Covariance of charged amino acids at positions 322 and 440 of HIV-1 Env contributes to coreceptor specificity of subtype B viruses, and can be used to improve the performance of V3 sequence-based coreceptor usage prediction algorithms

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Cashin, Kieran ^a,b   Sterjovski, Jasminka ^a   Harvey, Katherine L ^a,b   Ramsland, Paul A ^a,b,c,d   Churchill, Melissa J ^a,c   Gorry, Paul R ^a,b,c  

^a BURNET INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d CURTIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN GP 120; VIRUS ENVELOPE PROTEIN; BACTERIOPHAGE RECEPTOR; CCR5 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO TERMINAL SEQUENCE; ARTICLE; CODON; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENETIC ALGORITHM; GENETIC CONSERVATION; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE B; MOLECULAR INTERACTION; NONHUMAN; PREDICTION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; VIRUS STRAIN; ALGORITHM; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; HOST RANGE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; NUCLEOTIDE SEQUENCE; VIRUS ATTACHMENT;

CERCOPITHECINE HERPESVIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1;

ALGORITHMS; AMINO ACID SEQUENCE; ATTACHMENT SITES, MICROBIOLOGICAL; CONSERVED SEQUENCE; HIV ENVELOPE PROTEIN GP120; HIV-1; HOST SPECIFICITY; HUMANS; MODELS, MOLECULAR; RECEPTORS, CCR5; RECEPTORS, CXCR4; VIRUS ATTACHMENT;

EID: 84907992411     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109771     Document Type: Article

References (59)

