A signature in HIV-1 envelope leader peptide associated with transition from acute to chronic infection impacts envelope processing and infectivity

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Asmal, Mohammed ^a   Hellmann, Ina ^a   Liu, Weimin ^b   Keele, Brandon F ^b   Perelson, Alan S ^c   Bhattacharya, Tanmoy ^c,d   Gnanakaran, S ^c   Daniels, Marcus ^c   Haynes, Barton F ^e   Korber, Bette T ^c,d   Hahn, Beatrice H ^b   Shaw, George M ^b   Letvin, Norman L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b University of Alabama at Birmingham   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d SANTA FE INSTITUTE   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; HISTIDINE; SIGNAL PEPTIDE; GAG PROTEIN; VIRUS ENVELOPE PROTEIN;

ACUTE DISEASE; AMINO ACID SUBSTITUTION; ARTICLE; CHRONIC DISEASE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENRICHMENT CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MATHEMATICAL MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN TARGETING; SEQUENCE ANALYSIS; STEADY STATE; UNINDEXED SEQUENCE; VIRION; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS TRANSMISSION; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CHEMISTRY; DISEASE COURSE; GENETIC POLYMORPHISM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LEUKEMIA CELL LINE; METABOLISM; MOLECULAR GENETICS; PATHOGENICITY; PATHOLOGY; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; STATISTICAL MODEL; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

ACUTE DISEASE; AMINO ACID SEQUENCE; CHRONIC DISEASE; DISEASE PROGRESSION; ENDOPLASMIC RETICULUM; GENE PRODUCTS, ENV; HIV CORE PROTEIN P24; HIV INFECTIONS; HIV-1; HUMANS; JURKAT CELLS; LIKELIHOOD FUNCTIONS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; VIRION;

EID: 80051832232     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023673     Document Type: Article

References (49)

