Subtle evolutionary changes in the distribution of N-glycosylation sequons in the HIV-1 envelope glycoprotein 120

International Journal of Biological Sciences

Volumn 6, Issue 5, 2010, Pages 407-418

  Shyama Prasad Rao, R ^a   Wollenweber, Bernd ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

Glycoprotein; Human immunodeficiency virus; Molecular evolution; N glycosylation sequons

Indexed keywords

GLYCOPROTEIN GP 120; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ARTICLE; CHEMISTRY; GLYCOSYLATION; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; SEQUENCE ANALYSIS;

AMINO ACID MOTIFS; BASE SEQUENCE; EVOLUTION, MOLECULAR; GLYCOSYLATION; HIV ENVELOPE PROTEIN GP120; HIV-1; SEQUENCE ANALYSIS, PROTEIN;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77956954387     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (41)

1. Spiro RG. Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiol. 2002; 12: 43R-56R.
2. Dennis JW, Granovsky M, Warren CE. Protein glycosylation in development and disease. Bioessays. 1999; 21: 412-421.
3. Verki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiol. 1993; 3: 97-130.
4. Ben-Dor S, Esterman N, Rubin E, Sharon N. Biases and complex patterns in the residues flanking protein N-glycosylation sites. Glycobiol. 2004; 14: 95-101.
5. Petrescu A-J, Milac A-L, Petrescu SM, et al. Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiol. 2004; 14: 103-114.
6. Rao RSP, Buus OT, Wollenweber B. Evolutionary pattern of N-glycosylation sequon numbers in eukaryotic ABC protein superfamilies. Bioinf Biol Insights. 2010; 4: 9-17.
7. Kwong PD, Wyatt R, Robinson J, et al. Structure of an HIVgp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature. 1998; 393: 648-659.
8. Kwong PD, Doyle ML, Casper DJ, et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature. 2002; 420: 678-682.
9. Poumbourios P, Maerz AL, Drummer HE. Functional evolution of the HIV-1 envelope glycoprotein 120 association site of gly-coprotein 41. J Biol Chem. 2003; 278: 42149-42160.
10. Botarelli P, Houlden BA, Haigwood NL, et al. N-glycosylation of HIV-gp120 may constrain recognition by T lymphocytes. J Immunol. 1991; 9: 3128-3132.
11. Leonard CK, Spellman MW, Riddle L, et al. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J Biol Chem. 1990; 265: 10373-10382.
12. Zhu X, Borchers C, Bienstock RJ, Tomer KB. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochem. 2000; 39: 11194-11204.
13. Losman B, Bolmstedt A, Schønning K, et al. Protection of neutralization epitopes in the V3 loop of oligomeric human immunodeficiency virus type 1 glycoprotein 120 by N-linked oli-gosaccharides in the V1 region. AIDS Res Hum Retroviruses. 2001; 17: 1067-1076.
14. Montefiori DC, Robinson WR Jr, Mitchell WM. Role of protein N-glycosylation in pathogenesis of human immunodeficiency virus type 1. Proc Natl Acad Sci USA. 1988; 85: 9248-9252.
15. Dirckx L, Lindemann D, Ette R, et al. Mutation of conserved N-glycosylation sites around the CD4-binding site of human immunodeficiency virus type 1 GP120 affects viral infectivity. Virus Res. 1990; 18: 9-20.
16. Wei X, Decker JM, Wang S, et al. Antibody neutralization and escape by HIV-1. Nature. 2003; 422: 307-312.
17. Poon AFY, Lewis FI, Pond SLK, Frost SWD. Evolutionary interactions between N-linked glycosylation sites in the HIV-1 envelope. PLoS Comput Biol. 2007; 3: 110-119.
18. Balzarini J, Laethem KV, Hatse S, et al. Marked depletion of glycosylation sites in HIV-1 gp120 under selection pressure by the mannose-specific plant lectins of Hippeastrum hybrid and Galanthus nivalis. Mol Pharmacol. 2005; 67: 1556-1565.
19. Novitsky V, Lagakos S, Herzig M, et al. Evolution of proviral gp120 over the first year of HIV-1 subtype C infection. Virol. 2009; 383: 47-59.
