Identification of interdependent variables that influence coreceptor switch in R5 SHIVSF162P3N-infected macaques

Retrovirology

Volumn 9, Issue , 2012, Pages

  Zhuang, Ke ^a   Finzi, Andres ^b   Toma, Jonathan ^c   Frantzell, Arne ^c   Huang, Wei ^c   Sodroski, Joseph ^d   Cheng Mayer, Cecilia ^a  

^a AARON DIAMOND AIDS RESEARCH CENTER   (United States)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MONOGRAM BIOSCIENCES   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CD4 binding; Coreceptor switch; Macrophage infection; R5 SHIV

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; BINDING COMPETITION; BINDING SITE; CD4 LYMPHOCYTE COUNT; CELLULAR PARAMETERS; CONTROLLED STUDY; CORECEPTOR SWITCH; DISEASE COURSE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNE SYSTEM; LENTIVIRUS INFECTION; MACACA; MACROPHAGE; NONHUMAN; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN DOMAIN; SEROCONVERSION; SIMIAN HUMAN IMMUNODEFICIENCY VIRUS INFECTION; TARGET CELL; VIRAL TROPISM; VIRUS CELL INTERACTION; VIRUS LOAD; VIRUS NEUTRALIZATION; VIRUS REPLICATION;

ANIMALS; ANTIGENS, CD4; CD4 LYMPHOCYTE COUNT; HIV ENVELOPE PROTEIN GP120; HUMANS; MACACA; MACROPHAGES; PROTEIN BINDING; RECEPTORS, CCR5; RECEPTORS, CXCR4; RECEPTORS, HIV; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIRAL TROPISM; VIRUS INTERNALIZATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; MACACA MULATTA; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84870897823     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-106     Document Type: Article

References (89)

1. Berger EA, Murphy PM, Farber JM. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 1999, 17:657-700. 10.1146/annurev.immunol.17.1.657, 10358771.
2. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci USA 2008, 105:7552-7557. 10.1073/pnas.0802203105, 2387184, 18490657.
3. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, Decker JM, Wang S, Baalwa J, Kraus MH, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 2009, 206:1273-1289. 10.1084/jem.20090378, 2715054, 19487424.
4. Li H, Bar KJ, Wang S, Decker JM, Chen Y, Sun C, Salazar-Gonzalez JF, Salazar MG, Learn GH, Morgan CJ, et al. High multiplicity infection by HIV-1 in Men who have sex with Men. PLoS Pathog 2010, 6:e1000890. 10.1371/journal.ppat.1000890, 2869329, 20485520.
5. Koot M, Keet IP, Vos AH, de Goede RE, Roos MT, Coutinho RA, Miedema F, Schellekens PT, Tersmette M. Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. Ann Intern Med 1993, 118:681-688.
6. Scarlatti G, Tresoldi E, Bjorndal A, Fredriksson R, Colognesi C, Deng HK, Malnati MS, Plebani A, Siccardi AG, Littman DR, et al. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat Med 1997, 3:1259-1265. 10.1038/nm1197-1259, 9359702.
7. Cocchi F, DeVico AL, Garzino-Demo A, Cara A, Gallo RC, Lusso P. The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection. Nat Med 1996, 2:1244-1247. 10.1038/nm1196-1244, 8898753.
8. Fouchier RA, Groenink M, Kootstra NA, Tersmette M, Huisman HG, Miedema F, Schuitemaker H. Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J Virol 1992, 66:3183-3187. 241084, 1560543.
9. Moore JP, Kitchen SG, Pugach P, Zack JA. The CCR5 and CXCR4 coreceptors-central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. AIDS Res Hum Retroviruses 2004, 20:111-126. 10.1089/088922204322749567, 15000703.
10. Regoes RR, Bonhoeffer S. The HIV coreceptor switch: a population dynamical perspective. Trends Microbiol 2005, 13:269-277. 10.1016/j.tim.2005.04.005, 15936659.
