Major coexisting human immunodeficiency virus type 1 env gene subpopulations in the peripheral blood are produced by cells with similar turnover rates and show little evidence of genetic compartmentalization

Journal of Virology

Volumn 83, Issue 9, 2009, Pages 4068-4080

  Ince, William L ^a   Harrington, Patrick R ^b   Schnell, Gretja L ^b   Patel Chhabra, Milloni ^b   Burch, Christina L ^a   Menezes, Prema ^a   Price, Richard W ^c   Eron Jr , Joseph J ^a   Swanstrom, Ronald I ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; VIRUS RNA;

ARTICLE; BLOOD; CELL SUBPOPULATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; ENVELOPE GENE; GENE AMPLIFICATION; GENETIC COMPATIBILITY; GENETIC VARIABILITY; HETERODUPLEX ANALYSIS; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HOST CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; PHENOTYPE; PRIORITY JOURNAL; TARGET CELL; VIRUS GENE;

GENE PRODUCTS, ENV; HIV INFECTIONS; HIV-1; HUMANS; PHYLOGENY; RECEPTORS, CCR5; RECEPTORS, CXCR4;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 66149133580     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02486-08     Document Type: Article

References (102)

1. Arthos, J., C. Cicala, E. Martinelli, K. Macleod, D. Van Ryk, D. Wei, Z. Xiao, T. D. Veenstra, T. P. Conrad, R. A. Lempicki, S. McLaughlin, M. Pascuccio, R. Gopaul, J. McNally, C. C. Cruz, N. Censoplano, E. Chung, K. N. Reitano, S. Kottilil, D. J. Goode, and A. S. Fauci. 2008. HIV-1 envelope protein binds to and signals through integrin α4β7, the gut mucosal homing receptor for peripheral T cells. Nat. Immunol. 9:301-309.
2. Bjorndal, A., H. Deng, M. Jansson, J. R. Fiore, C. Colognesi, A. Karlsson, J. Albert, G. Scarlatti, D. R. Littman, and E. M. Fenyo. 1997. Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J. Virol. 71:7478-7487. (Pubitemid 27391688)
3. + T cell decline. Proc. Natl. Acad. Sci. USA 97:1269-1274.
4. Blankson, J. N., D. Finzi, T. C. Pierson, B. P. Sabundayo, K. Chadwick, J. B. Margolick, T. C. Quinn, and R. F. Siliciano. 2000. Biphasic decay of latently infected CD4+ T cells in acute human immunodeficiency virus type 1 infection. J. Infect. Dis. 182:1636-1642.
5. Bleul, C. C., L. Wu, J. A. Hoxie, T. A. Springer, and C. R. Mackay. 1997. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. USA 94:1925-1930.
6. Borrow, P., H. Lewicki, X. Wei, M. S. Horwitz, N. Peffer, H. Meyers, J. A. Nelson, J. E. Gairin, B. H. Hahn, M. B. Oldstone, and G. M. Shaw. 1997. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205-211. (Pubitemid 27064706)
7. Burkala, E. J., J. He, J. T. West, C. Wood, and C. K. Petito. 2005. Compartmentalization of HIV-1 in the central nervous system: role of the choroid plexus. AIDS 19:675-684.
8. Cameron, D. W., M. Heath-Chiozzi, S. Danner, C. Cohen, S. Kravcik, C. Maurath, E. Sun, D. Henry, R. Rode, A. Potthoff, J. Leonard, et al. 1998. Randomised placebo-controlled trial of ritonavir in advanced HIV-1 disease. Lancet 351:543-549.
9. Cheynier, R., S. Henrichwark, F. Hadida, E. Pelletier, E. Oksenhendler, B. Autran, and S. Wain-Hobson. 1995. Clonal expansion of T cells and HIV genotypes in microdissected splenic white pulps indicates viral replication in situ and infiltration of HIV-specific cytotoxic T lymphocytes. Adv. Exp. Med. Biol. 374:173-182.
