Phenotypic properties of transmitted founder HIV-1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 17, 2013, Pages 6626-6633

  Parrish, Nicholas F ^a,b   Gao, Feng ^c   Li, Hui ^a   Giorgi, Elena E ^d   Barbian, Hannah J ^a,b   Parrish, Erica H ^a   Zajic, Lara ^a   Iyer, Shilpa S ^a,b   Decker, Julie M ^e   Kumar, Amit ^c   Hora, Bhavna ^c   Berg, Anna ^c   Caic, Fangping ^c   Hopper, Jennifer ^c   Denny, Thomas N ^c   Ding, Haitao ^e   Ochsenbauer, Christina ^e   Kappes, John C ^e   Galimidi, Rachel P ^f   West, Anthony P ^f   Bjorkman, Pamela J ^f   Wilen, Craig B ^a,b   Doms, Robert W ^b,g   O'Brien, Meagan ^h   Bhardwaj, Nina ^h   Borrow, Persephone ⁱ   Haynes, Barton F ^c   Muldoon, Mark ^j   Theiler, James P ^d   Korber, Bette ^d   Shaw, George M ^a,b   Hahn, Beatrice H ^a,b   more..

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

^e University of Alabama at Birmingham   (United States)

^f CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^g CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^h NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

^j UNIVERSITY OF MANCHESTER   (United Kingdom)

more..

Author keywords

Acute HIV 1 infection; Epidemic HIV 1 spread; Innate immunity; Mucosal HIV 1 transmission

Indexed keywords

ALPHA INTERFERON;

ARTICLE; CD4+ T LYMPHOCYTE; CELL INTERACTION; CELL TRANSFER; CONTROLLED STUDY; DENDRITIC CELL; ENVELOPE GENE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTIOUS MOLECULAR CLONE; KINETICS; MOLECULAR CLONING; MONOCYTE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TRANSMITTED FOUNDER VIRUS; VIRION; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TRANSMISSION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84876867850     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1304288110     Document Type: Article

References (83)