11. Gulick RM, Su Z, Flexner C, Hughes MD, Skolnik PR, Wilkin TJ, Gross R, Krambrink A, Coakley E, Greaves WL, et al. Phase 2 study of the safety and efficacy of vicriviroc, a CCR5 inhibitor, in HIV-1-Infected, treatment-experienced patients: AIDS clinical trials group 5211. J Infect Dis 2007, 196:304-312. 10.1086/518797, 17570119.
12. Lalezari J, Thompson M, Kumar P, Piliero P, Davey R, Patterson K, Shachoy-Clark A, Adkison K, Demarest J, Lou Y, et al. Antiviral activity and safety of 873140, a novel CCR5 antagonist, during short-term monotherapy in HIV-infected adults. AIDS 2005, 19:1443-1448. 10.1097/01.aids.0000183633.06580.8a, 16135896.
13. Westby M, Lewis M, Whitcomb J, Youle M, Pozniak AL, James IT, Jenkins TM, Perros M, van der Ryst E. 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 2006, 80:4909-4920. 10.1128/JVI.80.10.4909-4920.2006, 1472081, 16641282.
14. Saag M, Goodrich J, Fatkenheuer G, Clotet B, Clumeck N, Sullivan J, Westby M, van der Ryst E, Mayer H. A double-blind, placebo-controlled trial of maraviroc in treatment-experienced patients infected with non-R5 HIV-1. J Infect Dis 2009, 199:1638-1647. 10.1086/598965, 19432546.
15. Wilkin TJ, Su Z, Krambrink A, Long J, Greaves W, Gross R, Hughes MD, Flexner C, Skolnik PR, Coakley E, et al. Three-year safety and efficacy of vicriviroc, a CCR5 antagonist, in HIV-1-infected treatment-experienced patients. J Acquir Immune Defic Syndr 2010, 54:470-476. 10.1097/QAI.0b013e3181e2cba0, 2917795, 20672447.
16. Ho SH, Tasca S, Shek L, Li A, Gettie A, Blanchard J, Boden D, Cheng-Mayer C. Coreceptor switch in R5-tropic simian/human immunodeficiency virus-infected macaques. J Virol 2007, 81:8621-8633. 10.1128/JVI.00759-07, 1951359, 17537860.
17. Ren W, Tasca S, Zhuang K, Gettie A, Blanchard J, Cheng-Mayer C. Different tempo and anatomic location of dual-tropic and X4 virus emergence in a model of R5 simian-human immunodeficiency virus infection. J Virol 2010, 84:340-351. 10.1128/JVI.01865-09, 2798429, 19846515.
18. Shakirzyanova M, Tsai L, Ren W, Gettie A, Blanchard J, Cheng-Mayer C. Pathogenic consequences of vaginal infection with CCR5-tropic SHIVSF162P3N. J Virol 2012, 86:9432-42. 10.1128/JVI.00852-12, 22740397.
19. De Jong JJ, De Ronde A, Keulen W, Tersmette M, Goudsmit J. 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 1992, 66:6777-6780. 240176, 1404617.
20. Speck RF, Wehrly K, Platt EJ, Atchison RE, Charo IF, Kabat D, Chesebro B, Goldsmith MA. Selective employment of chemokine receptors as human immunodeficiency virus type 1 coreceptors determined by individual amino acids within the envelope V3 loop. J Virol 1997, 71:7136-7139. 192016, 9261451.
21. Kuiken CL, de Jong JJ, Baan E, Keulen W, Tersmette M, Goudsmit J. 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 1992, 66:4622-4627. 241280, 1602564.
22. Pastore C, Ramos A, Mosier DE. Intrinsic obstacles to human immunodeficiency virus type 1 coreceptor switching. J Virol 2004, 78:7565-7574. 10.1128/JVI.78.14.7565-7574.2004, 434079, 15220431.
23. Tasca S, Ho SH, Cheng-Mayer C. R5X4 viruses are evolutionary, functional, and antigenic intermediates in the pathway of a simian-human immunodeficiency virus coreceptor switch. J Virol 2008, 82:7089-7099. 10.1128/JVI.00570-08, 2446975, 18480460.
24. Shakirzyanova M, Ren W, Zhuang K, Tasca S, Cheng-Mayer C. Fitness disadvantage of transitional intermediates contributes to dynamic change in the infecting-virus population during coreceptor switch in R5 simian/human immunodeficiency virus-infected macaques. J Virol 2010, 84:12862-12871. 10.1128/JVI.01478-10, 3004298, 20943985.
