Lack of adaptation to human tetherin in HIV-1 Group O and P

Retrovirology

Volumn 8, Issue , 2011, Pages

  Yang, Su Jung ^a   Lopez, Lisa A ^a   Exline, Colin M ^a   Haworth, Kevin G ^a   Cannon, Paula M ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CELL MEMBRANE PROTEIN; NEF PROTEIN; TETHERIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VPU PROTEIN; BST2 PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; LEUKOCYTE ANTIGEN; VIRUS PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ADAPTATION; ARTICLE; CONTROLLED STUDY; GENOME ANALYSIS; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE MAPPING; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRUS CELL INTERACTION; VIRUS CLASSIFICATION; VIRUS GENOME; CELL LINE; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; PRIMATES;

ANTIGENS, CD; CELL LINE; GPI-LINKED PROTEINS; HIV INFECTIONS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; PROTEIN BINDING; PROTEIN TRANSPORT; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 80053375827     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-8-78     Document Type: Article

References (68)

1. Neil SJ, Zang T, Bieniasz PD. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430. 10.1038/nature06553, 18200009.
2. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli JC. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3:245-252. 10.1016/j.chom.2008.03.001, 2474773, 18342597.
3. Sauter D, Schindler M, Specht A, Landford WN, Münch J, Kim KA, Votteler J, Schubert U, Bibollet-Ruche F, Keele BF, Takehisa J, Ogando Y, Ochsenbauer C, Kappes JC, Ayouba A, Peeters M, Learn GH, Shaw G, Sharp PM, Bieniasz PD, Hahn BH, Hatziioannou T, Kirchhoff F. Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 2009, 6:409-421. 10.1016/j.chom.2009.10.004, 2779047, 19917496.
4. Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog 2009, 5:e1000429. 10.1371/journal.ppat.1000429, 2673686, 19436700.
5. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, Johnson MC, Munch J, Kirchhoff F, Bieniasz PD, Hatziioannou T. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 2009, 6:54-67. 10.1016/j.chom.2009.05.008, 2852097, 19501037.
6. Lim ES, Malik HS, Emerman M. Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J Virol 2010, 84:7124-7134. 10.1128/JVI.00468-10, 2898239, 20444900.
7. Yang SJ, Lopez LA, Hauser H, Exline CM, Haworth KG, Cannon PM. Anti-tetherin activities in Vpu-expressing primate lentiviruses. Retrovirology 2010, 7:13. 10.1186/1742-4690-7-13, 2831821, 20167081.
8. Gupta RK, Mlcochova P, Pelchen-Matthews A, Petit SJ, Mattiuzzo G, Pillay D, Takeuchi Y, Marsh M, Towers GJ. Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc Natl Acad Sci USA 2009,
9. Bour S, Schubert U, Peden K, Strebel K. The envelope glycoprotein of human immunodeficiency virus type 2 enhances viral particle release: a Vpu-like factor?. J Virol 1996, 70:820-829. 189884, 8551620.
10. Le Tortorec A, Neil SJ. Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J Virol 2009, 83:11966-11978. 10.1128/JVI.01515-09, 2772693, 19740980.
11. Abada P, Noble B, Cannon PM. Functional domains within the human immunodeficiency virus type 2 envelope protein required to enhance virus production. J Virol 2005, 79:3627-3638. 10.1128/JVI.79.6.3627-3638.2005, 1075700, 15731257.
12. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Fofana IB, Johnson WE, Neil SJ, Bieniasz PD. Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 2009, 5:e1000300. 10.1371/journal.ppat.1000300, 2633611, 19214216.
13. Goffinet C, Allespach I, Homann S, Tervo HM, Habermann A, Rupp D, Oberbremer L, Kern C, Tibroni N, Welsch S, Krijnse-Locker J, Banting G, Kräusslich HG, Fackler OT, Keppler OT. HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 2009, 5:285-297. 10.1016/j.chom.2009.01.009, 19286137.
14. Corbet S, Müller-Trutwin MC, Versmisse P, Delarue S, Ayouba A, Lewis J, Brunak S, Martin P, Brun-Vezinet F, Simon F, Barre-Sinoussi F, Mauclere P. env sequences of simian immunodeficiency viruses from chimpanzees in Cameroon are strongly related to those of human immunodeficiency virus group N from the same geographic area. J Virol 2000, 74:529-534. 10.1128/JVI.74.1.529-534.2000, 111566, 10590144.