1. Learn GH, Muthui D, Brodie SJ, Zhu T, Diem K, et al. (2002) Virus population homogenization following acute human immunodeficiency virus type 1 infection. J Virol 76: 11953-11959.
2. McNearney T, Hornickova Z, Markham R, Birdwell A, Arens M, et al. (1992) Relationship of human immunodeficiency virus type 1 sequence heterogeneity to stage of disease. Proc Natl Acad Sci U S A 89: 10247-10251.
3. Wolfs TF, Zwart G, Bakker M, Goudsmit J, (1992) HIV-1 genomic RNA diversification following sexual and parenteral virus transmission. Virology 189: 103-110.
4. Zhu T, Mo H, Wang N, Nam DS, Cao Y, et al. (1993) Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261: 1179-1181.
5. Frater AJ, Edwards CT, McCarthy N, Fox J, Brown H, et al. (2006) Passive sexual transmission of human immunodeficiency virus type 1 variants and adaptation in new hosts. J Virol 80: 7226-7234.
6. Wolinsky SM, Wike CM, Korber BT, Hutto C, Parks WP, et al. (1992) Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 255: 1134-1137.
7. Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, et al. (1999) Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virol 73: 10489-10502.
8. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7557.
9. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, et al. (2009) Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J Virol 83: 3556-3567.
10. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, et al. (2009) The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 206: 1253-1272.
11. Zhang LQ, MacKenzie P, Cleland A, Holmes EC, Brown AJ, et al. (1993) Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. J Virol 67: 3345-3356.
12. Edwards CT, Holmes EC, Wilson DJ, Viscidi RP, Abrams EJ, et al. (2006) Population genetic estimation of the loss of genetic diversity during horizontal transmission of HIV-1. BMC Evol Biol 6: 28.
13. Margolis L, Shattock R, (2006) Selective transmission of CCR5-utilizing HIV-1: the 'gatekeeper' problem resolved? Nat Rev Microbiol 4: 312-317.
14. Enose Y, Okada M, Sata T, Ma W, Igarashi T, et al. (1997) Restriction of viral population by intravaginal infection of simian immunodeficiency viruses in macaque monkeys. Arch Virol 142: 37-51.
15. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, et al. (2004) Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303: 2019-2022.
16. Bhattacharya T, Daniels M, Heckerman D, Foley B, Frahm N, et al. (2007) Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 315: 1583-1586.
17. Li Y, Luo L, Thomas DY, Kang CY, (2000) The HIV-1 Env protein signal sequence retards its cleavage and down-regulates the glycoprotein folding. Virology 272: 417-428.
18. Land A, Zonneveld D, Braakman I, (2003) Folding of HIV-1 envelope glycoprotein involves extensive isomerization of disulfide bonds and conformation-dependent leader peptide cleavage. FASEB J 17: 1058-1067.
19. Crise B, Rose JK, (1992) Human immunodeficiency virus type 1 glycoprotein precursor retains a CD4-p56lck complex in the endoplasmic reticulum. J Virol 66: 2296-2301.
20. Jabbar MA, Nayak DP, (1990) Intracellular interaction of human immunodeficiency virus type 1 (ARV-2) envelope glycoprotein gp160 with CD4 blocks the movement and maturation of CD4 to the plasma membrane. J Virol 64: 6297-6304.
21. Li Y, Luo L, Thomas DY, Kang CY, (1994) Control of expression, glycosylation, and secretion of HIV-1 gp120 by homologous and heterologous signal sequences. Virology 204: 266-278.
22. Pfeiffer T, Pisch T, Devitt G, Holtkotte D, Bosch V, (2006) Effects of signal peptide exchange on HIV-1 glycoprotein expression and viral infectivity in mammalian cells. FEBS Lett 580: 3775-3778.
23. Nowak MA, Lloyd AL, Vasquez GM, Wiltrout TA, Wahl LM, et al. (1997) Viral dynamics of primary viremia and antiretroviral therapy in simian immunodeficiency virus infection. J Virol 71: 7518-7525.
24. Stafford MA, Corey L, Cao Y, Daar ES, Ho DD, et al. (2000) Modeling plasma virus concentration during primary HIV infection. J Theor Biol 203: 285-301.
25. Bedard K, Szabo E, Michalak M, Opas M, (2005) Cellular functions of endoplasmic reticulum chaperones calreticulin, calnexin, and ERp57. Int Rev Cytol 245: 91-121.
26. Ruddock LW, Molinari M, (2006) N-glycan processing in ER quality control. J Cell Sci 119: 4373-4380.
27. Maggioni C, Braakman I, (2005) Synthesis and quality control of viral membrane proteins. Curr Top Microbiol Immunol 285: 175-198.
28. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, et al. (2003) Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 17: 1871-1879.
29. Levine CG, Mitra D, Sharma A, Smith CL, Hegde RS, (2005) The efficiency of protein compartmentalization into the secretory pathway. Mol Biol Cell 16: 279-291.
30. Scheuner D, Kaufman RJ, (2008) The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 29: 317-333.
31. Rizzotto L, Pinotti M, Pinton P, Rizzuto R, Bernardi F, (2006) Intracellular evaluation of ER targeting elucidates a mild form of inherited coagulation deficiency. Mol Med 12: 137-142.
32. Stepanyuk GA, Xu H, Wu CK, Markova SV, Lee J, et al. (2008) Expression, purification and characterization of the secreted luciferase of the copepod Metridia longa from Sf9 insect cells. Protein Expr Purif 61: 142-148.
33. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
34. MacArthur EOWaRH, (1967) The Theory of Island Biogeography. Princeton, NJ Princeton Univ. Press.
35. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, et al. (1995) Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373: 123-126.
36. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD, (1996) HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271: 1582-1586.
37. Perelson AS, Nelson PW, (1999) Mathematical Analysis of HIV-1 Dynamics in Vivo. SIAM Review 41: 3- 44.
38. Hegde RS, Bernstein HD, (2006) The surprising complexity of signal sequences. Trends Biochem Sci 31: 563-571.
39. Kang SW, Rane NS, Kim SJ, Garrison JL, Taunton J, et al. (2006) Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell 127: 999-1013.
40. Li Y, Bergeron JJ, Luo L, Ou WJ, Thomas DY, et al. (1996) Effects of inefficient cleavage of the signal sequence of HIV-1 gp 120 on its association with calnexin, folding, and intracellular transport. Proc Natl Acad Sci U S A 93: 9606-9611.
41. Wang BZ, Liu W, Kang SM, Alam M, Huang C, et al. (2007) Incorporation of high levels of chimeric human immunodeficiency virus envelope glycoproteins into virus-like particles. J Virol 81: 10869-10878.
42. Bachrach E, Dreja H, Lin YL, Mettling C, Pinet V, et al. (2005) Effects of virion surface gp120 density on infection by HIV-1 and viral production by infected cells. Virology 332: 418-429.
43. Chertova E, Bess JW Jr, Jr, Crise BJ, Sowder IR, Schaden TM, et al. (2002) Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol 76: 5315-5325.
44. Zhu P, Chertova E, Bess J Jr, Lifson JD, Arthur LO, et al. (2003) Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc Natl Acad Sci U S A 100: 15812-15817.
45. Dahirel V, Shekhar K, Pereyra F, Miura T, Artyomov M, et al. (2011) From the Cover: Coordinate linkage of HIV evolution reveals regions of immunological vulnerability. Proc Natl Acad Sci U S A 108: 11530-11535.
46. Rosen O, Sharon M, Quadt-Akabayov SR, Anglister J, (2006) Molecular switch for alternative conformations of the HIV-1 V3 region: implications for phenotype conversion. Proc Natl Acad Sci U S A 103: 13950-13955.
47. Derdeyn CA, Decker JM, Sfakianos JN, Wu X, O'Brien WA, et al. (2000) Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J Virol 74: 8358-8367.
48. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D, (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.
49. Gouy M, Guindon S, Gascuel O, (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224.