25. Koot M, Van Leeuwen R, De Goede RE, Keet IP, Danner S, Eeftinck Schattenkerk JK, Reiss P, Tersmette M, Lange JM, Schuitemaker H. 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 1999, 179:254-258. 10.1086/314539, 9841850.
26. Casper C, Naver L, Clevestig P, Belfrage E, Leitner T, Albert J, Lindgren S, Ottenblad C, Bohlin AB, Fenyo EM, Ehrnst A. Coreceptor change appears after immune deficiency is established in children infected with different HIV-1 subtypes. AIDS Res Hum Retroviruses 2002, 18:343-352. 10.1089/088922202753519124, 11897036.
27. Richman DD, Bozzette SA. The impact of the syncytium-inducing phenotype of human immunodeficiency virus on disease progression. J Infect Dis 1994, 169:968-974. 10.1093/infdis/169.5.968, 7909549.
28. Bunnik EM, Quakkelaar ED, van Nuenen AC, Boeser-Nunnink B, Schuitemaker H. Increased neutralization sensitivity of recently emerged CXCR4-using human immunodeficiency virus type 1 strains compared to coexisting CCR5-using variants from the same patient. J Virol 2007, 81:525-531. 10.1128/JVI.01983-06, 1797458, 17079299.
29. Nabatov AA, Pollakis G, Linnemann T, Kliphius A, Chalaby MI, Paxton WA. 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 2004, 78:524-530. 10.1128/JVI.78.1.524-530.2004, 303404, 14671134.
30. Zhuang K, Finzi A, Tasca S, Shakirzyanova M, Knight H, Westmoreland S, Sodroski J, Cheng-Mayer C. Adoption of an "open" envelope conformation facilitating CD4 binding and structural remodeling precedes coreceptor switch in R5 SHIV-infected macaques. PLoS One 2011, 6:e21350. 10.1371/journal.pone.0021350, 3132741, 21760891.
31. Kolchinsky P, Kiprilov E, Sodroski J. Increased neutralization sensitivity of CD4-independent human immunodeficiency virus variants. J Virol 2001, 75:2041-2050. 10.1128/JVI.75.5.2041-2050.2001, 114788, 11160708.
32. Reeves JD, Gallo SA, Ahmad N, Miamidian JL, Harvey PE, Sharron M, Pohlmann S, Sfakianos JN, Derdeyn CA, Blumenthal R, et al. Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc Natl Acad Sci USA 2002, 99:16249-16254. 10.1073/pnas.252469399, 138597, 12444251.
33. Ho SH, Trunova N, Gettie A, Blanchard J, Cheng-Mayer C. Different mutational pathways to CXCR4 coreceptor switch of CCR5-using simian-human immunodeficiency virus. J Virol 2008, 82:5653-5656. 10.1128/JVI.00145-08, 2395221, 18385246.
34. Low AJ, Marchant D, Brumme CJ, Brumme ZL, Dong W, Sing T, Hogg RS, Montaner JS, Gill V, Cheung PK, Harrigan PR. CD4-dependent characteristics of coreceptor use and HIV type 1 V3 sequence in a large population of therapy-naive individuals. AIDS Res Hum Retroviruses 2008, 24:219-228. 10.1089/aid.2007.0140, 18240966.
35. Coetzer M, Nedellec R, Salkowitz J, McLaughlin S, Liu Y, Heath L, Mullins JI, Mosier DE. Evolution of CCR5 use before and during coreceptor switching. J Virol 2008, 82:11758-11766. 10.1128/JVI.01141-08, 2583682, 18815295.
36. Huang W, Toma J, Fransen S, Stawiski E, Reeves JD, Whitcomb JM, Parkin N, Petropoulos CJ. Coreceptor tropism can be influenced by amino acid substitutions in the gp41 transmembrane subunit of human immunodeficiency virus type 1 envelope protein. J Virol 2008, 82:5584-5593. 10.1128/JVI.02676-07, 2395220, 18353956.