15. Simon F, Mauclère P, Roques P, Loussert-Ajaka I, Müller-Trutwin MC, Saragosti S, Georges-Courbot MC, Barré-Sinoussi F, Brun-Vézinet F. Identification of a new human immunodeficiency virus type 1 distinct from group M and group O. Nat Med 1998, 4:1032-1037. 10.1038/2017, 9734396.
16. Charneau P, Borman AM, Quillent C, Guétard D, Chamaret S, Cohen J, Rémy G, Montagnier L, Clavel F. Isolation and envelope sequence of a highly divergent HIV-1 isolate: definition of a new HIV-1 group. Virology 1994, 205:247-253. 10.1006/viro.1994.1640, 7975221.
17. Plantier JC, Leoz M, Dickerson JE, De Oliveira F, Cordonnier F, Lemée V, Damond F, Robertson DL, Simon F. A new human immunodeficiency virus derived from gorillas. Nat Med 2009, 15:871-872. 10.1038/nm.2016, 19648927.
18. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, Sharp PM, Hahn BH. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999, 397:436-441. 10.1038/17130, 9989410.
19. Sharp PM, Hahn BH. The evolution of HIV-1 and the origin of AIDS. Philos Trans R Soc Lond B Biol Sci 2010, 365:2487-2494. 10.1098/rstb.2010.0031, 2935100, 20643738.
20. Hahn BH, Shaw GM, De Cock KM, Sharp PM. AIDS as a zoonosis: scientific and public health implications. Science 2000, 287:607-614. 10.1126/science.287.5453.607, 10649986.
21. Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, Liu W, Loul S, Butel C, Liegeois F, Bienvenue Y, Ngolle EM, Sharp PM, Shaw GM, Delaporte E, Hahn BH, Peeters M. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 2006, 444:164. 10.1038/444164a, 17093443.
22. Takehisa J, Kraus MH, Ayouba A, Bailes E, Van Heuverswyn F, Decker JM, Li Y, Rudicell RS, Learn GH, Neel C, Ngole EM, Shaw GM, Peeters M, Sharp PM, Hahn BH. Origin and biology of simian immunodeficiency virus in wild-living western gorillas. J Virol 2009, 83:1635-1648. 10.1128/JVI.02311-08, 2643789, 19073717.
23. Ayouba A, Souquières S, Njinku B, Martin PM, Müller-Trutwin MC, Roques P, Barré-Sinoussi F, Mauclère P, Simon F, Nerrienet E. HIV-1 group N among HIV-1-seropositive individuals in Cameroon. AIDS 2000, 14:2623-2625. 10.1097/00002030-200011100-00033, 11101082.
24. Bodelle P, Vallari A, Coffey R, McArthur CP, Beyeme M, Devare SG, Schochetman G, Brennan CA. Identification and genomic sequence of an HIV type 1 group N isolate from Cameroon. AIDS Res Hum Retroviruses 2004, 20:902-908. 10.1089/0889222041725262, 15320995.
25. Vergne L, Bourgeois A, Mpoudi-Ngole E, Mougnutou R, Mbuagbaw J, Liegeois F, Laurent C, Butel C, Zekeng L, Delaporte E, Peeters M. Biological and genetic characteristics of HIV infections in Cameroon reveals dual group M and O infections and a correlation between SI-inducing phenotype of the predominant CRF02_AG variant and disease stage. Virology 2003, 310:254-266.
26. Peeters M, Gueye A, Mboup S, Bibollet-Ruche F, Ekaza E, Mulanga C, Ouedrago R, Gandji R, Mpele P, Dibanga G, Koumare B, Saidou M, Esu-Williams E, Lombart JP, Badombena W, Luo N, Vanden Haesevelde M, Delaporte E. Geographical distribution of HIV-1 group O viruses in Africa. AIDS 1997, 11:493-498. 10.1097/00002030-199704000-00013, 9084797.
27. Quiñones-Mateu ME, Ball SC, Arts EJ. Role of Human Immunodeficiency Virus Type 1 Group O in the AIDS Pandemic. AIDS Rev 2000, 2:12.
