliger, Y., and Y. Shai. 1997. A leucine zipper-like sequence from the cytoplasmic tail of the HIV-1 envelope glycoprotein binds and perturbs lipid bilayers. Biochemistry 36:5157-5169. (Pubitemid 27199732)
34. Lambele, M., B. Labrosse, E. Roch, A. Moreau, B. Verrier, F. Barin, P. Roingeard, F. Mammano, and D. Brand. 2007. Impact of natural polymorphism within the gp41 cytoplasmic tail of human immunodeficiency virus type 1 on the intracellular distribution of envelope glycoproteins and viral assembly. J. Virol. 81:125-140. (Pubitemid 44975153)
35. Lee, S. J., W. Hu, A. G. Fisher, D. J. Looney, V. F. Kao, H. Mitsuya, L. Ratner, and F. Wong-Staal. 1989. Role of the carboxy-terminal portion of the HIV-1 transmembrane protein in viral transmission and cytopathogenicity. AIDS Res. Hum. Retrovir. 5:441-449.
36. Leslie, A. J., K. J. Pfafferott, P. Chetty, R. Draenert, M. M. Addo, M. Feeney, Y. Tang, E. C. Holmes, T. Allen, J. G. Prado, M. Altfeld, C. Brander, C. Dixon, D. Ramduth, P. Jeena, S. A. Thomas, A. St John, T. A. Roach, B. Kupfer, G. Luzzi, A. Edwards, G. Taylor, H. Lyall, G. Tudor-Williams, V. Novelli, J. Martinez-Picado, P. Kiepiela, B. D. Walker, and P. J. Goulder. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10:282-289.
37. Lodge, R., J. P. Lalonde, G. Lemay, and E. A. Cohen. 1997. The membrane-proximal intracytoplasmic tyrosine residue of HIV-1 envelope glycoprotein is critical for basolateral targeting of viral budding in MDCK cells. EMBO J. 16:695-705. (Pubitemid 27089517)
38. Lopez-Verges, S., G. Camus, G. Blot, R. Beauvoir, R. Benarous, and C. Berlioz-Torrent. 2006. 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. USA 103:14947-14952.
39. Luciw, P. A., K. E. Shaw, B. L. Shacklett, and M. L. Marthas. 1998. Importance of the intracytoplasmic domain of the simian immunodeficiency virus (SIV) envelope glycoprotein for pathogenesis. Virology 252:9-16.
40. Mammano, F., E. Kondo, J. Sodroski, A. Bukovsky, and H. G. Gottlinger. 1995. Rescue of human immunodeficiency virus type 1 matrix protein mutants by envelope glycoproteins with short cytoplasmic domains. J. Virol. 69:3824-3830.
41. Marechal, V., F. Clavel, J. M. Heard, and O. Schwartz. 1998. Cytosolic Gag p24 as an index of productive entry of human immunodeficiency virus type 1. J. Virol. 72:2208-2212. (Pubitemid 28100778)
42. Martinez-Picado, J., J. G. Prado, E. E. Fry, K. Pfafferott, A. Leslie, S. Chetty, C. Thobakgale, I. Honeyborne, H. Crawford, P. Matthews, T. Pillay, C. Rousseau, J. I. Mullins, C. Brander, B. D. Walker, D. I. Stuart, P. Kiepiela, and P. Goulder. 2006. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 80:3617-3623.
43. Murakami, T., and E. O. Freed. 2000. Genetic evidence for an interaction between human immunodeficiency virus type 1 matrix and alpha-helix 2 of the gp41 cytoplasmic tail. J. Virol. 74:3548-3554.
44. Murakami, T., and E. O. Freed. 2000. The long cytoplasmic tail of gp41 is required in a cell type-dependent manner for HIV-1 envelope glycoprotein incorporation into virions. Proc. Natl. Acad. Sci. USA 97:343-348.
45. Newman, J. T., T. J. Sturgeon, P. Gupta, and R. C. Montelaro. 2007. Differential functional phenotypes of two primary HIV-1 strains resulting from homologous point mutations in the LLP domains of the envelope gp41 intracytoplasmic domain. Virology 367:102-116.