37. Jansson M, Popovic M, Karlsson A, Cocchi F, Rossi P, Albert J, Wigzell H. Sensitivity to inhibition by beta-chemokines correlates with biological phenotypes of primary HIV-1 isolates. Proc Natl Acad Sci USA 1996, 93:15382-15387. 10.1073/pnas.93.26.15382, 26413, 8986820.
38. Koning FA, Kwa D, Boeser-Nunnink B, Dekker J, Vingerhoed J, Hiemstra H, Schuitemaker H. Decreasing sensitivity to RANTES (regulated on activation, normally T cell-expressed and -secreted) neutralization of CC chemokine receptor 5-using, non-syncytium-inducing virus variants in the course of human immunodeficiency virus type 1 infection. J Infect Dis 2003, 188:864-872. 10.1086/377105, 12964118.
39. Karlsson I, Antonsson L, Shi Y, Oberg M, Karlsson A, Albert J, Olde B, Owman C, Jansson M, Fenyo EM. Coevolution of RANTES sensitivity and mode of CCR5 receptor use by human immunodeficiency virus type 1 of the R5 phenotype. J Virol 2004, 78:11807-11815. 10.1128/JVI.78.21.11807-11815.2004, 523262, 15479822.
40. Repits J, Oberg M, Esbjornsson J, Medstrand P, Karlsson A, Albert J, Fenyo EM, Jansson M. Selection of human immunodeficiency virus type 1 R5 variants with augmented replicative capacity and reduced sensitivity to entry inhibitors during severe immunodeficiency. J Gen Virol 2005, 86:2859-2869. 10.1099/vir.0.81111-0, 16186242.
41. Etemad B, Fellows A, Kwambana B, Kamat A, Feng Y, Lee S, Sagar M. Human immunodeficiency virus type 1 V1-to-V5 envelope variants from the chronic phase of infection use CCR5 and fuse more efficiently than those from early after infection. J Virol 2009, 83:9694-9708. 10.1128/JVI.00925-09, 2748008, 19625411.
42. Orloff SL, Kennedy MS, Belperron AA, Maddon PJ, McDougal JS. Two mechanisms of soluble CD4 (sCD4)-mediated inhibition of human immunodeficiency virus type 1 (HIV-1) infectivity and their relation to primary HIV-1 isolates with reduced sensitivity to sCD4. J Virol 1993, 67:1461-1471. 237516, 8437224.
43. Moore JP, McKeating JA, Huang YX, Ashkenazi A, Ho DD. Virions of primary human immunodeficiency virus type 1 isolates resistant to soluble CD4 (sCD4) neutralization differ in sCD4 binding and glycoprotein gp120 retention from sCD4-sensitive isolates. J Virol 1992, 66:235-243. 238280, 1727487.
44. Thali M, Furman C, Helseth E, Repke H, Sodroski J. Lack of correlation between soluble CD4-induced shedding of the human immunodeficiency virus type 1 exterior envelope glycoprotein and subsequent membrane fusion events. J Virol 1992, 66:5516-5524. 289110, 1501286.
45. Stamatatos L, Werner A, Cheng-Mayer C. Differential regulation of cellular tropism and sensitivity to soluble CD4 neutralization by the envelope gp120 of human immunodeficiency virus type 1. J Virol 1994, 68:4973-4979. 236438, 8035496.
46. Haim H, Si Z, Madani N, Wang L, Courter JR, Princiotto A, Kassa A, DeGrace M, McGee-Estrada K, Mefford M, et al. Soluble CD4 and CD4-mimetic compounds inhibit HIV-1 infection by induction of a short-lived activated state. PLoS Pathog 2009, 5:e1000360. 10.1371/journal.ppat.1000360, 2655723, 19343205.
47. Kabat D, Kozak SL, Wehrly K, Chesebro B. Differences in CD4 dependence for infectivity of laboratory-adapted and primary patient isolates of human immunodeficiency virus type 1. J Virol 1994, 68:2570-2577. 236734, 8139036.
48. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 1998, 72:2855-2864. 109730, 9525605.
