Evolution of CCR5 use before and during coreceptor switching

Journal of Virology

Volumn 82, Issue 23, 2008, Pages 11758-11766

  Coetzer, Mia ^a   Nedellec, Rebecca ^a   Salkowitz, Janelle ^a,c   McLaughlin, Sherry ^b   Liu, Yi ^b   Heath, Laura ^b   Mullins, James I ^b   Mosier, Donald E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; DNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENVELOPE GENE; GENE SEQUENCE; GENE SWITCHING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INCIDENCE; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS TRANSMISSION;

ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HUMANS; RECEPTORS, CCR5; RECEPTORS, CXCR4;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 56449100427     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01141-08     Document Type: Article

References (77)

1. Baba, M., O. Nishimura, N. Kanzaki, M. Okamoto, H. Sawada, Y. Iizawa, M. Shiraishi, Y. Aramaki, K. Okonogi, Y. Ogawa, K. Meguro, and M. Fujino. 1999. A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc. Natl. Acad. Sci. USA 96:5698-5703.
2. Bozzette, S., J. McCutchan, S. Spector, B. Wright, and D. Richman. 1993. A cross-sectional comparison of persons with syncytium- and non-syncytium-inducing human immunodeficiency virus. J. Infect. Dis. 168:1374-1379.
3. Brumme, Z. L., J. Goodrich, H. B. Mayer, C. J. Brumme, B. M. Henrick, B. Wynhoven, J. J. Asselin, P. K. Cheung, R. S. Hogg, J. S. Montaner, and P. R. Harrigan. 2005. Molecular and clinical epidemiology of CXCR4-using HIV-1 in a large population of antiretroviral-naive individuals. J. Infect. Dis. 192:466-474.
4. Bunnik, E. M., L. Pisas, A. C. van Nuenen, and H. Schuitemaker. 2008. Autologous neutralizing humoral immunity and evolution of the viral envelope in the course of subtype B human immunodeficiency virus type 1 infection. J. Virol. 82:7932-7941.
5. Cann, A. J., M. J. Churcher, M. Boyd, W. O'Brien, J. Q. Zhao, J. Zack, and I. S. Chen. 1992. The region of the envelope gene of human immunodeficiency virus type 1 responsible for determination of cell tropism. J. Virol. 66:305-309.
6. Chesebro, B., K. Wehrly, J. Nishio, and S. Perryman. 1996. Mapping of independent V3 envelope determinants of human immunodeficiency virus type 1 macrophage tropism and syncytium formation in lymphocytes. J. Virol. 70:9055-9059.
7. Cho, M. W., M. K. Lee, M. C. Carney, J. F. Berson, R. W. Doms, and M. A. Martin. 1998. Identification of determinants on a dualtropic human immunodeficiency virus type 1 envelope glycoprotein that confer usage of CXCR4. J. Virol. 72:2509-2515.
8. Cilliers, T., J. Nhlapo, M. Coetzer, D. Orlovic, T. Ketas, W. C. Olson, J. P. Moore, A. Trkola, and L. Morris. 2003. The CCR5 and CXCR4 coreceptors are both used by human immunodeficiency virus type 1 primary isolates from subtype C. J. Virol. 77:4449-4456.
9. Coetzer, M., T. Cilliers, M. Papathanasopoulos, G. Ramjee, S. A. Karim, C. Williamson, and L. Morris. 2007. Longitudinal analysis of HIV type 1 subtype C envelope sequences from South Africa. AIDS Res. Hum. Retrovir. 23:316-321.
10. Coetzer, M., T. Cilliers, L. H. Ping, R. Swanstrom, and L. Morris. 2006. Genetic characteristics of the V3 region associated with CXCR4 usage in HIV-1 subtype C isolates. Virology 356:95-105.
11. Connor, R. I., B. K. Chen, S. Choe, and N. R. Landau. 1995. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206:935-944.
12. + T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J. Virol. 67:1772-1777.
13. Deng, H. K., D. Unutmaz, V. N. KewalRamani, and D. R. Littman. 1997. Expression cloning of new receptors used by simian and human immunodeficiency viruses. Nature 388:296-300.
14. Don, R. H., P. T. Cox, B. J. Wainwright, K. Baker, and J. S. Mattick. 1991. "Touchdown" PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 19:4008.