1. Shaw GM, Hunter E (2012) HIV transmission. Cold Spring Harb Perspect Med 2(11):pii: a006965.
2. Hladik F, McElrath MJ (2008) Setting the stage: Host invasion by HIV. Nat Rev Immunol 8(6):447-457.
3. Zhang Z, et al. (1999) Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286(5443):1353-1357.
4. Li Q, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458(7241):1034-1038.
5. Stacey AR, et al. (2009) Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 83(8): 3719-3733.
6. Schacker T, et al. (2001) Productive infection of T cells in lymphoid tissues during primary and early human immunodeficiency virus infection. J Infect Dis 183(4): 555-562.
7. Moss GB, et al. (1991) Association of cervical ectopy with heterosexual transmission of human immunodeficiency virus: Results of a study of couples in Nairobi, Kenya. J Infect Dis 164(3):588-591.
8. Gray RH, et al. (2001) Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357(9263):1149-1153.
9. Liu R, et al. (1996) Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86(3):367-377.
10. Zhu J, et al. (2009) Persistence of HIV-1 receptor-positive cells after HSV-2 reactivation is a potential mechanism for increased HIV-1 acquisition. Nat Med 15(8):886-892.
11. McLaren PJ, et al. (2010) HIV-exposed seronegative commercial sex workers show a quiescent phenotype in the CD4+ T cell compartment and reduced expression of HIV-dependent host factors. J Infect Dis 202(Suppl 3):S339-S344.
12. Laga M, et al. (1993) Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: Results from a cohort study. AIDS 7(1):95-102.
13. Atashili J, Poole C, Ndumbe PM, Adimora AA, Smith JS (2008) Bacterial vaginosis and HIV acquisition: A meta-analysis of published studies. AIDS 22(12):1493-1501.
14. Boeras DI, et al. (2011) Role of donor genital tract HIV-1 diversity in the transmission bottleneck. Proc Natl Acad Sci USA 108(46):E1156-E1163.
15. Bull ME, et al. (2013) Human immunodeficiency viruses appear compartmentalized to the female genital tract in cross-sectional analyses but genital lineages do not persist over time. J Infect Dis, in press.
16. Keele BF, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci USA 105(21): 7552-7557.
17. Derdeyn CA, et al. (2004) Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303(5666):2019-2022.
18. Chohan B, et al. (2005) Selection for human immunodeficiency virus type 1 envelope glycosylation variants with shorter V1-V2 loop sequences occurs during transmission of certain genetic subtypes and may impact viral RNA levels. J Virol 79(10):6528-6531.
19. Li B, et al. (2006) Evidence for potent autologous neutralizing antibody titers and compact envelopes in early infection with subtype C human immunodeficiency virus type 1. J Virol 80(11):5211-5218.
20. Liu Y, et al. (2008) Env length and N-linked glycosylation following transmission of human immunodeficiency virus Type 1 subtype B viruses. Virology 374(2):229-233.
21. Curlin ME, et al. (2010) HIV-1 envelope subregion length variation during disease progression. PLoS Pathog 6(12):e1001228.
22. Gnanakaran S, et al. (2011) Recurrent signature patterns in HIV-1 B clade envelope glycoproteins associated with either early or chronic infections. PLoS Pathog 7(9): e1002209.
23. Alexander M, et al. (2010) Donor and recipient envs from heterosexual human immunodeficiency virus subtype C transmission pairs require high receptor levels for entry. J Virol 84(8):4100-4104.
24. Isaacman-Beck J, et al. (2009) Heterosexual transmission of human immunodeficiency virus type 1 subtype C: Macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization. J Virol 83(16):8208-8220.
25. Zhang H, et al. (2010) Functional properties of the HIV-1 subtype C envelope glyco-protein associated with mother-to-child transmission. Virology 400(2):164-174.
26. Nawaz F, et al. (2011) The genotype of early-transmitting HIV gp120s promotes α (4) β(7)-reactivity, revealing α (4) β(7) +/CD4+ T cells as key targets in mucosal transmission. PLoS Pathog 7(2):e1001301.
27. Salazar-Gonzalez JF, et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82(8):3952-3970.
28. Wilen CB, et al. (2011) Phenotypic and immunologic comparison of clade B transmitted/founder and chronic HIV-1 envelope glycoproteins. J Virol 85(17):8514-8527.
29. Parrish NF, et al. (2012) Transmitted/founder and chronic subtype C HIV-1 use CD4 and CCR5 receptors with equal efficiency and are not inhibited by blocking the integrin α4β7. PLoS Pathog 8(5):e1002686.