10. Connor, R. I., K. E. Sheridan, D. Ceradini, S. Choe, and N. R. Landau. 1997. Change in coreceptor use coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 185:621-628. (Pubitemid 27098147)
11. Crowe, S., T. Zhu, and W. A. Muller. 2003. The contribution of monocyte infection and trafficking to viral persistence, and maintenance of the viral reservoir in HIV infection. J. Leukoc. Biol. 74:635-641.
12. Delwart, E., M. Magierowska, M. Royz, B. Foley, L. Peddada, R. Smith, C. Heldebrant, A. Conrad, and M. Busch. 2002. Homogeneous quasispecies in 16 out of 17 individuals during very early HIV-1 primary infection. AIDS 16:189-195.
13. Delwart, E. L., J. I. Mullins, P. Gupta, G. H. Learn, Jr., M. Holodniy, D. Katzenstein, B. D. Walker, and M. K. Singh. 1998. Human immunodeficiency virus type 1 populations in blood and semen. J. Virol. 72:617-623. (Pubitemid 28048879)
14. Delwart, E. L., H. W. Sheppard, B. D. Walker, J. Goudsmit, and J. I. Mullins. 1994. Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J. Virol. 68:6672-6683. (Pubitemid 24294918)
15. Diem, K., D. C. Nickle, A. Motoshige, A. Fox, S. Ross, J. I. Mullins, L. Corey, R. W. Coombs, and J. N. Krieger. 2008. Male genital tract compartmentalization of human immunodeficiency virus type 1 (HIV). AIDS Res. Hum. Retrovir. 24:561-571.
16. Edmonson, P. F., and J. I. Mullins. 1992. Efficient amplification of HIV half-genomes from tissue DNA. Nucleic Acids Res. 20:4933.
17. Fouchier, R. A., 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.
18. Frost, S. D., M. J. Dumaurier, S. Wain-Hobson, and A. J. Brown. 2001. Genetic drift and within-host metapopulation dynamics of HIV-1 infection. Proc. Natl. Acad. Sci. USA 98:6975-6980.
19. Frost, S. D., Y. Liu, S. L. Pond, C. Chappey, T. Wrin, C. J. Petropoulos, S. J. Little, and D. D. Richman. 2005. Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. J. Virol. 79:6523-6527. (Pubitemid 40617256)
20. Frost, S. D., T. Wrin, D. M. Smith, S. L. Kosakovsky Pond, Y. Liu, E. Paxinos, C. Chappey, J. Galovich, J. Beauchaine, C. J. Petropoulos, S. J. Little, and D. D. Richman. 2005. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl. Acad. Sci. USA 102:18514-18519.
21. + T cells during infection. J. Virol. 78:7883-7893.
22. + T cells and are potentially resistant to nucleoside reverse transcriptase inhibitors. J. Virol. 80:854-865.
23. Gorry, P. R., J. Taylor, G. H. Holm, A. Mehle, T. Morgan, M. Cayabyab, M. Farzan, H. Wang, J. E. Bell, K. Kunstman, J. P. Moore, S. M. Wolinsky, and D. Gabuzda. 2002. Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J. Virol. 76:6277-6292. (Pubitemid 34556323)
24. Gratton, S., R. Cheynier, M. J. Dumaurier, E. Oksenhendler, and S. Wain-Hobson. 2000. Highly restricted spread of HIV-1 and multiply infected cells within splenic germinal centers. Proc. Natl. Acad. Sci. USA 97:14566-14571.
25. Gray, L., J. Sterjovski, M. Churchill, P. Ellery, N. Nasr, S. R. Lewin, S. M. Crowe, S. L. Wesselingh, A. L. Cunningham, and P. R. Gorry. 2005. Uncoupling coreceptor usage of human immunodeficiency virus type 1 (HIV-1) from macrophage tropism reveals biological properties of CCR5-restricted HIV-1 isolates from patients with acquired immunodeficiency syndrome. Virology 337:384-398.
26. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
27. Gulick, R. M., X. J. Hu, S. A. Fiscus, C. V. Fletcher, R. Haubrich, H. Cheng, E. Acosta, S. W. Lagakos, R. Swanstrom, W. Freimuth, S. Snyder, C. Mills, M. Fischl, C. Pettinelli, and D. Katzenstein. 2000. Randomized study of saquinavir with ritonavir or nelfinavir together with delavirdine, adefovir, or both in human immunodeficiency virus-infected adults with virologic failure on indinavir: AIDS Clinical Trials Group Study 359. J. Infect. Dis. 182: 1375-1384.
28. Haddad, D. N., C. Birch, T. Middleton, D. E. Dwyer, A. L. Cunningham, and N. K. Saksena. 2000. Evidence for late stage compartmentalization of HIV-1 resistance mutations between lymph node and peripheral blood mononuclear cells. Aids 14:2273-2281.
29. Harrington, P. R., M. J. Connell, R. B. Meeker, P. R. Johnson, and R. Swanstrom. 2007. Dynamics of simian immunodeficiency virus populations in blood and cerebrospinal fluid over the full course of infection. J. Infect. Dis. 196:1058-1067. (Pubitemid 47580301)
30. Harrington, P. R., D. W. Haas, K. Ritola, and R. Swanstrom. 2005. Compartmentalized human immunodeficiency virus type 1 present in cerebrospinal fluid is produced by short-lived cells. J. Virol. 79:7959-7966. (Pubitemid 40853500)
31. 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.
32. He, J., S. Choe, R. Walker, P. Di Marzio, D. O. Morgan, and N. R. Landau. 1995. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69:6705-6711.
33. Henderson, G. J., N. G. Hoffman, L. H. Ping, S. A. Fiscus, I. F. Hoffman, K. M. Kitrinos, T. Banda, F. E. Martinson, P. N. Kazembe, D. A. Chilongozi, M. S. Cohen, and R. Swanstrom. 2004. HIV-1 populations in blood and breast milk are similar. Virology 330:295-303.
34. Ho, D. D., A. U. Neumann, A. S. Perelson, W. Chen, J. M. Leonard, and M. Markowitz. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123-126.
35. Hudson, R. R., D. D. Boos, and N. L. Kaplan. 1992. A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 9:138-151.
36. 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.
37. Katoh, K., and H. Toh. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9:286-298.
38. Keele, B. F., E. E. Giorgi, J. F. Salazar-Gonzalez, J. M. Decker, K. T. Pham, M. G. Salazar, C. Sun, T. Grayson, S. Wang, H. Li, X. Wei, C. Jiang, J. L. Kirchherr, F. Gao, J. A. Anderson, L. H. Ping, R. Swanstrom, G. D. Tomaras, W. A. Blattner, P. A. Goepfert, J. M. Kilby, M. S. Saag, E. L. Delwart, M. P. Busch, M. S. Cohen, D. C. Montefiori, B. F. Haynes, B. Gaschen, G. S. Athreya, H. Y. Lee, N. Wood, C. Seoighe, A. S. Perelson, T. Bhattacharya, B. T. Korber, B. H. Hahn, and G. M. Shaw. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 105:7552-7557.
39. Kemal, K. S., B. Foley, H. Burger, K. Anastos, H. Minkoff, C. Kitchen, S. M. Philpott, W. Gao, E. Robison, S. Holman, C. Dehner, S. Beck, W. A. Meyer III, A. Landay, A. Kovacs, J. Bremer, and B. Weiser. 2003. HIV-1 in genital tract and plasma of women: compartmentalization of viral sequences, coreceptor usage, and glycosylation. Proc. Natl. Acad. Sci. USA 100:12972-12977.