15. Donzella, G. A., D. Schols, S. W. Lin, J. A. Este, K. A. Nagashima, P. J. Maddon, G. P. Allaway, T. P. Sakmar, G. Henson, E. De Clercq, and J. P. Moore. 1998. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4:72-77.
16. Farzan, M., S. Chung, W. Li, N. Vasilieva, P. L. Wright, C. E. Schnitzler, R. J. Marchione, C. Gerard, N. P. Gerard, J. Sodroski, and H. Choe. 2002. Tyrosine-sulfated peptides functionally reconstitute a CCR5 variant lacking a critical amino-terminal region. J. Biol. Chem. 277:40397-40402.
17. Fernàndez, G., A. Llano, M. Esgleas, B. Clotet, J. A. Este, and M. A. Martinez. 2006. Purifying selection of CCR5-tropic human immunodeficiency virus type 1 variants in AIDS subjects that have developed syncytium-inducing, CXCR4-tropic viruses. J. Gen. Virol. 87:1285-1294.
18. Goodenow, M. M., and R. G. Collman. 2006. HIV-1 coreceptor preference is distinct from target cell tropism: a dual-parameter nomenclature to define viral phenotypes. J. Leukoc. Biol. 80:965-972.
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. Harouse, J. M., C. Buckner, A. Gettie, R. Fuller, R. Bohm, J. Blanchard, and C. Cheng-Mayer. 2003. CD8+ T cell-mediated CXC chemokine receptor 4-simian/human immunodeficiency virus suppression in dually infected rhesus macaques. Proc. Natl. Acad. Sci. USA 100:10977-10982.
21. Harrington, P. R., J. A. Nelson, K. M. Kitrinos, and R. Swanstrom. 2007. Independent evolution of human immunodeficiency virus type 1 env V1/V2 and V4/V5 hypervariable regions during chronic infection. J. Virol. 81:5413-5417.
22. Harrowe, G., and C. Cheng-Mayer. 1995. Amino acid substitutions in the V3 loop are responsible for adaptation to growth in transformed T-cell lines of a primary human immunodeficiency virus type 1. Virology 210:490-494.
23. Hartley, O., H. Gaertner, J. Wilken, D. Thompson, R. Fish, A. Ramos, C. Pastore, B. Dufour, F. Cerini, A. Melotti, N. Heveker, L. Picard, M. Alizon, D. Mosier, S. Kent, and R. Offord. 2004. Medicinal chemistry applied to a synthetic protein: development of highly potent HIV entry inhibitors. Proc. Natl. Acad. Sci. USA 101:16460-16465.
24. Hartley, O., P. J. Klasse, Q. J. Sattentau, and J. P. Moore. 2005. V3: HIV's switch-hitter. AIDS Res. Hum. Retrovir. 21:171-189.
25. Hébert, B., J. Bergeron, E. F. Potworowski, and P. Tijssen. 1993. Increased PCR sensitivity by using paraffin wax as a reaction mix overlay. Mol. Cell. Probes 7:249-252.
26. Herbeck, J. T., D. C. Nickle, G. H. Learn, G. S. Gottlieb, M. E. Curlin, L. Heath, and J. I. Mullins. 2006. Human immunodeficiency virus type 1 env evolves toward ancestral states upon transmission to a new host. J. Virol. 80:1637-1644.
27. Ho, S. H., S. Tasca, L. Shek, A. Li, A. Gettie, J. Blanchard, D. Boden, and C. Cheng-Mayer. 2007. Coreceptor switch in R5-tropic simian/human immunodeficiency virus-infected macaques. J. Virol. 81:8621-8633.
28. Hu, Q. X., A. P. Barry, Z. X. Wang, S. M. Connolly, S. C. Peiper, and M. L. Greenberg. 2000. Evolution of the human immunodeficiency virus type 1 envelope during infection reveals molecular corollaries of specificity for coreceptor utilization and AIDS pathogenesis. J. Virol. 74:11858-11872.
29. Huang, W., S. H. Eshleman, J. Toma, S. Fransen, E. Stawiski, E. E. Paxinos, J. M. Whitcomb, A. M. Young, D. Donnell, F. Mmiro, P. Musoke, L. A. Guay, J. B. Jackson, N. T. Parkin, and C. J. Petropoulos. 2007. Coreceptor tropism in human immunodeficiency virus type 1 subtype D: high prevalence of CXCR4 tropism and heterogeneous composition of viral populations. J. Virol. 81:7885-7893.
30. Hwang, S. S., T. J. Boyle, H. K. Lyerly, and B. R. Cullen. 1991. Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 253:71-74.