20. Gunthard HF, Leigh-Brown AJ, D'Aquila RT, et al. Higher selection pressure from antiretroviral drugs in vivo results in increased evolutionary distance in HIV-1 pol. Virol. 1999; 259: 154-165.
21. Zhang M, Gaschen B, Blay W, et al. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiol. 2004; 14: 1229-1246.
22. Cui J, Smith T, Robbins PW, Samuelson J. Darwinian selection for sites of Asn-linked glycosylation in phylogenetically disparate eukaryotes and viruses. Proc Natl Acad Sci USA. 2009; 106: 13421-13426.
23. Wolk T, Schreiber M. N-Glycans in the gp120 V1/V2 domain of the HIV-1 strain NL4-3 are indispensable for viral infectivity and resistance against antibody neutralization. Med Microbiol Immunol. 2006; 195: 165-172.
24. Ewens WJ, Wilf HS. Computing the distribution of the maximum in balls-and-boxes problems with application to clusters of disease cases. Proc Natl Acad Sci USA. 2007; 104: 11189-11191.
25. Feller W. An introduction to probability theory and its applications. New York, USA: Wiley; 1968.
26. Lamboy WF, Moreno-Hagelsieb G. A new method of solution for the occupancy problem and its application to operon size prediction. J Theor Biol. 2004; 227: 315-322.
27. Park CJ. A note on the classical occupancy problem. Ann Math Stat. 1972; 43: 1698-1701.
28. Williamson PP, Mays DP, Asmerom GA, Yang Y. Revisiting the classical occupancy problem. Am stat. 2009; 63: 356-360.
29. Wu G, Yan S-M. Analysis of distribution of amino acids in the primary structure of tumor suppressor p53 family according to the random mechanism. J Mol Model. 2002; 8: 191-198.
30. Alexander S, Elder JH. Carbohydrate dramatically influences immune reactivity of antisera to viral glycoprotein antigens. Science. 1984; 226: 1328-1330.
31. Chen H, Xu X, Jones IM. Immunogenicity of the outer domain of a HIV-1 clade C gp120. Retrovirol. 2007; 4: 33.
32. Hotzel I. Conservation of inner domain modules in the surface envelope glycoproteins of an ancient rabbit lentivirus and extant lentiviruses and betaretroviruses. Virol. 2008; 372: 201-207.
33. Doria-Rose NA, Learn GH, Rodrigo AG, et al. Human immunodeficiency virus type 1 subtype B ancestral envelope protein is functional and elicits neutralizing antibodies in rabbits similar to those elicited by a circulating subtype B envelope. J Virol. 2005; 79: 11214-11224.
34. Ohgimoto S, Shioda T, Mori K, et al. Location-specific, unequal contribution of the N glycans in simian immunodeficiency virus gp120 to viral infectivity and removal of multiple glycans without disturbing infectivity. J Virol. 1998; 72: 8365-8370.
35. Lee WR, Syu WJ, Du B, et al. Nonrandom distribution of gp120 N-linked glycosylation sites important for infectivity of human immunodeficiency virus type 1. Proc Natl Acad Sci USA. 1992; 89: 2213-2217.
36. Belair M, Dovat M, Foley B, et al. The polymorphic nature of HIV type 1 env V4 affects the patterns of potential N-glycosylation sites in proviral DNA at the intrahost level. Aids Res Hum Retroviruses 2009; 25: 199-206.
37. Delos SE, Burdick MJ, White JM. A single glycosylation site within the receptor-binding domain of the avian sarco-ma/leukosis virus glycoprotein is critical for receptor binding. Virol. 2002; 294: 354-363.
38. Walmsley AR, Hooper NM. Distance of sequons to the C-terminus influences the cellular N-glycosylation of the prion protein. Biochem J. 2003; 370: 351-355.
39. Weber ANR, Morse MA, Gay NJ. Four N-linked glycosylation sites in human toll-like receptor 2 cooperate to direct efficient biosynthesis and secretion. J Biol Chem. 2004; 279: 34589-34594.
40. Wojczyk BS, Takahashi N, Levy MT, et al. N-glycosylation at one rabies virus glycoprotein sequon influences N-glycan processing at a distant sequon on the same molecule. Glycobiol. 2005; 15: 655-666.
41. Lin G, Simmons G, Pohlmann S, et al. Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR. J Virol. 2003; 77: 1337-1346.