40. Kirchherr, J. L., X. Lu, W. Kasongo, V. Chalwe, L. Mwananyanda, R. M. Musonda, S. M. Xia, R. M. Scearce, H. X. Liao, D. C. Montefiori, B. F. Haynes, and F. Gao. 2007. High throughput functional analysis of HIV-1 env genes without cloning. J. Virol. Methods 143:104-111.
41. Kitrinos, K. M., N. G. Hoffman, J. A. 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. (Pubitemid 36666875)
42. Koot, M., R. van Leeuwen, R. E. de Goede, I. P. Keet, S. Danner, J. K. Eeftinck Schattenkerk, P. Reiss, M. Tersmette, J. M. Lange, and H. Schuitemaker. 1999. Conversion rate towards a syncytium-inducing (SI) phenotype during different stages of human immunodeficiency virus type 1 infection and prognostic value of SI phenotype for survival after AIDS diagnosis. J. Infect. Dis. 179:254-258. (Pubitemid 29028366)
43. Korber, B. T., K. J. Kunstman, B. K. Patterson, M. Furtado, M. M. McEvilly, R. Levy, and S. M. Wolinsky. 1994. Genetic differences between blood- and brain-derived viral sequences from human immunodeficiency virus type 1-infected patients: evidence of conserved elements in the V3 region of the envelope protein of brain-derived sequences. J. Virol. 68:7467-7481.
44. Koup, R. A., J. T. Safrit, Y. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
45. 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. (Pubitemid 35304295)
46. Lee, B., M. Sharron, L. J. Montaner, D. Weissman, and R. W. Doms. 1999. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc. Natl. Acad. Sci. USA 96:5215-5220.
47. + T cells of patients with discontinued therapy. J. Leukoc. Biol. 80:1118-1126.
48. Malkevitch, N., D. H. McDermott, Y. Yi, J. C. Grivel, D. Schols, E. De Clercq, P. M. Murphy, S. Glushakova, R. G. Collman, and L. Margolis. 2001. Coreceptor choice and T cell depletion by R5, X4, and R5X4 HIV-1 variants in CCR5-deficient (CCR5Δ32) and normal human lymphoid tissue. Virology 281:239-247.
49. Markowitz, M., M. Louie, A. Hurley, E. Sun, M. Di Mascio, A. S. Perelson, and D. D. Ho. 2003. A novel antiviral intervention results in more accurate assessment of human immunodeficiency virus type 1 replication dynamics and T-cell decay in vivo. J. Virol. 77:5037-5038.
50. Martin, D. P., D. Posada, K. A. Crandall, and C. Williamson. 2005. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res. Hum. Retrovir. 21:98-102. (Pubitemid 40179806)
51. Mild, M., J. Esbjornsson, E. M. Fenyo, and P. Medstrand. 2007. Frequent intrapatient recombination between human immunodeficiency virus type 1 R5 and X4 envelopes: implications for coreceptor switch. J. Virol. 81:3369-3376.
52. Mitsuya, Y., V. Varghese, C. Wang, T. F. Liu, S. P. Holmes, P. Jayakumar, B. Gharizadeh, M. Ronaghi, D. Klein, W. J. Fessel, and R. W. Shafer. 2008. Minority human immunodeficiency virus type 1 variants in antiretroviral-naive persons with reverse transcriptase codon 215 revertant mutations. J. Virol. 82:10747-10755. (Pubitemid 352691166)
53. Murray, J. M., S. Emery, A. D. Kelleher, M. Law, J. Chen, D. J. Hazuda, B. Y. Nguyen, H. Teppler, and D. A. Cooper. 2007. Antiretroviral therapy with the integrase inhibitor raltegravir alters decay kinetics of HIV, significantly reducing the second phase. AIDS 21:2315-2321.
