Loss of a tyrosine-dependent trafficking motif in the simian immunodeficiency virus envelope cytoplasmic tail spares mucosal CD4 cells but does not prevent disease progression

Journal of Virology

Volumn 87, Issue 3, 2013, Pages 1528-1543

  Breed, Matthew W ^a   Jordan, Andrea P O ^b   Aye, Pyone P ^a   Lichtveld, Cornelis F ^a   Midkiff, Cecily C ^a   Schiro, Faith R ^a   Haggarty, Beth S ^b   Sugimoto, Chie ^a   Alvarez, Xavier ^a   Sandler, Netanya G ^c   Douek, Daniel C ^c   Kuroda, Marcelo J ^a   Pahar, Bapi ^a   Piatak, Michael ^d   Lifson, Jeffrey D ^d   Keele, Brandon F ^d   Hoxie, James A ^b   Lackner, Andrew A ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; TYROSINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVITY; CELL DISRUPTION; CELL LEVEL; CELL MIGRATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CLINICAL EVALUATION; CLINICAL FEATURE; CONTROLLED STUDY; CYTOPLASM; DISEASE COURSE; FEMALE; IMMUNOSTIMULATION; IN VIVO STUDY; INFECTION PREVENTION; LAMINA PROPRIA; LONGITUDINAL STUDY; MACROPHAGE; MALE; MICROBIAL TRANSLOCATION; MUCOSA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOLOGY; PRIORITY JOURNAL; PROTEIN DEPLETION; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS ENVELOPE; VIRUS REPLICATION;

EID: 84873049240     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01928-12     Document Type: Article

References (90)

1. Bosinger SE, Sodora DL, Silvestri G. 2011. Generalized immune activation and innate immune responses in simian immunodeficiency virus infection. Curr. Opin. HIV AIDS 6:411-418.
2. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, Blazar BR, Rodriguez B, Teixeira-Johnson L, Landay A, Martin JN, Hecht FM, Picker LJ, Lederman MM, Deeks SG, Douek DC. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12:1365-1371.
3. Brenchley JM, Silvestri G, Douek DC. 2010. Nonprogressive and progressive primate immunodeficiency lentivirus infections. Immunity 32: 737-742.
4. Chahroudi A, Bosinger SE, Vanderford TH, Paiardini M, Silvestri G. 2012. Natural SIV hosts: showing AIDS the door. Science 335:1188-1193.
5. Douek D. 2007. HIV disease progression: immune activation, microbes, and a leaky gut. Top. HIV Med. 15:114-117.
6. Estes JD, Harris LD, Klatt NR, Tabb B, Pittaluga S, Paiardini M, Barclay GR, Smedley J, Pung R, Oliveira KM, Hirsch VM, Silvestri G, Douek DC, Miller CJ, Haase AT, Lifson J, Brenchley JM. 2010. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 6. doi:10.1371/journal.ppat.1001052.
7. + T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J. Immunol. 179:3026-3034.
8. Paiardini M, Cervasi B, Reyes-Aviles E, Micci L, Ortiz AM, Chahroudi A, Vinton C, Gordon SN, Bosinger SE, Francella N, Hallberg PL, Cramer E, Schlub T, Chan ML, Riddick NE, Collman RG, Apetrei C, Pandrea I, Else J, Munch J, Kirchhoff F, Davenport MP, Brenchley JM, Silvestri G. 2011. Low levels of SIV infection in sooty mangabey central memory CD T cells are associated with limited CCR5 expression. Nat. Med. 17:830-836.
9. + T cell depletion. J. Immunol. 181:6687-6691.
10. + T cells in not predictive of simian immunodeficiency virus virulence. J. Immunol. 179:3035-3046.
11. + T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J. Virol. 77:11708-11717.
12. + T cells. Nature 434:1148-1152.
13. + T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200:761-770.
14. + T cell depletion and viral replication in SIV infection. Science 280:427-431.
15. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, Shih R, Lewis J, Wiley DJ, Phair JP, Wolinsky SM, Detels R. 1999. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 179:859-870.
16. Rodriguez B, Sethi AK, Cheruvu VK, Mackay W, Bosch RJ, Kitahata M, Boswell SL, Mathews WC, Bangsberg DR, Martin J, Whalen CC, Sieg S, Yadavalli S, Deeks SG, Lederman MM. 2006. Predictive value of plasma HIV RNA level on rate of CD4 T-cell decline in untreated HIV infection. JAMA 296:1498-1506.