46. Nobile, C., C. Petit, A. Moris, K. Skrabal, J. P. Abastado, F. Mammano, and O. Schwartz. 2005. Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J. Virol. 79:5386-5399. (Pubitemid 40548207)
47. Ohno, H., R. C. Aguilar, M. C. Fournier, S. Hennecke, P. Cosson, and J. S. Bonifacino. 1997. Interaction of endocytic signals from the HIV-1 envelope glycoprotein complex with members of the adaptor medium chain family. Virology 238:305-315. (Pubitemid 28218148)
48. Owens, R. J., J. W. Dubay, E. Hunter, and R. W. Compans. 1991. Human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells. Proc. Natl. Acad. Sci. USA 88:3987-3991.
49. Perez-Bercoff, D., A. David, H. Sudry, F. Barre-Sinoussi, and G. Pancino. 2003. Fcgamma receptor-mediated suppression of human immunodeficiency virus type 1 replication in primary human macrophages. J. Virol. 77:4081-4094. (Pubitemid 36350948)
50. Piller, S. C., J. W. Dubay, C. A. Derdeyn, and E. Hunter. 2000. Mutational analysis of conserved domains within the cytoplasmic tail of gp41 from human immunodeficiency virus type 1: effects on glycoprotein incorporation and infectivity. J. Virol. 74:11717-11723.
51. Platt, E. J., K. Wehrly, S. E. Kuhmann, B. Chesebro, and D. Kabat. 1998. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J. Virol. 72:2855-2864. (Pubitemid 28175522)
52. Prabakaran, P., A. S. Dimitrov, T. R. Fouts, and D. S. Dimitrov. 2007. Structure and function of the HIV envelope glycoprotein as entry mediator, vaccine immunogen, and target for inhibitors. Adv. Pharmacol. 55:33-97.
53. Rudner, L., S. Nydegger, L. V. Coren, K. Nagashima, M. Thali, and D. E. Ott. 2005. Dynamic fluorescent imaging of human immunodeficiency virus type 1 gag in live cells by biarsenical labeling. J. Virol. 79:4055-4065. (Pubitemid 40392503)
54. Saha, K., H. Yan, J. A. Nelson, and B. Zerhouni-Layachi. 2005. Infection of human and non-human cells by a highly fusogenic primary CD4-independent HIV-1 isolate with a truncated envelope cytoplasmic tail. Virology 337:30-44. (Pubitemid 40725438)
55. Sattentau, Q. 2008. Avoiding the void: cell-to-cell spread of human viruses. Nat. Rev. Microbiol. 6:815-826.
56. Sourisseau, M., N. Sol-Foulon, F. Porrot, F. Blanchet, and O. Schwartz. 2007. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J. Virol. 81:1000-1012. (Pubitemid 46067924)
57. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
58. Wei, X., J. M. Decker, H. Liu, Z. Zhang, R. B. Arani, J. M. Kilby, M. S. Saag, X. Wu, G. M. Shaw, and J. C. Kappes. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46:1896-1905.
59. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888. (Pubitemid 28299385)
60. Wyss, S., C. Berlioz-Torrent, M. Boge, G. Blot, S. Honing, R. Benarous, and M. Thali. 2001. The highly conserved C-terminal dileucine motif in the cytosolic domain of the human immunodeficiency virus type 1 envelope glycoprotein is critical for its association with the AP-1 clathrin adaptor. J. Virol. 75:2982-2992. (Pubitemid 32185063)
61. Wyss, S., A. S. Dimitrov, F. Baribaud, T. G. Edwards, R. Blumenthal, and J. A. Hoxie. 2005. Regulation of human immunodeficiency virus type 1 envelope glycoprotein fusion by a membrane-interactive domain in the gp41 cytoplasmic tail. J. Virol. 79:12231-12241. (Pubitemid 41346084)
62. Yang, X., S. Kurteva, S. Lee, and J. Sodroski. 2005. Stoichiometry of antibody neutralization of human immunodeficiency virus type 1. J. Virol. 79:3500-3508. (Pubitemid 40327938)
63. Yu, X., X. Yuan, M. F. McLane, T. H. Lee, and M. Essex. 1993. Mutations in the cytoplasmic domain of human immunodeficiency virus type 1 transmembrane protein impair the incorporation of Env proteins into mature virions. J. Virol. 67:213-221. (Pubitemid 23002981)
64. + lymphocytes. J. Virol. 78:1243-1255.