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

Journal of Virology

Volumn 78, Issue 1, 2004, Pages 524-530

  Nabatov, Alexey A ^a   Pollakis, Georgios ^a   Linnemann, Thomas ^a   Kliphius, Aletta ^a   Chalaby, Moustapha I M ^a,b   Paxton, William A ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b GENMAB   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CHEMOKINE; BETA CHEMOKINE; CD4 ANTIGEN; GLYCOPROTEIN GP 120; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 2G12; MONOCLONAL ANTIBODY B12; RANTES; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CHIMERA; DISEASE COURSE; GENE MAPPING; GLYCOSYLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STRUCTURE; VIROGENESIS; VIRUS ENVELOPE; VIRUS GENE; VIRUS INHIBITION; VIRUS ISOLATION; VIRUS STRAIN;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD4; CHEMOKINES, CC; CHEMOKINES, CXC; DISEASE PROGRESSION; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; MUTATION; NEUTRALIZATION TESTS; PEPTIDE FRAGMENTS; RANTES; RECEPTORS, CCR5; RECEPTORS, CXCR4; SOLUBILITY;

EID: 0346365289     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.1.524-530.2004     Document Type: Article

References (57)

1. Back, N. K. T., L. Smit, J. J. de Jong, W. Keulen, M. Schutten, J. Goudsmit, and M. Tersmette. 1994. An N-glycan within the human immunodeficiency virus type 1 gp120 V3 loop affects virus neutralization. Virology 199:431-438.
2. Berger, E. A. 1997. HIV entry and tropism: the chemokine receptor connection. AIDS 11(Suppl. A):S3-S16.
3. Berger, E. A., R. W. Doms, E. M. Fenyo, B. T. Korber, D. R. Littman, J. P. Moore, Q. J. Sattentau, H. Schuitemaker, J. Sodroski, and R. A. Weiss. 1998. A new classification for HIV-1. Nature 391:240.
4. Bleul, C. C., M. Farzan, H. Choe, C. Parolin, I. Clark-Lewis, J. Sodroski, and T. A. Springer. 1996. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382:829-833.
5. Bouma, P., M. Leavitt, P. F. Zhang, I. A. Sidorov, D. S. Dimitrov, and G. V. Quinnan, Jr. 2003. Multiple interactions across the surface of the gp120 core structure determine the global neutralization resistance phenotype of human immunodeficiency virus type 1. J. Virol. 77:8061-8071.
6. Boyer, P. L., H. Q. Gao, and S. H. Hughes. 1998. A mutation at position 190 of human immunodeficiency virus type 1 reverse transcriptase interacts with mutations at positions 74 and 75 via the template primer. Antimicrob. Agents Chemother. 42:447-452.
7. Carrillo, A., and L. Ratner. 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.
8. + T cells. Science 270:1811-1815.
9. + T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J. Virol. 67:1772-1777.
10. Cornelissen, M., G. Mulder-Kampinga, J. Veenstra, F. Zorgdrager, C. Kuiken, S. Hartman, J. Dekker, L. van der Hoek, C. Sol, R. Coutinho, and J. Goudsmit. 1995. Syncytium-inducing (SI) phenotype suppression at seroconversion after intramuscular inoculation of a non-syncytium-inducing/SI phenotypically mixed human immunodeficiency virus population. J. Virol. 69:1810-1818.
11. de Jong, J. J., A. de Ronde, W. Keulen, M. Tersmette, and J. Goudsmit. 1992. Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing (SI) phenotype: analysis by single amino acid substitution. J. Virol. 66:6777-6780.
12. de Jong, J. J., J. Goudsmit, W. Keulen, B. Klaver, W. Krone, M. Tersmette, and A. de Ronde. 1992. Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium formation and replication capacity. J. Virol. 66:757-765.