17. + T cell count in HIV-seropositive individuals with undetectable plasma HIVRNAlevels in the absence of therapy. J. Infect. Dis. 197:126-133.
18. Kuller LH, Tracy R, Belloso W, De Wit S, Drummond F, Lane HC, Ledergerber B, Lundgren J, Neuhaus J, Nixon D, Paton NI, Neaton JD. 2008. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med. 5:e203. doi:10.1371/journal.pmed .0050203.
19. Sandler NG, Wand H, Roque A, Law M, Nason MC, Nixon DE, Pedersen C, Ruxrungtham K, Lewin SR, Emery S, Neaton JD, Brenchley JM, Deeks SG, Sereti I, Douek DC. 2011. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J. Infect. Dis. 203:780-790.
20. Pandrea I, Apetrei C, Dufour J, Dillon N, Barbercheck J, Metzger M, Jacquelin B, Bohm R, Marx PA, Barre-Sinoussi F, Hirsch VM, Muller- Trutwin MC, Lackner AA, Veazey RS. 2006. Simian immunodeficiency virus SIVagm.sab infection of Caribbean African green monkeys: a new model for the study of SIV pathogenesis in natural hosts. J. Virol. 80:4858-4867.
21. + T cells is a typical feature of natural SIV hosts. Blood 109:1069-1076.
22. Kestler HW, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD, Desrosiers RC. 1991. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65:651-662.
23. Mori K, Ringler DJ, Kodama T, Desrosiers RC. 1992. Complex determinants of macrophage tropism in env of simian immunodeficiency virus. J. Virol. 66:2067-2075.
24. Daniel MD, Kirchoff F, Czajak SC, Sehgal PK, Desrosiers RC. 1992. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 258:1938-1941.
25. Johnson RP. 2002. Mechanisms of protection against simian immunodeficiency virus infection. Vaccine 20:1985-1987.
26. Koff WC, Johnson PR, Watkins DI, Burton DR, Lifson JD, Hasenkrug KJ, McDermott AB, Schultz A, Zamb TJ, Boyle R, Desrosiers RC. 2006. HIV vaccine design: insights from live attenuated SIV vaccines. Nat. Immunol. 7:19-23.
27. Reynolds MR, Weiler AM, Piaskowski SM, Kolar HL, Hessell AJ, Weiker M, Weisgrau KL, Leon EJ, Rogers WE, Makowsky R, McDermott AB, Boyle R, Wilson NA, Allison DB, Burton DR, Koff WC, Watkins DI. 2010. Macaques vaccinated with simian immunodeficiency virus SIVmac239δnef delay acquisition and control replication after repeated low-dose heterologous SIV challenge. J. Virol. 84:9190-9199.
28. Sugimoto C, Watanabe S, Naruse T, Kajiwara E, Shiino T, Umano N, Ueda K, Sato H, Ohgimoto S, Hirsch V, Villinger F, Ansari AA, Kimura A, Miyazawa M, Suzuki Y, Yamamoto N, Nagai Y, Mori K. 2010. Protection of macaques with diverse MHC genotypes against a heterologous SIV by vaccination with a deglycosylated live-attenuated SIV. PLoS One 5:e11678. doi:10.1371/journal.pone.0011678.
29. Wyand MS, Manson KH, Garcia-Moll M, Montefiori D, Desrosiers RC. 1996. Vaccine protection by a triple deletion mutant of simian immunodeficiency virus. J. Virol. 70:3724-3733.
30. Alexander L, Illyinskii PO, Lang SM, Means RE, Lifson J, Mansfield K, Desrosiers RC. 2003. Determinants of increased replicative capacity of serially passaged simian immunodeficiency virus with nef deleted in rhesus monkeys. J. Virol. 77:6823-6835.
31. Connor RI, Montefiori DC, Binley JM, Moore JP, Bonhoeffer S, Gettie A, Fenamore EA, Sheridan KE, Ho DD, Dailey PJ, Marx PA. 1998. Temporal analyses of virus replication, immune responses, and efficacy in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J. Virol. 72:7501-7509.