49. Mori K, Rosenzweig M, Desrosiers RC. Mechanisms for adaptation of simian immunodeficiency virus to replication in alveolar macrophages. J Virol 2000, 74:10852-10859. 10.1128/JVI.74.22.10852-10859.2000, 110966, 11044136.
50. Mori K, Ringler DJ, Desrosiers RC. Restricted replication of simian immunodeficiency virus strain 239 in macrophages is determined by env but is not due to restricted entry. J Virol 1993, 67:2807-2814. 237605, 7682627.
51. Tasca S, Zhuang K, Gettie A, Knight H, Blanchard J, Westmoreland S, Cheng-Mayer C. Effect of B-cell depletion on coreceptor switching in R5 simian-human immunodeficiency virus infection of rhesus macaques. J Virol 2011, 85:3086-3094. 10.1128/JVI.02150-10, 3067891, 21248033.
52. Bozzette SA, McCutchan JA, Spector SA, Wright B, Richman DD. A cross-sectional comparison of persons with syncytium- and non-syncytium-inducing human immunodeficiency virus. J Infect Dis 1993, 168:1374-1379. 10.1093/infdis/168.6.1374, 7902382.
53. Brumme ZL, Goodrich J, Mayer HB, Brumme CJ, Henrick BM, Wynhoven B, Asselin JJ, Cheung PK, Hogg RS, Montaner JS, Harrigan PR. Molecular and clinical epidemiology of CXCR4-using HIV-1 in a large population of antiretroviral-naive individuals. J Infect Dis 2005, 192:466-474. 10.1086/431519, 15995960.
54. Furrer H, Wendland T, Minder C, Christen A, von Overbeck J, Grunow R, Pichler W, Malinverni RP. Association of syncytium-inducing phenotype of HIV-1 with CD4 cell count, viral load and sociodemographic characteristics. AIDS 1998, 12:1341-1346. 10.1097/00002030-199811000-00016, 9708414.
55. Melby T, Despirito M, Demasi R, Heilek-Snyder G, Greenberg ML, Graham N. HIV-1 coreceptor use in triple-class treatment-experienced patients: baseline prevalence, correlates, and relationship to enfuvirtide response. J Infect Dis 2006, 194:238-246. 10.1086/504693, 16779731.
56. Wilkin TJ, Su Z, Kuritzkes DR, Hughes M, Flexner C, Gross R, Coakley E, Greaves W, Godfrey C, Skolnik PR, et al. HIV type 1 chemokine coreceptor use among antiretroviral-experienced patients screened for a clinical trial of a CCR5 inhibitor: AIDS Clinical Trial Group A5211. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 2007, 44:591-595.
57. Moyle GJ, Wildfire A, Mandalia S, Mayer H, Goodrich J, Whitcomb J, Gazzard BG. Epidemiology and predictive factors for chemokine receptor use in HIV-1 infection. J Infect Dis 2005, 191:866-872. 10.1086/428096, 15717260.
58. van Rij RP, Hazenberg MD, van Benthem BH, Otto SA, Prins M, Miedema F, Schuitemaker H. 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 Retroviruses 2003, 19:389-398. 10.1089/088922203765551737, 12803997.
59. Kassaye S, Johnston E, McColgan B, Kantor R, Zijenah L, Katzenstein D. Envelope coreceptor tropism, drug resistance, and viral evolution among subtype C HIV-1-infected individuals receiving nonsuppressive antiretroviral therapy. J Acquir Immune Defic Syndr 2009, 50:9-18. 10.1097/QAI.0b013e31818ffdff, 2818215, 19295330.
60. Wout AB V, Blaak H, Ran LJ, Brouwer M, Kuiken C, Schuitemaker H. Evolution of syncytium-inducing and non-syncytium-inducing biological virus clones in relation to replication kinetics during the course of human immunodeficiency virus type 1 infection. J Virol 1998, 72:5099-5107. 110075, 9573281.
61. Asjo B, Morfeldt-Manson L, Albert J, Biberfeld G, Karlsson A, Lidman K, Fenyo EM. Replicative capacity of human immunodeficiency virus from patients with varying severity of HIV infection. Lancet 1986, 2:660-662.
62. Connor RI, Mohri H, Cao Y, Ho DD. Increased viral burden and cytopathicity correlate temporally with CD4+ T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J Virol 1993, 67:1772-1777. 240220, 8095306.