30. Parker ZF, et al. (2013) Transmitted/founder and chronic HIV-1 envelope proteins are distinguished by differential utilization of CCR5. J Virol 87(5):2401-2411.
31. Salazar-Gonzalez JF, et al. (2009) Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 206(6):1273-1289.
32. Li H, et al. (2010) High multiplicity infection by HIV-1 in men who have sex with men. PLoS Pathog 6(5):e1000890.
33. Ochsenbauer C, et al. (2012) 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 86(5):2715-2728.
34. Jiang C, et al. (2011) Primary infection by a human immunodeficiency virus with atypical coreceptor tropism. J Virol 85(20):10669-10681.
35. Ma ZM, et al. (2009) High specific infectivity of plasma virus from the pre-ramp-up and ramp-up stages of acute simian immunodeficiency virus infection. J Virol 83(7): 3288-3297.
36. Platt EJ, Kozak SL, Durnin JP, Hope TJ, Kabat D (2010) Rapid dissociation of HIV-1 from cultured cells severely limits infectivity assays, causes the inactivation ascribed to entry inhibitors, and masks the inherently high level of infectivity of virions. J Virol 84(6): 3106-3110.
37. Asmal M, et al. (2011) A signature in HIV-1 envelope leader peptide associated with transition from acute to chronic infection impacts envelope processing and infectivity. PLoS One 6(8):e23673.
38. West AP, Jr., et al. (2010) Evaluation of CD4-CD4i antibody architectures yields potent, broadly cross-reactive anti-human immunodeficiency virus reagents. J Virol 84(1): 261-269.
39. Hladik F, et al. (2007) Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 26(2):257-270.
40. Fahrbach KM, Barry SM, Anderson MR, Hope TJ (2010) Enhanced cellular responses and environmental sampling within inner foreskin explants: Implications for the foreskin's role in HIV transmission. Mucosal Immunol 3(4):410-418.
41. Geijtenbeek TB, et al. (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100(5):587-597.
42. Turville SG, et al. (2002) Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3(10):975-983.
43. Puryear WB, Yu X, Ramirez NP, Reinhard BM, Gummuluru S (2012) HIV-1 incorporation of host-cell-derived glycosphingolipid GM3 allows for capture by mature dendritic cells. Proc Natl Acad Sci USA 109(19):7475-7480.
44. Cameron PU, et al. (1992) Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257(5068): 383-387.
45. Fahrbach KM, et al. (2007) Activated CD34-derived Langerhans cells mediate tran-sinfection with human immunodeficiency virus. J Virol 81(13):6858-6868.
46. Ballweber L, et al. (2011) Vaginal langerhans cells nonproductively transporting HIV-1 mediate infection of T cells. J Virol 85(24):13443-13447.
47. Pöhlmann S, et al. (2001) DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus. J Virol 75(10):4664-4672.
48. Gummuluru S, Rogel M, Stamatatos L, Emerman M (2003) Binding of human immunodeficiency virus type 1 to immature dendritic cells can occur independently of DC-SIGN and mannose binding C-type lectin receptors via a cholesterol-dependent pathway. J Virol 77(23):12865-12874.
49. Mehandru S, et al. (2004) Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 200(6):761-770.
50. Siegal FP, et al. (1999) The nature of the principal type 1 interferon-producing cells in human blood. Science 284(5421):1835-1837.
51. Der SD, Zhou A, Williams BR, Silverman RH (1998) Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 95(26):15623-15628.
52. Schoggins JW, et al. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472(7344):481-485.
53. Hansen BD, et al. (1992) Loss of infectivity by progeny virus from alpha interferon-treated human immunodeficiency virus type 1-infected T cells is associated with defective assembly of envelope gp120. J Virol 66(12):7543-7548.
54. Chertova E, et al. (2002) Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol 76(11):5315-5325.
55. Yang X, Kurteva S, Ren X, Lee S, Sodroski J (2005) Stoichiometry of envelope glyco-protein trimers in the entry of human immunodeficiency virus type 1. J Virol 79(19): 12132-12147.
56. Bachrach E, et al. (2005) Effects of virion surface gp120 density on infection by HIV-1 and viral production by infected cells. Virology 332(1):418-429.
57. Martellini JA, et al. (2009) Cationic polypeptides contribute to the anti-HIV-1 activity of human seminal plasma. FASEB J 23(10):3609-3618.
58. Ongradi J, Ceccherini-Nelli L, Pistello M, Specter S, Bendinelli M (1990) Acid sensitivity of cell-free and cell-associated HIV-1: Clinical implications. AIDS Res Hum Retroviruses 6(12):1433-1436.
59. Izquierdo-Useros N, et al. (2007) Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J Virol 81(14): 7559-7570.