32. Reynolds MR, Weiler AM, Weisgrau KL, Piaskowski SM, Furlott JR, Weinfurter JT, Kaizu M, Soma T, Leon EJ, MacNair C, Leaman DP, Zwick MB, Gostick E, Musani SK, Price DA, Friedrich TC, Rakasz EG, Wilson NA, McDermott AB, Boyle R, Allison DB, Burton DR, Koff WC, Watkins DI. 2008. Macaques vaccinated with live-attenuated SIV control replication of heterologous virus. J. Exp. Med. 205:2537-2550.
33. Munch J, Stolte N, Fuchs D, Stahl-Hennig C, Kirchhoff F. 2001. Efficient class I major histocompatibility complex downregulation by simian immunodeficiency virus Nef is associated with a strong selective advantage in infected rhesus macaques. J. Virol. 75:10532-10536.
34. Schindler M, Munch J, Kutsch O, Li H, Santiago ML, Bibollet-Ruche F, Muller-Trutwin MC, Novembre FJ, Peeters M, Courgnaud V, Bailes E, Roques P, Sodora DL, Silvestri G, Sharp PM, Hahn BH, Kirchhoff F. 2006. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125:1055-1067.
35. Serra-Moreno R, Jia B, Breed M, Alvarez X, Evans DT. 2011. Compensatory changes in the cytoplasmic tail of gp41 confer resistance to tetherin/ BST-2 in a pathogenic nef-deleted SIV. Cell Host Microbe 9:46-57.
36. Fultz PN, Vance PJ, Endres MJ, Tao B, Dvorin JD, Davis IC, Lifson JD, Montefiori DC, Marsh M, Malim MH, Hoxie JA. 2001. In vivo attenuation of simian immunodeficiency virus by disruption of a tyrosinedependent sorting signal in the envelope glycoprotein cytoplasmic tail. J. Virol. 75:278-291.
37. Bowers K, Pelchen-Matthews A, Honing S, Vance PJ, Creary L, Haggarty BS, Romano J, Ballensiefen W, Hoxie JA, Marsh M. 2000. The simian immunodeficiency virus envelope glycoprotein contains multiple signals that regulate its cell surface expression and endocytosis. Traffic 1:661-674.
38. Berlioz-Torrent C, Shacklett BL, Erdtmann L, Delamarre L, Bouchaert I, Sonigo P, Dokhelar MC, Benarous R. 1999. Interactions of the cytoplasmic domains of human and simian retroviral transmembrane proteins with components of the clathrin adaptor complexes modulate intracellular and cell surface expression of envelope glycoproteins. J. Virol. 73:1350-1361.
39. Boge M, Wyss S, Bonifacino JS, Thali M. 1998. A membrane-proximal tyrosine-based signal mediates internalization of the HIV-1 envelope glycoprotein via interaction with the AP-2 clathrin adaptor. J. Biol. Chem. 273:15773-15778.
40. Bowers K, Pitcher C, Marsh M. 1997. CD4: a coreceptor in the immune response and HIV infection. Int. J. Biochem. Cell Biol. 29:871-875.
41. Ohno H, Aguilar RC, Fournier MC, Hennecke S, Cosson P, Bonifacino JS. 1997. Interaction of endocytic signals from the HIV-1 envelope glycoprotein complex with members of the adaptor medium chain family. Virology 238:305-315.
42. Sauter MM, Pelchen-Matthews A, Bron R, Marsh M, LaBranche CC, Vance PJ, Romano J, Haggarty BS, Hart TK, Lee WM, Hoxie JA. 1996. An internalization signal in the simian immunodeficiency virus transmembrane protein cytoplasmic domain modulates expression of envelope glycoproteins on the cell surface. J. Cell Biol. 132:795-811.
43. LaBranche CC, Sauter MM, Haggarty BS, Vance PJ, Romano J, Hart TK, Bugelski PJ, Marsh M, Hoxie JA. 1995. A single amino acid change in the cytoplasmic domain of the simian immunodeficiency virus transmembrane molecule increases envelope glycoprotein expression on infected cells. J. Virol. 69:5217-5227.
44. Thomas DC, Roth MG. 1994. The basolateral targeting signal in the cytoplasmic domain of glycoprotein G from vesicular stomatitis virus resembles a variety of intracellular targeting motifs related by primary sequence but having diverse targeting activities. J. Biol. Chem. 269:15732-15739.