13. de Wolf, F., E. Hogervorst, J. Goudsmit, E.-M. Fenyö, H. Rübsamen-Waigmann, H. Holmes, B. Galvao-Castro, E. Karita, C. Wasi, S. D. K. Sempala, E. Baan, F. Zorgdrager, V. Lukashov, S. Osmanov, C. Kuiken, M. Cornelissen, and WHO Network on HIV Isolation and Characterization. 1994. Syncytium-inducing and non-syncytium-inducing capacity of human immunodeficiency virus type 1 subtypes other than B: phenotypic and genotypic characteristics. AIDS Res. Hum. Retrovir. 10:1387-1400.
14. Doranz, B. J., J. Rucker, Y. Yi, R. J. Smyth, M. Samson, S. C. Peiper, M. Parmentier, R. G. Collman, and R. W. Doms. 1996. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85:1149-1158.
15. Fouchier, R. A. M., M. Groenink, N. A. Kootstra, M. Tersmette, H. G. Huisman, F. Miedema, and H. Schuitemaker. 1992. Phenotype associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J. Virol. 66:3183-3187.
16. Gallo, R. C., S. Z. Salahuddin, M. Popovic, G. M. Shearer, M. Kaplan, B. F. Haynes, T. J. Palker, R. Redfield, J. Oleske, B. Safai, G. White, P. Foster, and P. D. Markham. 1984. Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS. Science 224:500-503.
17. Gonda, M. A., F. Wong-Staal, R. C. Gallo, J. E. Clements, O. Narayan, and R. V. Gilden. 1985. Sequence homology and morphologic similarity of HTLV-III and visna virus, a pathogenic lentivirus. Science 227:173-177.
18. Gram, G. J., A. Hemming, A. Bolmstedt, B. Jansson, S. Olofsson, L. Akerblom, J. O. Nielsen, and J. E. Hansen. 1994. Identification of an N-linked glycan in the V1-loop of HIV-1 gp120 influencing neutralization by anti-V3 antibodies and soluble CD4. Arch. Virol. 139:253-261.
19. Groenink, M., R. A. Fouchier, S. Broersen, C. H. Baker, M. Koot, A. B. van't Wout, H. G. Huisman, F. Miedema, M. Tersmette, and H. Schuitemaker. 1993. Relation of phenotype evolution of HIV-1 to envelope V2 configuration. Science 260:1513-1516.
20. Hammond, A. L., J. Lewis, J. May, J. Albert, P. Balfe, and J. A. McKeating. 2001. Antigenic variation within the CD4 binding site of human immunodeficiency virus type 1 gp120: effects on chemokine receptor utilization. J. Virol. 75:5593-5603.
21. Hwang, S. S., T. J. Boyle, H. K. Lyerly, and B. R. Cullen. 1992. Identification of envelope V3 loop as the major determinant of CD4 neutralization sensitivity of HIV-1. Science 257:535-537.
22. Johnson, W. E., J. M. Sauvron, and R. C. Desrosiers. 2001. Conserved, N-linked carbohydrates of human immunodeficiency virus type 1 gp41 are largely dispensable for viral replication. J. Virol. 75:11426-11436.
23. Kitrinos, K. M., N. G. Hoffman, J. A. E. Nelson, and R. Swanstrom. 2003. Turnover of env variable region 1 and 2 genotypes in subjects with late-stage human immunodeficiency virus type 1 infection. J. Virol. 77:6811-6822.
24. Kohlstaedt, L. A., J. Wang, J. M. Friedman, P. A. Rice, and T. A. Steitz. 1992. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256:1783-1790.
25. Koito, A., G. Harrowe, J. A. Levy, and C. Cheng-Mayer. 1994. Functional role of the V1/V2 region of human immunodeficiency virus type 1 envelope glycoprotein gp120 in infection of primary macrophages and soluble CD4 neutralization. J. Virol. 68:2253-2259.
26. Koito, A., L. Stamatatos, and C. Cheng-Mayer. 1995. Small amino acid sequence changes within the V2 domain can affect the function of a T-cell line-tropic human immunodeficiency virus type 1 envelope gp120. Virol. 206:878-884.