60. Granelli-Piperno A, et al. (1996) Efficient interaction of HIV-1 with purified dendritic cells via multiple chemokine coreceptors. J Exp Med 184(6):2433-2438.
61. Spira AI, et al. (1996) Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J Exp Med 183(1):215-225.
62. Hsu M, et al. (2003) Increased mucosal transmission but not enhanced pathogenicity of the CCR5-tropic, simian AIDS-inducing simian/human immunodeficiency virus SHIV (SF162P3) maps to envelope gp120. J Virol 77(2):989-998.
63. Wang Y, et al. (2005) The Toll-like receptor 7 (TLR7) agonist, imiquimod, and the TLR9 agonist, CpG ODN, induce antiviral cytokines and chemokines but do not prevent vaginal transmission of simian immunodeficiency virus when applied intravaginally to rhesus macaques. J Virol 79(22):14355-14370.
64. Sandler N, et al. (2013) Blockade of Type I Interferon During Acute SIV Infection Results in Accelerated Progression to AIDS and Death. The Conference on Retro-viruses and Opportunistic Infections: March 3-6, 2013 (Atlanta, Georgia). Available at http://www.retroconference.org/2013b/Abstracts/46260.htm. Accessed March 17, 2013.
65. Hirbod T, et al. (2006) Upregulation of interferon-alpha and RANTES in the cervix of HIV-1-seronegative women with high-risk behavior. J Acquir Immune Defic Syndr 43(2):137-143.
66. Ball TB, et al. (2007) Polymorphisms in IRF-1 associated with resistance to HIV-1 infection in highly exposed uninfected Kenyan sex workers. AIDS 21(9):1091-1101.
67. Vendrame D, Sourisseau M, Perrin V, Schwartz O, Mammano F (2009) Partial inhibition of human immunodeficiency virus replication by type I interferons: Impact of cell-to-cell viral transfer. J Virol 83(20):10527-10537.
68. Yasuda Y, et al. (1990) Interferon-alpha treatment leads to accumulation of virus particles on the surface of cells persistently infected with the human immunodeficiency virus type 1. J Acquir Immune Defic Syndr 3(11):1046-1051.
69. Neil SJ, Zang T, Bieniasz PD (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451(7177):425-430.
70. Sheehy AM, Gaddis NC, Choi JD, Malim MH (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418(6898): 646-650.
71. Schröder HC, et al. (1990) Binding of Tat protein to TAR region of human immunodeficiency virus type 1 blocks TAR-mediated activation of (2′-5′)oligoadenylate syn-thetase. AIDS Res Hum Retroviruses 6(5):659-672.
72. Roy S, et al. (1990) Control of the interferon-induced 68-kilodalton protein kinase by the HIV-1 tat gene product. Science 247(4947):1216-1219.
73. Barr SD, Smiley JR, Bushman FD (2008) The interferon response inhibits HIV particle production by induction of TRIM22. PLoS Pathog 4(2):e1000007.
74. Reynolds MR, et al. (2011) The TRIM5α genotype of rhesus macaques affects acquisition of simian immunodeficiency virus SIVsmE660 infection after repeated limiting-dose intrarectal challenge. J Virol 85(18):9637-9640.
75. Yeh WW, et al. (2011) The TRIM5 gene modulates penile mucosal acquisition of simian immunodeficiency virus in rhesus monkeys. J Virol 85(19):10389-10398.
76. Jeeninga RE, et al. (2000) Functional differences between the long terminal repeat transcriptional promoters of human immunodeficiency virus type 1 subtypes A through G. J Virol 74(8):3740-3751.
77. Bachu M, et al. (2012) Multiple NF-κB sites in HIV-1 subtype C long terminal repeat confer superior magnitude of transcription and thereby the enhanced viral predominance. J Biol Chem 287(53):44714-44735.
78. Spotts DR, Reich RM, Kalkhan MA, Kinney RM, Roehrig JT (1998) Resistance to alpha/beta interferons correlates with the epizootic and virulence potential of Venezuelan equine encephalitis viruses and is determined by the 5′ noncoding region and gly-coproteins. J Virol 72(12):10286-10291.
79. Charleston B, Fray MD, Baigent S, Carr BV, Morrison WI (2001) Establishment of persistent infection with non-cytopathic bovine viral diarrhoea virus in cattle is associated with a failure to induce type I interferon. J Gen Virol 82(Pt 8):1893-1897.
80. Meier A, et al. (2009) Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat Med 15(8):955-959.
81. Klein JS, Bjorkman PJ (2010) Few and far between: How HIV may be evading antibody avidity. PLoS Pathog 6(5):e1000908.
82. Li H, et al. (2012) Elucidation of hepatitis C virus transmission and early diversification by single genome sequencing. PLoS Pathog 8(8):e1002880.
83. Biancotto A, et al. (2009) A highly sensitive and dynamic immunofluorescent cyto-metric bead assay for the detection of HIV-1 p24. J Virol Methods 157(1):98-101.