31. Jensen, M. A., F. S. Li, A. B. van 't Wout, D. C. Nickle, D. Shriner, H. X. He, S. McLaughlin, R. Shankarappa, J. B. Margolick, and J. I. Mullins. 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.
32. Karlsson, I., L. Antonsson, Y. Shi, M. Oberg, A. Karlsson, J. Albert, B. Olde, C. Owman, M. Jansson, and E. M. Fenyo. 2004. Coevolution of RANTES sensitivity and mode of CCR5 receptor use by human immunodeficiency virus type 1 of the R5 phenotype. J. Virol. 78:11807-11815.
33. Kaslow, R. A., D. G. Ostrow, R. Detels, J. P. Phair, B. F. Polk, and C. R. Rinaldo, Jr. 1987. The Multicenter AIDS Cohort Study: rationale, organization, and selected characteristics of the participants. Am. J. Epidemiol. 126:310-318.
34. Kiselyeva, Y., R. Nedellec, A. Ramos, C. Pastore, L. B. Margolis, and D. E. Mosier. 2007. Evolution of CXCR4-using human immunodeficiency virus type 1 SF162 is associated with two unique envelope mutations. J. Virol. 81:3657-3661.
35. Koot, M., A. B. van 't Wout, N. A. Kootstra, R. E. de Goede, M. Tersmette, and H. Schuitemaker. 1996. Relation between changes in cellular load, evolution of viral phenotype, and the clonal composition of virus populations in the course of human immunodeficiency virus type 1 infection. J. Infect. Dis. 173:349-354.
36. Korber, B. T. M., B. Brander, B. F. Haynes, R. Koup, J. P. Moore, B. D. Walker, and D. I. Watkins (ed.). 2006-2007. HIV molecular immunology, vol. LA-UR 07-4752. Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, NM.
37. Kozak, S. L., J. M. Heard, and D. Kabat. 2002. Segregation of CD4 and CXCR4 into distinct lipid microdomains in T lymphocytes suggests a mechanism for membrane destabilization by human immunodeficiency virus. J. Virol. 76:1802-1815.
38. Kozak, S. L., E. J. Platt, N. Madani, F. E. Ferro, Jr., K. Peden, and D. Kabat. 1997. CD4, CXCR-4, and CCR-5 dependencies for infections by primary patient and laboratory-adapted isolates of human immunodeficiency virus type 1. J. Virol. 71:873-882.
39. Kuiken, C. L., J. J. de Jong, E. Baan, W. Keulen, M. Tersmette, and J. Goudsmit. 1992. Evolution of the V3 envelope domain in proviral sequences and isolates of human immunodeficiency virus type 1 during transition of the viral biological phenotype. J. Virol. 66:4622-4627.
40. 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.
41. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
42. Learn, G. H., D. Muthui, S. J. Brodie, T. Zhu, K. Diem, J. I. Mullins, and L. Corey. 2002. Virus population homogenization following acute human immunodeficiency virus type 1 infection. J. Virol. 76:11953-11959.
43. Liu, Y., J. McNevin, J. Cao, H. Zhao, I. Genowati, K. Wong, S. McLaughlin, M. D. McSweyn, K. Diem, C. E. Stevens, J. Maenza, H. He, D. C. Nickle, D. Shriner, S. E. Holte, A. C. Collier, L. Corey, M. J. McElrath, and J. I. Mullins. 2006. Selection on the human immunodeficiency virus type 1 proteome following primary infection. J. Virol. 80:9519-9529.
44. Long, E. M., H. L. Martin, Jr., J. K. Kreiss, S. M. Rainwater, L. Lavreys, D. J. Jackson, J. Rakwar, K. Mandaliya, and J. Overbaugh. 2000. Gender differences in HIV-1 diversity at time of infection. Nat. Med. 6:71-75.
45. Low, A. J., D. Marchant, C. J. Brumme, Z. L. Brumme, W. Dong, T. Sing, R. S. Hogg, J. S. Montaner, V. Gill, P. K. Cheung, and P. R. Harrigan. 2008. CD4-dependent characteristics of coreceptor use and HIV type 1 V3 sequence in a large population of therapy-naive individuals. AIDS Res. Hum. Retrovir. 24:219-228.