27. Kolchinsky, P., E. Kiprilov, P. Bartley, R. Rubinstein, and J. Sodroski. 2001. Loss of a single N-linked glycan allows CD4-independent human immunodeficiency virus type 1 infection by altering the position of the gp120 V1/V2 variable loops. J. Virol. 75:3435-3443.
28. + cell depletion and progression of AIDS. Ann. Intern. Med. 118:681-688.
29. Korber, B. T. M., K. MacInnes, R. F. Smith, and G. Myers. 1994. Mutational trends in V3 loop protein sequences observed in different genetic lineages of human immunodeficiency virus type 1. J. Virol 68:6730-6744.
30. Labrosse, B., C. Treboute, A. Brelot, and M. Alizon. 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.
31. Land, A., and I. Braakman. 2001. Folding of the human immunodeficiency virus type 1 envelope glycoprotein in the endoplasmic reticulum. Biochimie. 83:783-790.
32. Lee, M. K., J. Heaton, and M. W. Cho. 1999. Identification of determinants of interaction between CXCR4 and gp120 of a dual-tropic HIV-1DH12 isolate. Virology 257:290-296.
33. Ly, A., and L. Stamatatos. 2000. V2 loop glycosylation of the human immunodeficiency virus type 1 SF162 envelope facilitates interaction of this protein with CD4 and CCR5 receptors and protects the virus from neutralization by anti-V3 loop and anti-CD4 binding site antibodies. J. Virol. 74:6769-6776.
34. Malenbaum, S. E., D. Yang, L. Cavacini, M. Posner, J. Robinson, and C. Cheng-Mayer. 2000. The N-terminal V3 loop glycan modulates the interaction of clade A and B human immunodeficiency virus type 1 envelopes with CD4 and chemokine receptors. J. Virol. 74:11008-11016.
35. McKnight, A., R. A. Weiss, C. Shotton, Y. Takeuchi, H. Hoshino, and P. R. Clapham. 1995. Change in tropism upon immune escape by human immunodeficiency virus. J. Virol. 69:3167-3170.
36. Narayan, O., M. C. Zink, D. Huso, D. Sheffer, S. Crane, S. Kennedy-Stoskopf, P. E. Jolly, and J. E. Clements. 1988. Lentiviruses of animals are biological models of the human immunodeficiency viruses. Microb. Pathog. 5:149-157.
37. Ogert, R. A., M. K. Lee, W. Ross, A. Buckler-White, M. A. Martin, and M. W. Cho. 2001. N-linked glycosylation sites adjacent to and within the V1/V2 and the V3 loops of dualtropic human immunodeficiency virus type 1 isolate DH12 gp120 affect coreceptor usage and cellular tropism. J. Virol. 75:5998-6006.
38. Pollakis, G., S. Kang, A. Kliphuis, M. I. Chalaby, J. Goudsmit, and W. A. Paxton. 2001. N-linked glycosylation of the HIV type 1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J. Biol. Chem. 276:13433-13441.
39. Purtscher, M., A. Trkola, G. Gruber, A. Buchacher, R. Predl, F. Steindl, C. Tauer, R. Berger, N. Barrett, and A. Jungbauer. 1994. A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 10:1651-1658.
40. Roben, P., J. P. Moore, M. Thali, J. Sodroski, C. F. Barbas III, and D. R. Burton. 1994. Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1. J. Virol. 68:4821-4828.
41. Sanders, R. W., M. Venturi, L. Schiffner, R. Kalyanaraman, H. Katinger, K. O. Lloyd, P. D. Kwong, and J. P. Moore. 2002. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76:7293-7305.
42. Sattentau, Q. J., A. G. Dalgleish, R. A. Weiss, and P. C. L. Beverley. 1986. Epitopes of the CD4 antigen and HIV infection. Science 234:1120-1123.
43. Scarlatti, G., E. Tresoldi, A. Bjorndal, R. Fredriksson, C. Colognesi, H. K. Deng, M. S. Malnati, A. Plebani, A. G. Siccardi, D. R. Littman, E. M. Fenyo, and P. Lusso. 1997. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat. Med. 3:1259-1265.