54. Nelson, J. A., F. Baribaud, T. Edwards, and R. Swanstrom. 2000. Patterns of changes in human immunodeficiency virus type 1 V3 sequence populations late in infection. J. Virol. 74:8494-8501. (Pubitemid 30666700)
55. Nicholson, J. K., S. W. Browning, R. L. Hengel, E. Lew, L. E. Gallagher, D. Rimland, and J. S. McDougal. 2001. CCR5 and CXCR4 expression on memory and naive T cells in HIV-1 infection and response to highly active antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 27:105-115. (Pubitemid 32595160)
56. Ohagen, A., A. Devitt, K. J. Kunstman, P. R. Gorry, P. P. Rose, B. Korber, J. Taylor, R. Levy, R. L. Murphy, S. M. Wolinsky, and D. Gabuzda. 2003. Genetic and functional analysis of full-length human immunodeficiency virus type 1 env genes derived from brain and blood of patients with AIDS. J. Virol. 77:12336-12345.
57. + T cells are infected in human immunodeficiency virus type 1-infected individuals. J. Virol. 73:6430-6435.
58. Ostrowski, M. A., S. J. Justement, A. Catanzaro, C. A. Hallahan, L. A. Ehler, S. B. Mizell, P. N. Kumar, J. A. Mican, T. W. Chun, and A. S. Fauci. 1998. Expression of chemokine receptors CXCR4 and CCR5 in HIV-1-infected and uninfected individuals. J. Immunol. 161:3195-3201. (Pubitemid 28425749)
59. Ostrowski, M. A., D. C. Krakauer, Y. Li, S. J. Justement, G. Learn, L. A. Ehler, S. K. Stanley, M. Nowak, and A. S. Fauci. 1998. Effect of immune activation on the dynamics of human immunodeficiency virus replication and on the distribution of viral quasispecies. J. Virol. 72:7772-7784. (Pubitemid 28421767)
60. Overbaugh, J., R. J. Anderson, J. O. Ndinya-Achola, and J. K. Kreiss. 1996. Distinct but related human immunodeficiency virus type 1 variant populations in genital secretions and blood. AIDS Res. Hum. Retrovir. 12:107-115. (Pubitemid 26039709)
61. Palmer, S., M. Kearney, F. Maldarelli, E. K. Halvas, C. J. Bixby, H. Bazmi, D. Rock, J. Falloon, R. T. Davey, Jr., R. L. Dewar, J. A. Metcalf, S. Hammer, J. W. Mellors, and J. M. Coffin. 2005. Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J. Clin. Microbiol. 43: 406-413.
62. Perelson, A. S., P. Essunger, Y. Cao, M. Vesanen, A. Hurley, K. Saksela, M. Markowitz, and D. D. Ho. 1997. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387:188-191.
63. Perelson, A. S., A. U. Neumann, M. Markowitz, J. M. Leonard, and D. D. Ho. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271:1582-1586.
64. 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. (Pubitemid 38781530)
65. Philpott, S., H. Burger, C. Tsoukas, B. Foley, K. Anastos, C. Kitchen, and B. Weiser. 2005. Human immunodeficiency virus type 1 genomic RNA sequences in the female genital tract and blood: compartmentalization and intrapatient recombination. J. Virol. 79:353-363.
66. Philpott, S., B. Weiser, K. Anastos, C. M. Kitchen, E. Robison, W. A. Meyer, 3rd, H. S. Sacks, U. Mathur-Wagh, C. Brunner, and H. Burger. 2001. Preferential suppression of CXCR4-specific strains of HIV-1 by antiviral therapy. J. Clin. Investig. 107:431-438.