45. Kuroda MJ, Schmitz JE, Barouch DH, Craiu A, Allen TM, Sette A, Watkins DI, Forman MA, Letvin NL. 1998. Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J. Exp. Med. 187:1373-1381.
46. Cline AN, Bess JW, Piatak M, Jr. , Lifson JD. 2005. Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J. Med. Primatol. 34:303-312.
47. Ling B, Veazey RS, Luckay A, Penedo C, Xu K, Lifson JD, Marx PA. 2002. SIV(mac) pathogenesis in rhesus macaques of Chinese and Indian origin compared with primary HIV infections in humans. AIDS 16:1489-1496.
48. Van Rompay KK, Greenier JL, Cole KS, Earl P, Moss B, Steckbeck JD, Pahar B, Rourke T, Montelaro RC, Canfield DR, Tarara RP, Miller C, McChesney MB, Marthas ML. 2003. Immunization of newborn rhesus macaques with simian immunodeficiency virus (SIV) vaccines prolongs survival after oral challenge with virulent SIVmac251. J. Virol. 77:179-190.
49. Rotger M, Dalmau J, Rauch A, McLaren P, Bosinger SE, Martinez R, Sandler NG, Roque A, Liebner J, Battegay M, Bernasconi E, Descombes P, Erkizia I, Fellay J, Hirschel B, Miro JM, Palou E, Hoffmann M, Massanella M, Blanco J, Woods M, Gunthard HF, de Bakker P, Douek DC, Silvestri G, Martinez-Picado J, Telenti A. 2011. Comparative transcriptomics of extreme phenotypes of human HIV-1 infection and SIV infection in sooty mangabey and rhesus macaque. J. Clin. Invest. 121: 2391-2400.
50. Burdo TH, Soulas C, Orzechowski K, Button J, Krishnan A, Sugimoto C, Alvarez X, Kuroda MJ, Williams KC. 2010. Increased monocyte turnover from bone marrow correlates with severity of SIV encephalitis and CD163 levels in plasma. PLoS Pathog. 6:e1000842. doi:10.1371 /journal.ppat.1000842.
51. Hasegawa A, Liu H, Ling B, Borda JT, Alvarez X, Sugimoto C, Vinet- Oliphant H, Kim WK, Williams KC, Ribeiro RM, Lackner AA, Veazey RS, Kuroda MJ. 2009. The level of monocyte turnover predicts disease progression in the macaque model of AIDS. Blood 114:2917-2925.
52. + T cells occurs in the intestinal tract of neonatal rhesus macaques in acute SIV infection. Blood 109:1174-1181.
53. Vinet-Oliphant H, Alvarez X, Buza E, Borda JT, Mohan M, Aye PP, Tuluc F, Douglas SD, Lackner AA. 2010. Neurokinin-1 receptor (NK1-R) expression in the brains of SIV-infected rhesus macaques: implications for substance P in NK1-R immune cell trafficking into the CNS. Am. J. Pathol. 177:1286-1297.
54. *17-positive simian immunodeficiency virus-infected rhesus macaques. J. Virol. 82:5245-5254.
55. Ratai EM, Bombardier JP, Joo CG, Annamalai L, Burdo TH, Campbell J, Fell R, Hakimelahi R, He J, Autissier P, Lentz MR, Halpern EF, Masliah E, Williams KC, Westmoreland SV, Gonzalez RG. 2010. Proton magnetic resonance spectroscopy reveals neuroprotection by oral minocycline in a nonhuman primate model of accelerated NeuroAIDS. PLoS One 5:e10523. doi:10.1371/journal.pone.0010523.
56. Zink MC, Brice AK, Kelly KM, Queen SE, Gama L, Li M, Adams RJ, Bartizal C, Varrone J, Rabi SA, Graham DR, Tarwater PM, Mankowski JL, Clements JE. 2010. Simian immunodeficiency virus-infected macaques treated with highly active antiretroviral therapy have reduced central nervous system viral replication and inflammation but persistence of viral DNA. J. Infect. Dis. 202:161-170.
57. + T cells in multiple tissues during acute SIV infection. Nature 434:1093-1097.
58. Borda JT, Alarez X, Kondova I, Aye P, Simon MA, Desrosiers RC, Lackner AA. 2004. Cell tropism of simian immunodeficiency virus in culture is not predictive of in vivo tropism or pathogenesis. Am. J. Pathol. 165:2111-2122.
59. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, Lackner AA. 2001. Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J. Exp. Med. 193:905-915.
60. Sodora DL, Silvestri G. 2010. HIV, mucosal tissues, and T helper 17 cells: where we come from, where we are, and where we go from here. Curr. Opin. HIV AIDS 5:111-113.
61. Ancuta P, Kamat A, Kunstman KJ, Kim EY, Autissier P, Wurcel A, Zaman T, Stone D, Mefford M, Morgello S, Singer EJ, Wolinsky SM, Gabuzda D. 2008. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS One 3:e2516. doi:10.1371/journal.pone.0002516.
62. Benecke A, Gale M, Jr, Katze MG. 2012. Dynamics of innate immunity are key to chronic immune activation in AIDS. Curr. Opin. HIV AIDS 7:79-85.
63. Bosinger SE, Jacquelin B, Benecke A, Silvestri G, Muller-Trutwin M. 2012. Systems biology of natural simian immunodeficiency virus infections. Curr. Opin. HIV AIDS 7:71-78.
64. Harris LD, Tabb B, Sodora DL, Paiardini M, Klatt NR, Douek DC, Silvestri G, Muller-Trutwin M, Vasile-Pandrea I, Apetrei C, Hirsch V, Lifson J, Brenchley JM, Estes JD. 2010. Downregulation of robust acute type I interferon responses distinguishes nonpathogenic simian immuno- deficiency virus (SIV) infection of natural hosts from pathogenic SIV infection of rhesus macaques. J. Virol. 84:7886-7891.
65. Manches O, Bhardwaj N. 2009. Resolution of immune activation defines nonpathogenic SIV infection. J. Clin. Invest. 119:3512-3515.
66. Rowell JF, Stanhope PE, Siliciano RF. 1995. Endocytosis of endogenously synthesized HIV-1 envelope protein: mechanism and role in processing for association with class II MHC. J. Immunol. 155:473-488.
67. Lodge R, Lalonde JP, Lemay G, Cohen EA. 1997. The membraneproximal intracytoplasmic tyrosine residue of HIV-1 envelope glycoprotein is critical for basolateral targeting of viral budding in MDCK cells. EMBO J. 16:695-705.
68. Deschambeault J, Lalonde JP, Cervantes-Acosta G, Lodge R, Cohen EA, Lemay G. 1999. Polarized human immunodeficiency virus budding in lymphocytes involves a tyrosine-based signal and favors cell-to-cell viral transmission. J. Virol. 73:5010-5017.
69. Martin N, Sattentau Q. 2009. Cell-to-cell HIV-1 spread and its implications for immune evasion. Curr. Opin. HIV AIDS 4:143-149.
70. Chen P, Hubner W, Spinelli MA, Chen BK. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582-12595.
71. Hubner W, McNerney GP, Chen P, Dale BM, Gordon RE, Chuang FY, Li XD, Asmuth DM, Huser T, Chen BK. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743-1747.
72. Ansari AA, Reimann KA, Mayne AE, Takahashi Y, Stephenson ST, Wang R, Wang X, Li J, Price AA, Little DM, Zaidi M, Lyles R, Villinger F. 2011. Blocking of +47 gut-homing integrin during acute infection leads to decreased plasma and gastrointestinal tissue viral loads in simian immunodeficiency virus-infected rhesus macaques. J. Immunol. 186: 1044-1059.
73. Kwa S, Kannanganat S, Nigam P, Siddiqui M, Shetty RD, Armstrong W, Ansari A, Bosinger SE, Silvestri G, Amara RR. 2011. Plasmacytoid dendritic cells are recruited to the colorectum and contribute to immune activation during pathogenic SIV infection in rhesus macaques. Blood 118:2763-2773.
74. Arthos J, Cicala C, Martinelli E, Macleod K, Van Ryk D, Wei D, Xiao Z, Veenstra TD, Conrad TP, Lempicki RA, McLaughlin S, Pascuccio M, Gopaul R, McNally J, Cruz CC, Censoplano N, Chung E, Reitano KN, Kottilil S, Goode DJ, Fauci AS. 2008. HIV-1 envelope protein binds to and signals through integrin +47, the gut mucosal homing receptor for peripheral T cells. Nat. Immunol. 9:301-309.