1. Choe H, Farzan M, Sun Y, Sullivan N, Rollins B, et al. (1996) The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85: 1135-1148.
2. De Jong JJ, De Ronde A, Keulen W, Tersmette M, Goudsmit J (1992) Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. J Virol 66: 6777-6780.
3. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y, et al. (1996) HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381: 667-673.
4. Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272: 872-877.
5. Berger EA, Doms RW, Fenyo EM, Korber BT, Littman DR, et al. (1998) A new classification for HIV-1. Nature 391: 240.
6. Shaw GM, Hunter E (2012) HIV transmission. Cold Spring Harb Perspect Med 2.
7. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, et al. (2009) Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 206: 1273-1289.
8. Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR (1997) Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 185: 621-628.
9. Groot F, van Capel TM, Schuitemaker J, Berkhout B, de Jong EC (2006) Differential susceptibility of naive, central memory and effector memory T cells to dendritic cell-mediated HIV-1 transmission. Retrovirology 3: 52.
10. Vergis EN, Mellors JW (2000) Natural history of HIV-1 infection. Infect Dis Clin North Am 14: 809-825, v-vi.
11. Melby T, Despirito M, Demasi R, Heilek-Snyder G, Greenberg ML, et al. (2006) HIV-1 coreceptor use in triple-class treatment-experienced patients: baseline prevalence, correlates, and relationship to enfuvirtide response. J Infect Dis 194: 238-246.
12. Mathers CD, Loncar D (2006) Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3: e442.
13. Jakobsen MR EA, Churchill MJ, Gorry PR (2010) Viral tropism, fitness and pathogenicity of HIV-1 subtype C. Futur Virol.5: 219-231.
14. Dorr P, Westby M, Dobbs S, Griffin P, Irvine B, et al. (2005) Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broad-spectrum anti-human immunodeficiency virus type 1 activity. Antimicrob Agents Chemother 49: 4721-4732.
15. Gulick RM, Lalezari J, Goodrich J, Clumeck N, DeJesus E, et al. (2008) Maraviroc for previously treated patients with R5 HIV-1 infection. N Engl J Med 359: 1429-1441.
16. Whitcomb JM, Huang W, Fransen S, Limoli K, Toma J, et al. (2007) Development and characterization of a novel single-cycle recombinant-virus assay to determine human immunodeficiency virus type 1 coreceptor tropism. Antimicrob Agents Chemother 51: 566-575.
17. Hunt JS, Romanelli F (2009) Maraviroc, a CCR5 coreceptor antagonist that blocks entry of human immunodeficiency virus type 1. Pharmacotherapy 29: 295-304.
18. Gorry PR EA, Lewin SR (2010) Maraviroc. In Kucers' The Use of Antibiotics 6th edition Edited by Grayson L, Crowe S, McCarthy J, Mills J, Mouton J, Norrby SR, Paterson D, Pfaller M London: Hodder & Stoughton Ltd: 2869-2876.
19. Wilkin TJ, Goetz MB, Leduc R, Skowron G, Su Z, et al. (2011) Reanalysis of coreceptor tropism in HIV-1-infected adults using a phenotypic assay with enhanced sensitivity. Clin Infect Dis 52: 925-928.
20. Huang CC, Lam SN, Acharya P, Tang M, Xiang SH, et al. (2007) Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317: 1930-1934.
21. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, et al. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
22. Hwang SS, Boyle TJ, Lyerly HK, Cullen BR (1991) Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 253: 71-74.
23. Fouchier RA, Groenink M, Kootstra NA, Tersmette M, Huisman HG, et al. (1992) Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J Virol 66: 3183-3187.
24. Hoffman NG, Seillier-Moiseiwitsch F, Ahn J, Walker JM, Swanstrom R (2002) Variability in the human immunodeficiency virus type 1 gp120 Env protein linked to phenotype-associated changes in the V3 loop. J Virol 76: 3852-3864.
25. Jensen MA, Li FS, van 't Wout AB, Nickle DC, Shriner D, et al. (2003) Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J Virol 77: 13376-13388.
26. Jakobsen MR, Cashin K, Roche M, Sterjovski J, Ellett A, et al. (2013) Longitudinal Analysis of CCR5 and CXCR4 Usage in a Cohort of Antiretroviral Therapy-Naive Subjects with Progressive HIV-1 Subtype C Infection. PLoS One 8: e65950.
27. Shioda T, Levy JA, Cheng-Mayer C (1992) Small amino acid changes in the V3 hypervariable region of gp120 can affect the T-cell-line and macrophage tropism of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 89: 9434-9438.
28. Lengauer T, Sander O, Sierra S, Thielen A, Kaiser R (2007) Bioinformatics prediction of HIV coreceptor usage. Nat Biotechnol 25: 1407-1410.
29. Jensen MA, Coetzer M, van 't Wout AB, Morris L, Mullins JI (2006) A reliable phenotype predictor for human immunodeficiency virus type 1 subtype C based on envelope V3 sequences. J Virol 80: 4698-4704.
30. McGovern RA, Thielen A, Mo T, Dong W, Woods CK, et al. (2010) Population-based V3 genotypic tropism assay: a retrospective analysis using screening samples from the A4001029 and MOTIVATE studies. AIDS 24: 2517-2525.
31. McGovern RA, Thielen A, Portsmouth S, Mo T, Dong W, et al. (2012) Population-based sequencing of the V3-loop can predict the virological response to maraviroc in treatment-naive patients of the MERIT trial. J Acquir Immune Defic Syndr 61: 279-286.
32. Swenson LC, Mo T, Dong WW, Zhong X, Woods CK, et al. (2011) Deep sequencing to infer HIV-1 co-receptor usage: application to three clinical trials of maraviroc in treatment-experienced patients. J Infect Dis 203: 237-245.
33. Swenson LC, Mo T, Dong WW, Zhong X, Woods CK, et al. (2011) Deep V3 sequencing for HIV type 1 tropism in treatment-naive patients: a reanalysis of the MERIT trial of maraviroc. Clin Infect Dis 53: 732-742.