67. Platt, E. J., K. Wehrly, S. E. Kuhmann, B. Chesebro, and D. Kabat. 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. (Pubitemid 28175522)
68. Poles, M. A., W. J. Boscardin, J. Elliott, P. Taing, M. M. Fuerst, I. McGowan, S. Brown, and P. A. Anton. 2006. Lack of decay of HIV-1 in gut-associated lymphoid tissue reservoirs in maximally suppressed individuals. J. Acquir. Immune Defic. Syndr. 43:65-68. (Pubitemid 44306490)
69. Pond, S. L., S. D. Frost, and S. V. Muse. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
70. Poss, M., A. G. Rodrigo, J. J. Gosink, G. H. Learn, D. de Vange Panteleeff, H. L. Martin, Jr., J. Bwayo, J. K. Kreiss, and J. Overbaugh. 1998. Evolution of envelope sequences from the genital tract and peripheral blood of women infected with clade A human immunodeficiency virus type 1. J. Virol. 72:8240-8251. (Pubitemid 28421821)
71. Resch, W., N. Parkin, E. L. Stuelke, T. Watkins, and R. Swanstrom. 2001. A multiple-site-specific heteroduplex tracking assay as a tool for the study of viral population dynamics. Proc. Natl. Acad. Sci. USA 98:176-181.
72. Rich, E. A., I. S. Chen, J. A. Zack, M. L. Leonard, and W. A. O'Brien. 1992. Increased susceptibility of differentiated mononuclear phagocytes to productive infection with human immunodeficiency virus-1 (HIV-1). J. Clin. Investig. 89:176-183.
73. Ritola, K., K. Robertson, S. A. Fiscus, C. Hall, and R. Swanstrom. 2005. Increased human immunodeficiency virus type 1 (HIV-1) env compartmentalization in the presence of HIV-1-associated dementia. J. Virol. 79:10830-10834.
74. Ross, H. A., and A. G. Rodrigo. 2002. Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration. J. Virol. 76:11715-11720. (Pubitemid 35231326)
75. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
76. Salazar-Gonzalez, J. F., E. Bailes, K. T. Pham, M. G. Salazar, M. B. Guffey, B. F. Keele, C. A. Derdeyn, P. Farmer, E. Hunter, S. Allen, O. Manigart, J. Mulenga, J. A. Anderson, R. Swanstrom, B. F. Haynes, G. S. Athreya, B. T. Korber, P. M. Sharp, G. M. Shaw, and B. H. Hahn. 2008. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J. Virol. 82:3952-3970.
77. Salemi, M., B. R. Burkhardt, R. R. Gray, G. Ghaffari, J. W. Sleasman, and M. M. Goodenow. 2007. Phylodynamics of HIV-1 in lymphoid and non-lymphoid tissues reveals a central role for the thymus in emergence of CXCR4-using quasispecies. PLoS ONE 2:e950.
78. Salminen, M. O., J. K. Carr, D. S. Burke, and F. E. McCutchan. 1995. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res. Hum. Retrovir. 11:1423-1425.
79. Schnell, G., W. L. Ince, and R. Swanstrom. 2008. Identification and recovery of minor HIV-1 variants using the heteroduplex tracking assay and biotinylated probes. Nucleic Acids Res. 36:e146.
80. Sedaghat, A. R., J. B. Dinoso, L. Shen, C. O. Wilke, and R. F. Siliciano. 2008. Decay dynamics of HIV-1 depend on the inhibited stages of the viral life cycle. Proc. Natl. Acad. Sci. USA 105:4832-4837.
81. Shapshak, P., D. M. Segal, K. A. Crandall, R. K. Fujimura, B. T. Zhang, K. Q. Xin, K. Okuda, C. K. Petito, C. Eisdorfer, and K. Goodkin. 1999. Independent evolution of HIV type 1 in different brain regions. AIDS Res. Hum. Retrovir. 15:811-820. (Pubitemid 29265011)
82. Simmonds, P., P. Balfe, C. A. Ludlam, J. O. Bishop, and A. J. Brown. 1990. Analysis of sequence diversity in hypervariable regions of the external glycoprotein of human immunodeficiency virus type 1. J. Virol. 64:5840-5850.