63. Cheng-Mayer C, Seto D, Tateno M, Levy JA. Biologic features of HIV-1 that correlate with virulence in the host. Science 1988, 240:80-82. 10.1126/science.2832945, 2832945.
64. Harouse JM, Tan RC, Gettie A, Dailey P, Marx PA, Luciw PA, Cheng-Mayer C. In vitro infection of primate PBMC with simian/human immunodeficiency virus, SHIV(SF33A): correlation to in vivo outcome. J Med Primatol 1998, 27:81-86. 10.1111/j.1600-0684.1998.tb00230.x, 9747947.
65. Igarashi T, Endo Y, Englund G, Sadjadpour R, Matano T, Buckler C, Buckler-White A, Plishka R, Theodore T, Shibata R, Martin M. Emergence of a highly pathogenic simian/human immunodeficiency virus in a rhesus macaque treated with anti-CD8 mAb during a primary infection with a nonpathogenic virus. Proc Natl Acad Sci USA 1999, 96:14049-14054. 10.1073/pnas.96.24.14049, 24188, 10570196.
66. Joag SV, Li Z, Foresman L, Stephens EB, Zhao LJ, Adany I, Pinson DM, McClure HM, Narayan O. Chimeric simian/human immunodeficiency virus that causes progressive loss of CD4+ T cells and AIDS in pig-tailed macaques. J Virol 1996, 70:3189-3197. 190182, 8627799.
67. Reimann KA, Li JT, Veazey R, Halloran M, Park IW, Karlsson GB, Sodroski J, Letvin NL. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J Virol 1996, 70:6922-6928. 190741, 8794335.
68. Harouse JM, Buckner C, Gettie A, Fuller R, Bohm R, Blanchard J, Cheng-Mayer C. CD8+ T cell-mediated CXC chemokine receptor 4-simian/human immunodeficiency virus suppression in dually infected rhesus macaques. Proc Natl Acad Sci USA 2003, 100:10977-10982. 10.1073/pnas.1933268100, 196912, 12963814.
69. Ho SH, Shek L, Gettie A, Blanchard J, Cheng-Mayer C. V3 loop-determined coreceptor preference dictates the dynamics of CD4+-T-cell loss in simian-human immunodeficiency virus-infected macaques. J Virol 2005, 79:12296-12303. 10.1128/JVI.79.19.12296-12303.2005, 1211551, 16160156.
70. Nishimura Y, Igarashi T, Donau OK, Buckler-White A, Buckler C, Lafont BA, Goeken RM, Goldstein S, Hirsch VM, Martin MA. Highly pathogenic SHIVs and SIVs target different CD4+ T cell subsets in rhesus monkeys, explaining their divergent clinical courses. Proc Natl Acad Sci USA 2004, 101:12324-12329. 10.1073/pnas.0404620101, 514404, 15297611.
71. Isaacman-Beck J, Hermann EA, Yi Y, Ratcliffe SJ, Mulenga J, Allen S, Hunter E, Derdeyn CA, Collman RG. Heterosexual transmission of human immunodeficiency virus type 1 subtype C: Macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization. J Virol 2009, 83:8208-8220. 10.1128/JVI.00296-09, 2715751, 19515785.
72. Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, Salazar MG, Salazar-Gonzalez JF, Shattock R, Haynes BF, Shaw GM, et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol 2012, 86:2715-2728. 10.1128/JVI.06157-11, 3302286, 22190722.
73. Kozak SL, Platt EJ, Madani N, Ferro FE, Peden K, Kabat D. CD4, CXCR-4, and CCR-5 dependencies for infections by primary patient and laboratory-adapted isolates of human immunodeficiency virus type 1. J Virol 1997, 71:873-882. 191134, 8995603.
74. Platt EJ, Madani N, Kozak SL, Kabat D. Infectious properties of human immunodeficiency virus type 1 mutants with distinct affinities for the CD4 receptor. J Virol 1997, 71:883-890. 191135, 8995604.