75. Cicala C, Martinelli E, McNally JP, Goode DJ, Gopaul R, Hiatt J, Jelicic K, Kottilil S, Macleod K, O'Shea A, Patel N, Van Ryk D, Wei D, Pascuccio M, Yi L, McKinnon L, Izulla P, Kimani J, Kaul R, Fauci AS, Arthos J. 2009. The integrin alpha4beta7 forms a complex with cellsurface CD4 and defines a T-cell subset that is highly susceptible to infection by HIV-1. Proc. Natl. Acad. Sci. U. S. A. 106:20877-20882.
76. Byland R, Vance PJ, Hoxie JA, Marsh M. 2007. A conserved dileucine motif mediates clathrin and AP-2-dependent endocytosis of the HIV-1 envelope protein. Mol. Biol. Cell 18:414-425.
77. Mori K, Ringler DJ, Desrosiers RC. 1993. Restricted replication of simian immunodeficiency virus strain 239 in macrophages is determined by env but is not due to restricted entry. J. Virol. 67:2807-2814.
78. Mori K, Rosenzweig M, Desrosiers RC. 2000. Mechanisms for adaptation of simian immunodeficiency virus to replication in alveolar macrophages. J. Virol. 74:10852-10859.
79. + CD11c/123+ CD13+ CD14+ mononuclear cells are preferentially infected during acute simian immunodeficiency virus infection. J. Virol. 86:1069-1078.
80. Kim WK, Corey S, Alvarez X, Williams K. 2003. Monocyte/macrophage traffic in HIV and SIV encephalitis. J. Leukoc. Biol. 74:650-656.
81. Borda JT, Alvarez X, Mohan M, Hasegawa A, Bernardino A, Jean S, Aye P, Lackner AA. 2008. CD163, a marker of perivascular macrophages, is upregulated by microglia in simian immunodeficiency virus encephalitis after haptoglobin-hemoglobin complex stimulation and is suggestive of breakdown of the blood-brain barrier. Am. J. Pathol. 172:725-737.
82. Lane JH, Sasseville VG, Smith MO, Vogel P, Pauley DR, Heyes MP, Lackner AA. 1996. Neuroinvasion by simian immunodeficiency virus coincides with increased numbers of perivascular macrophages/microglia and intrathecal immune activation. J. Neurovirol. 2:423-432.
83. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, Lackner AA. 2001. Perivascular macrophages are the primary cell type productively infected by SIV in the brain of macaques: implications for the neuropathogenesis of AIDS. J. Exp. Med. 193:905-916.
84. Ganor Y, Zhou Z, Tudor D, Schmitt A, Vacher-Lavenu MC, Gibault L, Thiounn N, Tomasini J, Wolf JP, Bomsel M. 2010. Within 1 h, HIV-1 uses viral synapses to enter efficiently the inner, but not outer, foreskin mucosa and engages Langerhans-T cell conjugates. Mucosal Immunol. 3:506-522.
85. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, Southern PJ, Reilly CS, Peterson ML, Schultz-Darken N, Brunner KG, Nephew KR, Pambuccian S, Lifson JD, Carlis JV, Haase AT. 2009. Glycerol monolaurate prevents mucosal SIV transmission. Nature 458:1034-1038.
86. Stoltzfus CM, Madsen JM. 2006. Role of viral splicing elements and cellular RNA binding proteins in regulation of HIV-1 alternative RNA splicing. Curr. HIV Res. 4:43-55.
87. Ganser-Pornillos BK, Yeager M, Sundquist WI. 2008. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18:203-217.
88. Martin-Serrano J, Eastman SW, Chung W, Bieniasz PD. 2005. HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein- sorting pathway. J. Cell Biol. 168:89-101.
89. Cruz Jde L, Ali A, Ng HL, Yang OO. 2009. Disruption of an env tyrosine-dependent sorting signal does not affect susceptibility of HIV-1 to cytotoxic T lymphocytes. AIDS 23:1449-1451.
90. Klatt NR, Canary LA, Vanderford TH, Vinton CL, Engram JC, Dunham RM, Cronise HE, Swerczek JM, Lafont BA, Picker LJ, Silvestri G, Brenchley JM. 2011. Dynamics of simian immunodeficiency virus SIVmac239 infection in pigtail macaques. J. Virol. 86:1203-1213.