28. Ayouba A, Mauclère P, Martin PM, Cunin P, Mfoupouendoun J, Njinku B, Souquières S, Simon F. HIV-1 group O infection in Cameroon, 1986 to 1998. Emerg Infect Dis 2001, 7:466-467. 2631804, 11384531.
29. Brennan CA, Bodelle P, Coffey R, Devare SG, Golden A, Hackett JJ, Harris B, Holzmayer V, Luk KC, Schochetman G, Swanson P, Yamaguchi J, Vallari A, Ndembi N, Ngansop C, Makamche F, Mbanya D, Gürtler LG, Zekeng L, Kaptué L. The prevalence of diverse HIV-1 strains was stable in Cameroonian blood donors from 1996 to 2004. J Acquir Immune Defic Syndr 2008, 49:432-439. 10.1097/QAI.0b013e31818a6561, 18931623.
30. Vallari A, Holzmayer V, Harris B, Yamaguchi J, Ngansop C, Makamche F, Mbanya D, Kaptué L, Ndembi N, Gürtler L, Devare S, Brennan CA. Confirmation of putative HIV-1 group P in Cameroon. J Virol 2011, 85:1403-1407. 10.1128/JVI.02005-10, 3020498, 21084486.
31. Ariën KK, Abraha A, Quiñones-Mateu ME, Kestens L, Vanham G, Arts EJ. The replicative fitness of primary human immunodeficiency virus type 1 (HIV-1) group M, HIV-1 group O, and HIV-2 isolates. J Virol 2005, 79:8979-8990. 10.1128/JVI.79.14.8979-8990.2005, 1168791, 15994792.
32. Geuenich S, Kaderali L, Allespach I, Sertel S, Keppler OT. Biological signature characteristics of primary isolates from human immunodeficiency virus type 1 group O in ex vivo human tonsil histocultures. J Virol 2009, 83:10494-10503. 10.1128/JVI.00928-09, 2753123, 19706709.
33. Laurent C, Bourgeois A, Faye MA, Mougnutou R, Seydi M, Gueye M, Liégeois F, Kane CT, Butel C, Mbuagbaw J, Zekeng L, Mboup S, Mpoudi-Ngolé E, Peeters M, Delaporte E. No difference in clinical progression between patients infected with the predominant human immunodeficiency virus type 1 circulating recombinant form (CRF) 02_AG strain and patients not infected with CRF02_AG, in Western and West-Central Africa: a four-year prospective multicenter study. J Infect Dis 2002, 186:486-492. 10.1086/341833, 12195375.
34. Gueudin M, Plantier JC, Damond F, Roques P, Mauclère P, Simon F. Plasma viral RNA assay in HIV-1 group O infection by real-time PCR. J Virol Methods 2003, 113:43-49. 10.1016/S0166-0934(03)00223-4, 14500126.
35. Jonassen TO, Stene-Johansen K, Berg ES, Hungnes O, Lindboe CF, Frøland SS, Grinde B. Sequence analysis of HIV-1 group O from Norwegian patients infected in the 1960s. Virology 1997, 231:43-47. 10.1006/viro.1997.8510, 9143301.
36. Bibollet-Ruche F, Loussert-Ajaka I, Simon F, Mboup S, Ngole EM, Saman E, Delaporte E, Peeters M. Genetic characterization of accessory genes from human immunodeficiency virus type 1 group O strains. AIDS Res Hum Retroviruses 1998, 14:951-961. 10.1089/aid.1998.14.951, 9686641.
37. Loussert-Ajaka I, Chaix ML, Korber B, Letourneur F, Gomas E, Allen E, Ly TD, Brun-Vézinet F, Simon F, Saragosti S. Variability of human immunodeficiency virus type 1 group O strains isolated from Cameroonian patients living in France. J Virol 1995, 69:5640-5649. 189421, 7637010.
38. Schubert U, Antón LC, Bacík I, Cox JH, Bour S, Bennink JR, Orlowski M, Strebel K, Yewdell JW. CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. J Virol 1998, 72:2280-2288. 109526, 9499087.
39. Ruiz A, Guatelli JC, Stephens EB. The Vpu Protein: New Concepts in Virus Release and CD4 Down-Modulation. Curr HIV Res 2010,
40. Lindwasser OW, Chaudhuri R, Bonifacino JS. Mechanisms of CD4 downregulation by the Nef and Vpu proteins of primate immunodeficiency viruses. Curr Mol Med 2007, 7:171-184. 10.2174/156652407780059177, 17346169.