46. Mansky, L. M., and H. M. Temin. 1995. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J. Virol. 69:5087-5094.
47. Moyle, G. J., A. Wildfire, S. Mandalia, H. Mayer, J. Goodrich, J. Whitcomb, and B. G. Gazzard. 2005. Epidemiology and predictive factors for chemokine receptor use in HIV-1 infection. J. Infect. Dis. 191:866-872.
48. Overbaugh, J., and C. R. Bangham. 2001. Selection forces and constraints on retroviral sequence variation. Science 292:1106-1109.
49. Pastore, C., R. Nedellec, A. Ramos, O. Hartley, J. L. Miamidian, J. D. Reeves, and D. E. Mosier. 2007. Conserved changes in envelope function during human immunodeficiency virus type 1 coreceptor switching. J. Virol. 81:8165-8179.
50. Pastore, C., R. Nedellec, A. Ramos, S. Pontow, L. Ratner, and D. E. Mosier. 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.
51. Pastore, C., G. R. Picchio, F. Galimi, R. Fish, O. Hartley, R. E. Offord, and D. E. Mosier. 2003. Two mechanisms for human immunodeficiency virus type 1 inhibition by N-terminal modifications of RANTES. Antimicrob. Agents Chemother. 47:509-517.
52. Pastore, C., A. Ramos, and D. E. Mosier. 2004. Intrinsic obstacles to human immunodeficiency virus type 1 coreceptor switching. J. Virol. 78:7565-7574.
53. Patel, M. B., N. G. Hoffman, and R. Swanstrom. 2008. Subtype-specific conformational differences within the V3 region of subtype B and subtype C human immunodeficiency virus type 1 Env proteins. J. Virol. 82:903-916.
54. Peeters, M., R. Vincent, J. L. Perret, M. Lasky, D. Patrel, F. Liegeois, V. Courgnaud, R. Seng, T. Matton, S. Molinier, and E. Delaporte. 1999. Evidence for differences in MT2 cell tropism according to genetic subtypes of HIV-1: syncytium-inducing variants seem rare among subtype C HIV-1 viruses. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 20:115-121.
55. Peters, P. J., J. Bhattacharya, S. Hibbitts, M. T. Dittmar, G. Simmons, J. Bell, P. Simmonds, and P. R. Clapham. 2004. Biological analysis of human immunodeficiency virus type 1 R5 envelopes amplified from brain and lymph node tissues of AIDS patients with neuropathology reveals two distinct tropism phenotypes and identifies envelopes in the brain that confer an enhanced tropism and fusigenicity for macrophages. J. Virol. 78:6915-6926.
56. Ping, L. H., J. A. Nelson, I. F. Hoffman, J. Schock, S. L. Lamers, M. Goodman, P. Vernazza, P. Kazembe, M. Maida, D. Zimba, M. M. Goodenow, J. J. Eron, Jr., S. A. Fiscus, M. S. Cohen, and R. Swanstrom. 1999. Characterization of V3 sequence heterogeneity in subtype C human immunodeficiency virus type 1 isolates from Malawi: underrepresentation of X4 variants. J. Virol. 73:6271-6281.
57. Rinaldo, C. R., Jr., P. Gupta, X. L. Huang, Z. Fan, J. I. Mullins, S. Gange, H. Farzadegan, R. Shankarappa, A. Munoz, and J. B. Margolick. 1998. Anti-HIV type 1 memory cytotoxic T lymphocyte responses associated with changes in CD4+ T cell numbers in progression of HIV type 1 infection. AIDS Res. Hum. Retrovir. 14:1423-1433.
58. Rolland, M., C. Brander, D. C. Nickle, J. T. Herbeck, G. S. Gottlieb, M. S. Campbell, B. S. Maust, and J. I. Mullins. 2007. HIV-1 over time: fitness loss or robustness gain? Nat. Rev. Microbiol. 5:C1.
59. Sagar, M., E. Kirkegaard, E. M. Long, C. Celum, S. Buchbinder, E. S. Daar, and J. Overbaugh. 2004. Human immunodeficiency virus type 1 (HIV-1) diversity at time of infection is not restricted to certain risk groups or specific HIV-1 subtypes. J. Virol. 78:7279-7283.
60. Schuitemaker, H., M. Koot, N. A. Kootstra, M. W. Dercksen, R. E. de Goede, R. P. van Steenwijk, J. M. Lange, J. K. 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 population. J. Virol. 66:1354-1360.
61. Shankarappa, R., J. B. Margolick, S. J. Gange, A. G. Rodrigo, D. Upchurch, H. Farzadegan, P. Gupta, C. R. Rinaldo, G. H. Learn, X. He, X. L. Huang, and J. I. Mullins. 1999. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73:10489-10502.