83. Slatkin, M., and W. P. Maddison. 1989. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 123:603-613.
84. Sonza, S., A. Maerz, N. Deacon, J. Meanger, J. Mills, and S. Crowe. 1996. Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes. J. Virol. 70:3863-3869. (Pubitemid 26157366)
85. Stalmeijer, E. H., R. P. Van Rij, B. Boeser-Nunnink, J. A. Visser, M. A. Naarding, D. Schols, and H. Schuitemaker. 2004. In vivo evolution of X4 human immunodeficiency virus type 1 variants in the natural course of infection coincides with decreasing sensitivity to CXCR4 antagonists. J. Virol. 78:2722-2728.
86. Stanley, S. K., M. A. Ostrowski, J. S. Justement, K. Gantt, S. Hedayati, M. Mannix, K. Roche, D. J. Schwartzentruber, C. H. Fox, and A. S. Fauci. 1996. Effect of immunization with a common recall antigen on viral expression in patients infected with human immunodeficiency virus type 1. N. Engl. J. Med. 334:1222-1230. (Pubitemid 26137993)
87. Staprans, S., N. Marlowe, D. Glidden, T. Novakovic-Agopian, R. M. Grant, M. Heyes, F. Aweeka, S. Deeks, and R. W. Price. 1999. Time course of cerebrospinal fluid responses to antiretroviral therapy: evidence for variable compartmentalization of infection. AIDS 13:1051-1061.
88. Stevenson, M., T. L. Stanwick, M. P. Dempsey, and C. A. Lamonica. 1990. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J. 9:1551-1560. (Pubitemid 20137012)
89. Thomas, E. R., R. L. Dunfee, J. Stanton, D. Bogdan, J. Taylor, K. Kunstman, J. E. Bell, S. M. Wolinsky, and D. Gabuzda. 2007. Macrophage entry mediated by HIV Envs from brain and lymphoid tissues is determined by the capacity to use low CD4 levels and overall efficiency of fusion. Virology 360:105-119.
90. van Marle, G., M. J. Gill, D. Kolodka, L. McManus, T. Grant, and D. L. Church. 2007. Compartmentalization of the gut viral reservoir in HIV-1 infected patients. Retrovirology 4:87.
91. 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.
92. van Rij, R. P., M. Worobey, J. A. Visser, and H. Schuitemaker. 2003. Evolution of R5 and X4 human immunodeficiency virus type 1 gag sequences in vivo: evidence for recombination. Virology 314:451-459.
93. van't Wout, A. B., N. A. Kootstra, G. A. Mulder-Kampinga, N. Albrecht-van Lent, H. J. Scherpbier, J. Veenstra, K. Boer, R. A. Coutinho, F. Miedema, and H. Schuitemaker. 1994. Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J. Clin. Investig. 94:2060-2067.
94. + T cell depletion and viral replication in SIV infection. Science 280:427-431.
95. Walter, B. L., K. Wehrly, R. Swanstrom, E. Platt, D. Kabat, and B. Chesebro. 2005. Role of low CD4 levels in the influence of human immunodeficiency virus type 1 envelope V1 and V2 regions on entry and spread in macrophages. J. Virol. 79:4828-4837. (Pubitemid 40464233)
96. Wei, X., S. K. Ghosh, M. E. Taylor, V. A. Johnson, E. A. Emini, P. Deutsch, J. D. Lifson, S. Bonhoeffer, M. A. Nowak, B. H. Hahn, et al. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373:117-122.
97. Wolinsky, S. M., B. T. Korber, A. U. Neumann, M. Daniels, K. J. Kunstman, A. J. Whetsell, M. R. Furtado, Y. Cao, D. D. Ho, and J. T. Safrit. 1996. Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 272:537-542.
98. 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. (Pubitemid 40459095)
99. 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. (Pubitemid 23143709)
100. + T cells. Science 286:1353-1357.
101. 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.
102. + monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy. J. Virol. 76:707-716.