41. Bour S, Schubert U, Strebel K. The human immunodeficiency virus type 1 Vpu protein specifically binds to the cytoplasmic domain of CD4: implications for the mechanism of degradation. J Virol 1995, 69:1510-1520. 188742, 7853484.
42. Roques P, Robertson DL, Souquière S, Damond F, Ayouba A, Farfara I, Depienne C, Nerrienet E, Dormont D, Brun-Vézinet F, Simon F, Mauclère P. Phylogenetic analysis of 49 newly derived HIV-1 group O strains: high viral diversity but no group M-like subtype structure. Virology 2002, 302:259-273. 10.1006/viro.2002.1430, 12441070.
43. Yamaguchi J, Vallari AS, Swanson P, Bodelle P, Kaptué L, Ngansop C, Zekeng L, Gürtler LG, Devare SG, Brennan CA. Evaluation of HIV type 1 group O isolates: identification of five phylogenetic clusters. AIDS Res Hum Retroviruses 2002, 18:269-282. 10.1089/088922202753472847, 11860674.
44. Yamaguchi J, Bodelle P, Kaptué L, Zekeng L, Gürtler LG, Devare SG, Brennan CA. Near full-length genomes of 15 HIV type 1 group O isolates. AIDS Res Hum Retroviruses 2003, 19:979-988. 10.1089/088922203322588332, 14678605.
45. Tebit DM, Zekeng L, Kaptué L, Gürtler L, Fackler OT, Keppler OT, Herchenröder O, Kräusslich HG. Construction and characterization of an HIV-1 group O infectious molecular clone and analysis of vpr- and nef-negative derivatives. Virology 2004, 326:329-339. 10.1016/j.virol.2004.05.027, 15321704.
46. Hauser H, Lopez LA, Yang SJ, Oldenburg JE, Exline CM, Guatelli JC, Cannon PM. HIV-1 Vpu and HIV-2 Env counteract BST-2/tetherin by sequestration in a perinuclear compartment. Retrovirology 2010, 7:51. 10.1186/1742-4690-7-51, 2890665, 20529266.
47. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Früh K, Moses AV. Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a {beta}TrCP-dependent mechanism. J Virol 2009, 83:7931-7947. 10.1128/JVI.00242-09, 2715753, 19515779.
48. Dubé M, Roy BB, Guiot-Guillain P, Binette J, Mercier J, Chiasson A, Cohen EA. Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathog 2010, 6:e1000856. 10.1371/journal.ppat.1000856, 2851737, 20386718.
49. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, Ruiz A, Stephens EB, Margottin-Goguet F, Benarous R, Guatelli JC. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog 2009, 5:e1000450. 10.1371/journal.ppat.1000450, 2679223, 19478868.
50. Rong L, Zhang J, Lu J, Pan Q, Lorgeoux RP, Aloysius C, Guo F, Liu SL, Wainberg MA, Liang C. The transmembrane domain of BST-2 determines its sensitivity to down-modulation by human immunodeficiency virus type 1 Vpu. J Virol 2009, 83:7536-7546. 10.1128/JVI.00620-09, 2708638, 19474106.
51. Piguet V, Gu F, Foti M, Demaurex N, Gruenberg J, Carpentier JL, Trono D. Nef-induced CD4 degradation: a diacidic-based motif in Nef functions as a lysosomal targeting signal through the binding of beta-COP in endosomes. Cell 1999, 97:63-73. 10.1016/S0092-8674(00)80715-1, 10199403.
52. Dubé M, Roy BB, Guiot-Guillain P, Mercier J, Binette J, Leung G, Cohen EA. Suppression of Tetherin-restricting activity upon human immunodeficiency virus type 1 particle release correlates with localization of Vpu in the trans-Golgi network. J Virol 2009, 83:4574-4590. 10.1128/JVI.01800-08, 2668474, 19244337.
53. Mangeat B, Gers-Huber G, Lehmann M, Zufferey M, Luban J, Piguet V. HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog 2009, 5:e1000574. 10.1371/journal.ppat.1000574, 2729927, 19730691.
54. Vigan R, Neil SJ. Determinants of tetherin antagonism in the transmembrane domain of the human immunodeficiency virus type 1 Vpu protein. J Virol 2010, 84:12958-12970. 10.1128/JVI.01699-10, 3004320, 20926557.