62. Shriner, D., A. G. Rodrigo, D. C. Nickle, and J. I. Mullins. 2004. Pervasive genomic recombination of HIV-1 in vivo. Genetics 167:1573- 1583.
63. Smyth, R. J., Y. Yi, A. Singh, and R. G. Collman. 1998. Determinants of entry cofactor utilization and tropism in a dualtropic human immunodeficiency virus type 1 primary isolate. J. Virol. 72:4478-4484.
64. Sougrat, R., A. Bartesaghi, J. D. Lifson, A. E. Bennett, J. W. Bess, D. J. Zabransky, and S. Subramaniam. 2007. Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog. 3:e63.
65. van Rij, R. P., H. Blaak, J. A. Visser, M. Brouwer, R. Rientsma, S. Broersen, A. M. de Roda Husman, and H. Schuitemaker. 2000. Differential coreceptor expression allows for independent evolution of non-syncytium-inducing and syncytium-inducing HIV-1. J. Clin. Investig. 106:1039-1052.
66. van Rij, R. P., M. D. Hazenberg, B. H. van Benthem, S. A. Otto, M. Prins, F. Miedema, and H. Schuitemaker. 2003. Early viral load and CD4+ T cell count, but not percentage of CCR5+ or CXCR4+ CD4+ T cells, are associated with R5-to-X4 HIV type 1 virus evolution. AIDS Res. Hum. Retrovir. 19:389-398.
67. Wang, R. F., and J. I. Mullins. 1995. Mammalian cell/vaccinia virus expression vectors with increased stability of retroviral sequences in Escherichia coli: production of feline immunodeficiency virus envelope protein. Gene 153:197-202.
68. Westby, M., M. Lewis, J. Whitcomb, M. Youle, A. L. Pozniak, I. T. James, T. M. Jenkins, M. Perros, and E. van der Ryst. 2006. Emergence of CXCR4-using human immunodeficiency virus type 1 (HIV-1) variants in a minority of HIV-1-infected patients following treatment with the CCR5 antagonist maraviroc is from a pretreatment CXCR4-using virus reservoir. J. Virol. 80:4909-4920.
69. Whitcomb, J. M., W. Huang, S. Fransen, K. Limoli, J. Toma, T. Wrin, C. Chappey, L. D. Kiss, E. E. Paxinos, and C. J. Petropoulos. 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.
70. Wilke, C. O., J. L. Wang, C. Ofria, R. E. Lenski, and C. Adami. 2001. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412:331-333.
71. Wilkin, T. J., Z. Su, D. R. Kuritzkes, M. Hughes, C. Flexner, R. Gross, E. Coakley, W. Greaves, C. Godfrey, P. R. Skolnik, J. Timpone, B. Rodriguez, and R. M. Gulick. 2007. HIV type 1 chemokine coreceptor use among antiretroviral-experienced patients screened for a clinical trial of a CCR5 inhibitor: AIDS Clinical Trial Group A5211. Clin. Infect. Dis. 44:591-595.
72. Wolinsky, S. M., C. M. Wike, B. T. Korber, C. Hutto, W. P. Parks, L. L. Rosenblum, K. J. Kunstman, M. R. Furtado, and J. L. Munoz. 1992. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 255:1134-1137.
73. Yi, Y., F. Shaheen, and R. G. Collman. 2005. Preferential use of CXCR4 by R5X4 human immunodeficiency virus type 1 isolates for infection of primary lymphocytes. J. Virol. 79:1480-1486.
74. Yi, Y., A. Singh, F. Shaheen, A. Louden, C. Lee, and R. G. Collman. 2003. Contrasting use of CCR5 structural determinants by R5 and R5X4 variants within a human immunodeficiency virus type 1 primary isolate quasispecies. J. Virol. 77:12057-12066.
75. Zhang, L. Q., P. MacKenzie, A. Cleland, E. C. Holmes, A. J. Brown, and P. Simmonds. 1993. Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. J. Virol. 67:3345-3356.
76. Zhang, M., B. Gaschen, W. Blay, B. Foley, N. Haigwood, C. Kuiken, and B. Korber. 2004. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14:1229-1246.
77. Zhu, T., H. Mo, N. Wang, D. S. Nam, Y. Cao, R. A. Koup, and D. D. Ho. 1993. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261:1179-1181.