34. Carrillo A, Ratner L (1996) Cooperative effects of the human immunodeficiency virus type 1 envelope variable loops V1 and V3 in mediating infectivity for T cells. J Virol 70: 1310-1316.
35. Coetzer M, Nedellec R, Cilliers T, Meyers T, Morris L, et al. (2011) Extreme genetic divergence is required for coreceptor switching in HIV-1 subtype C. J Acquir Immune Defic Syndr 56: 9-15.
36. Pastore C, Nedellec R, Ramos A, Pontow S, Ratner L, et al. (2006) Human immunodeficiency virus type 1 coreceptor switching: V1/V2 gain-of-fitness mutations compensate for V3 loss-of-fitness mutations. J Virol 80: 750-758.
37. Carrillo A, Ratner L (1996) Human immunodeficiency virus type 1 tropism for T-lymphoid cell lines: role of the V3 loop and C4 envelope determinants. J Virol 70: 1301-1309.
38. Labrosse B, Treboute C, Brelot A, Alizon M (2001) Cooperation of the V1/V2 and V3 domains of human immunodeficiency virus type 1 gp120 for interaction with the CXCR4 receptor. J Virol 75: 5457-5464.
39. Nabatov AA, Pollakis G, Linnemann T, Kliphius A, Chalaby MI, et al. (2004) Intrapatient alterations in the human immunodeficiency virus type 1 gp120 V1V2 and V3 regions differentially modulate coreceptor usage, virus inhibition by CC/CXC chemokines, soluble CD4, and the b12 and 2G12 monoclonal antibodies. J Virol 78: 524-530.
40. Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143: 29-36.
41. Cashin K, Gray LR, Jakobsen MR, Sterjovski J, Churchill MJ, et al. (2013) CoRSeqV3-C: a novel HIV-1 subtype C specific V3 sequence based coreceptor usage prediction algorithm. Retrovirology 10: 24.
42. Roche M, Jakobsen MR, Sterjovski J, Ellett A, Posta F, et al. (2011) HIV-1 escape from the CCR5 antagonist maraviroc associated with an altered and lessefficient mechanism of gp120-CCR5 engagement that attenuates macrophage tropism. J Virol 85: 4330-4342.
43. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
44. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
45. Thielen A, Lengauer T, Swenson LC, Dong WW, McGovern RA, et al. (2011) Mutations in gp41 are correlated with coreceptor tropism but do not improve prediction methods substantially. Antivir Ther 16: 319-328.
46. Rosen O, Samson AO, Anglister J (2008) Correlated mutations at gp120 positions 322 and 440: implications for gp120 structure. Proteins 71: 1066-1070.
47. Yamaguchi-Kabata Y, Yamashita M, Ohkura S, Hayami M, Miura T (2004) Linkage of amino acid variation and evolution of human immunodeficiency virus type 1 gp120 envelope glycoprotein (subtype B) with usage of the second receptor. J Mol Evol 58: 333-340.
48. Biscone MJ, Miamidian JL, Muchiri JM, Baik SS, Lee FH, et al. (2006) Functional impact of HIV coreceptor-binding site mutations. Virology 351: 226-236.
49. Tsuchiya K, Ode H, Hayashida T, Kakizawa J, Sato H, et al. (2013) Arginine insertion and loss of N-linked glycosylation site in HIV-1 envelope V3 region confer CXCR4-tropism. Sci Rep 3: 2389.
50. Schnur E, Noah E, Ayzenshtat I, Sargsyan H, Inui T, et al. (2011) The conformation and orientation of a 27-residue CCR5 peptide in a ternary complex with HIV-1 gp120 and a CD4-mimic peptide. J Mol Biol 410: 778-797.
51. Moore JP, Thali M, Jameson BA, Vignaux F, Lewis GK, et al. (1993) Immunochemical analysis of the gp120 surface glycoprotein of human immunodeficiency virus type 1: probing the structure of the C4 and V4 domains and the interaction of the C4 domain with the V3 loop. J Virol 67: 4785-4796.
52. Suphaphiphat P, Essex M, Lee TH (2007) Mutations in the V3 stem versus the V3 crown and C4 region have different effects on the binding and fusion steps of human immunodeficiency virus type 1 gp120 interaction with the CCR5 coreceptor. Virology 360: 182-190.
53. Cimbro R, Gallant TR, Dolan MA, Guzzo C, Zhang P, et al. (2014) Tyrosine sulfation in the second variable loop (V2) of HIV-1 gp120 stabilizes V2-V3 interaction and modulates neutralization sensitivity. Proc Natl Acad Sci U S A 111: 3152-3157.
54. McGovern RA, Mo T, Woods C, Zhong X, Thielen A, et al. (2009) Abstract PE3.4/8. Program and abstracts of the 12th European AIDS Conference. Cologne, Germany; 2009. Optimization of clinically relevant cut-points for the determination of HIV co-receptor usage to predict maraviroc responses in treatment experienced (TE) patients using population V3 genotyping; p. 11-4. European AIDS Clinical Society.
55. Mulinge M, Lemaire M, Servais JY, Rybicki A, Struck D, et al. (2013) HIV-1 tropism determination using a phenotypic Env recombinant viral assay highlights overestimation of CXCR4-usage by genotypic prediction algorithms for CRRF01-AE and CRF02-AG. PLoS One 8: e60566.
56. Recordon-Pinson P, Soulie C, Flandre P, Descamps D, Lazrek M, et al. (2010) Evaluation of the genotypic prediction of HIV-1 coreceptor use versus a phenotypic assay and correlation with the virological response to maraviroc: the ANRS GenoTropism study. Antimicrob Agents Chemother 54: 3335-3340.
57. Raymond S, Delobel P, Mavigner M, Ferradini L, Cazabat M, et al. (2010) Prediction of HIV type 1 subtype C tropism by genotypic algorithms built from subtype B viruses. J Acquir Immune Defic Syndr 53: 167-175.
58. Garrido C, Roulet V, Chueca N, Poveda E, Aguilera A, et al. (2008) Evaluation of eight different bioinformatics tools to predict viral tropism in different human immunodeficiency virus type 1 subtypes. J Clin Microbiol 46: 887-891.
59. Raymond S, Delobel P, Mavigner M, Cazabat M, Souyris C, et al. (2008) Correlation between genotypic predictions based on V3 sequences and phenotypic determination of HIV-1 tropism. AIDS 22: F11-16.