55. Skasko MA, Tokarev A, Chen CC, Fischer WB, Pillai SK, Guatelli JC. BST-2 is rapidly down-regulated from the cell surface by the HIV-1 protein Vpu: Evidence for a post-ER mechanism of Vpu-action. Virology 2011,
56. Pacyniak E, Gomez ML, Gomez LM, Mulcahy ER, Jackson M, Hout DR, Wisdom BJ, Stephens EB. Identification of a region within the cytoplasmic domain of the subtype B Vpu protein of human immunodeficiency virus type 1 (HIV-1) that is responsible for retention in the golgi complex and its absence in the Vpu protein from a subtype C HIV-1. AIDS Res Hum Retroviruses 2005, 21:379-394. 10.1089/aid.2005.21.379, 15929700.
57. Park SH, Mrse AA, Nevzorov AA, Mesleh MF, Oblatt-Montal M, Montal M, Opella SJ. Three-dimensional structure of the channel-forming trans-membrane domain of virus protein "u" (Vpu) from HIV-1. J Mol Biol 2003, 333:409-424. 10.1016/j.jmb.2003.08.048, 14529626.
58. Hout DR, Gomez LM, Pacyniak E, Miller JM, Hill MS, Stephens EB. A single amino acid substitution within the transmembrane domain of the human immunodeficiency virus type 1 Vpu protein renders simian-human immunodeficiency virus (SHIV(KU-1bMC33)) susceptible to rimantadine. Virology 2006, 348:449-461. 10.1016/j.virol.2005.12.025, 16458946.
59. Andrew AJ, Miyagi E, Kao S, Strebel K. The formation of cysteine-linked dimers of BST-2/tetherin is important for inhibition of HIV-1 virus release but not for sensitivity to Vpu. Retrovirology 2009, 6:80. 10.1186/1742-4690-6-80, 2754425, 19737401.
60. Vigan R, Neil SJ. Separable Determinants of Subcellular Localization and Interaction Account for the Inability of Group O HIV-1 Vpu To Counteract Tetherin. J Virol 2011, 85:9737-9748. 10.1128/JVI.00479-11, 21775465.
61. Diop OM, Ploquin MJ, Mortara L, Faye A, Jacquelin B, Kunkel D, Lebon P, Butor C, Hosmalin A, Barré-Sinoussi F, Müller-Trutwin MC. Plasmacytoid dendritic cell dynamics and alpha interferon production during Simian immunodeficiency virus infection with a nonpathogenic outcome. J Virol 2008, 82:5145-5152. 10.1128/JVI.02433-07, 2395206, 18385227.
62. Lim ES, Emerman M. Simian immunodeficiency virus SIVagm from African green monkeys does not antagonize endogenous levels of African green monkey tetherin/BST-2. J Virol 2009, 83:11673-11681. 10.1128/JVI.00569-09, 2772663, 19726508.
63. Sharp PM, Shaw GM, Hahn BH. Simian immunodeficiency virus infection of chimpanzees. J Virol 2005, 79:3891-3902. 10.1128/JVI.79.7.3891-3902.2005, 1061584, 15767392.
64. Kirchhoff F. Is the high virulence of HIV-1 an unfortunate coincidence of primate lentiviral evolution?. Nat Rev Microbiol 2009, 7:467-476.
65. Schubert U, Strebel K. Differential activities of the human immunodeficiency virus type 1-encoded Vpu protein are regulated by phosphorylation and occur in different cellular compartments. J Virol 1994, 68:2260-2271. 236702, 8139011.
66. Gomez LM, Pacyniak E, Flick M, Hout DR, Gomez ML, Nerrienet E, Ayouba A, Santiago ML, Hahn BH, Stephens EB. Vpu-mediated CD4 down-regulation and degradation is conserved among highly divergent SIV(cpz) strains. Virology 2005, 335:46-60. 10.1016/j.virol.2005.01.049, 15823605.
67. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 1986, 59:284-291. 253077, 3016298.
68. Achour L, Scott MG, Shirvani H, Thuret A, Bismuth G, Labbé-Jullié C, Marullo S. CD4-CCR5 interaction in intracellular compartments contributes to receptor expression at the cell surface. Blood 2009, 113:1938-1947. 10.1182/blood-2008-02-141275, 2793409, 19064722.