75. Sullivan N, Sun Y, Sattentau Q, Thali M, Wu D, Denisova G, Gershoni J, Robinson J, Moore J, Sodroski J. CD4-Induced conformational changes in the human immunodeficiency virus type 1 gp120 glycoprotein: consequences for virus entry and neutralization. J Virol 1998, 72:4694-4703. 109994, 9573233.
76. Alexander M, Lynch R, Mulenga J, Allen S, Derdeyn CA, Hunter E. Donor and recipient envs from heterosexual human immunodeficiency virus subtype C transmission pairs require high receptor levels for entry. J Virol 2010, 84:4100-4104. 10.1128/JVI.02068-09, 2849512, 20147398.
77. Brown CR, Czapiga M, Kabat J, Dang Q, Ourmanov I, Nishimura Y, Martin MA, Hirsch VM. Unique pathology in simian immunodeficiency virus-infected rapid progressor macaques is consistent with a pathogenesis distinct from that of classical AIDS. J Virol 2007, 81:5594-5606. 10.1128/JVI.00202-07, 1900277, 17376901.
78. Gray L, Sterjovski J, Churchill M, Ellery P, Nasr N, Lewin SR, Crowe SM, Wesselingh SL, Cunningham AL, Gorry PR. 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 2005, 337:384-398. 10.1016/j.virol.2005.04.034, 15916792.
79. Li S, Juarez J, Alali M, Dwyer D, Collman R, Cunningham A, Naif HM. Persistent CCR5 utilization and enhanced macrophage tropism by primary blood human immunodeficiency virus type 1 isolates from advanced stages of disease and comparison to tissue-derived isolates. J Virol 1999, 73:9741-9755. 113021, 10559284.
80. Tuttle DL, Anders CB, Aquino-De Jesus MJ, Poole PP, Lamers SL, Briggs DR, Pomeroy SM, Alexander L, Peden KW, Andiman WA, et al. Increased replication of non-syncytium-inducing HIV type 1 isolates in monocyte-derived macrophages is linked to advanced disease in infected children. AIDS Res Hum Retroviruses 2002, 18:353-362. 10.1089/088922202753519133, 11897037.
81. Ebert LM, McColl SR. Up-regulation of CCR5 and CCR6 on distinct subpopulations of antigen-activated CD4+ T lymphocytes. J Immunol 2002, 168:65-72.
82. Weyand CM, Goronzy J, Fathman CG. Modulation of CD4 by antigenic activation. J Immunol 1987, 138:1351-1354.
83. Paillard F, Sterkers G, Vaquero C. Transcriptional and post-transcriptional regulation of TcR, CD4 and CD8 gene expression during activation of normal human T lymphocytes. EMBO J 1990, 9:1867-1872. 551892, 2140772.
84. Hwang SS, Boyle TJ, Lyerly HK, Cullen BR. Identification of envelope V3 loop as the major determinant of CD4 neutralization sensitivity of HIV-1. Science 1992, 257:535-537. 10.1126/science.1636088, 1636088.
85. O'Brien WA, Chen IS, Ho DD, Daar ES. Mapping genetic determinants for human immunodeficiency virus type 1 resistance to soluble CD4. J Virol 1992, 66:3125-3130. 241075, 1373203.
86. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 2002, 46:1896-1905. 10.1128/AAC.46.6.1896-1905.2002, 127242, 12019106.
87. Ho SH, Martin F, Higginbottom A, Partridge LJ, Parthasarathy V, Moseley GW, Lopez P, Cheng-Mayer C, Monk PN. Recombinant extracellular domains of tetraspanin proteins are potent inhibitors of the infection of macrophages by human immunodeficiency virus type 1. J Virol 2006, 80:6487-6496. 10.1128/JVI.02539-05, 1488983, 16775336.
88. Connor RI, Chen BK, Choe S, Landau NR. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 1995, 206:935-944. 10.1006/viro.1995.1016, 7531918.
89. Chowdhury IH, Koyanagi Y, Takamatsu K, Yoshida O, Kobayashi S, Yamamoto N. Evaluation of anti-human immunodeficiency virus effect of recombinant CD4-immunoglobulin in vitro: a good candidate for AIDS treatment. Medical microbiology and immunology 1991, 180:183-192.