44. Schock, H. B., V. M. Garsky, and L. C. Kuo. 1996. Mutational anatomy of an HIV-1 protease variant conferring cross-resistance to protease inhibitors in clinical trials. Compensatory modulations of binding and activity. J. Biol. Chem. 271:31957-31963.
45. Schuitemaker, H., M. Koot, N. A. Kootstra, M. W. Dercksen, R. E. Y. de Goede, R. P. van Steenwijk, J. M. A. Lange, J. K. M. Eeftinck Schattenkerk, F. Miedema, and M. Tersmette. 1992. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus populations. J. Virol. 66:1354-1360.
46. Schuitemaker, H., N. A. Kootstra, R. E. Y. de Goede, F. de Wolf, F. Miedema, and M. Tersmette. 1991. Monocytotropic human immunodeficiency virus type 1 (HIV-1) variants detectable in all stages of HIV-1 infection lack T-cell line tropism and syncytium-inducing ability in primary T-cell culture. J. Virol. 65:356-363.
47. Shioda, T., S. Oka, S. M. Xin, H. Liu, R. Harukuni, A. Kurotani, M. Fukushima, M. K. Hasan, T. Shino, Y. Takebe, A. Iwamoto, and Y. Nagai. 1997. In vivo sequence variability of human immunodeficiency virus type 1 envelope gp120: association of V2 extension with slow disease progression. J. Virol. 71:4871-4881.
48. Spijkerman, I. J. B., M. Koot, M. Prins, I. P. M. Keet, A. J. A. R. van den Hoek, F. Miedema, and R. A. Coutinho. 1995. Lower prevalence and incidence of HIV-1 syncytium-inducing phenotype among injecting drug users compared with homosexual men. AIDS 9:1085-1092.
49. Tersmette, M., J. M. A. Lange, R. E. Y. de Goede, F. de Wolf, J. K. M. Eeftinck Schattenkerk, P. T. A. Schellekens, R. A. Coutinho, J. G. Huisman, J. Goudsmit, and F. Miedema. 1989. Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality. Lancet i:983-985.
50. Trkola, A., W. A. Paxton, S. P. Monard, J. A. Hoxie, M. A. Siani, D. A. Thompson, L. Wu, C. R. Mackay, R. Horuk, and J. P. Moore. 1998. Genetic subtype-independent inhibition of human immunodeficiency virus type 1 replication by CC and CXC chemokines. J. Virol. 72:396-404.
51. Trkola, A., M. Purtscher, T. Muster, C. Ballaun, A. Buchacher, N. Sullivan, K. Srinivasan, J. Sodroski, J. P. Moore, and H. Katinger. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70:1100-1108.
52. Tscherning, C., A. Alaeus, R. Fredriksson, A. Bjorndal, H. Deng, D. R. Littman, E. M. Fenyo, and J. Albert. 1998. Differences in chemokine coreceptor usage between genetic subtypes of HIV-1. Virology 241:181-188.
53. Van Rij, R. P., and H. Schuitemaker. 2002. Host genetic factors in the clinical course of HIV-1 infection: chemokines and chemokine receptors. Community Genet. 5:88-101.
54. Watkins, B. A., R. Crowley, A. E. Davis, A. T. Louie, and M. S. Reitz, Jr. 1997. Syncytium formation induced by human immunodeficiency virus type 1 isolates correlates with affinity for CD4. J. Gen. Virol. 78(Pt. 10):2513-2522.
55. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
56. Xiang, S. H., P. D. Kwong, R. Gupta, C. D. Rizzuto, D. J. Casper, R. Wyatt, L. Wang, W. A. Hendrickson, M. L. Doyle, and J. Sodroski. 2002. Mutagenic stabilization and/or disruption of a CD4-bound state reveals distinct conformations of the human immunodeficiency virus type 1 gp120 envelope glycoprotein. J. Virol. 76:9888-9899.
57. Zhang, Y. J., and J. P. Moore. 1999. Will multiple coreceptors need to be targeted by inhibitors of human immunodeficiency virus type 1 entry? J. Virol. 73:3443-3448.