Postnatally-transmitted HIV-1 Envelope variants have similar neutralization-sensitivity and function to that of nontransmitted breast milk variants

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Fouda, Genevieve G ^a   Mahlokozera, Tatenda ^a   Salazar Gonzalez, Jesus F ^b   Salazar, Maria G ^b   Learn, Gerald ^c   Kumar, Surender B ^d   Dennison, S Moses ^a   Russell, Elizabeth ^e,f   Rizzolo, Katherine ^g   Jaeger, Frederick ^a   Cai, Fangping ^a   Vandergrift, Nathan A ^a   Gao, Feng ^a   Hahn, Beatrice ^c   Shaw, George M ^c   Ochsenbauer, Christina ^b   Swanstrom, Ronald ^e,f   Meshnick, Steve ^e,f   Mwapasa, Victor ^h   Kalilani, Linda ^h   Fiscus, Susan ^e,f   Montefiori, David ^a   Haynes, Barton ^a   Kwiek, Jesse ^d   Alam, S Munir ^a   Permar, Sallie R ^a   more..

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d OHIO STATE UNIVERSITY   (United States)

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

^f IL   (United States)

^g BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^h UNIVERSITY OF MALAWI   (Malawi)

Author keywords

Dendritic cells; Galcer; HIV; Mother to child transmission; Neutralizing antibodies

Indexed keywords

CHEMOKINE RECEPTOR CCR5; MATERNAL ANTIBODY; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY;

ADULT; ARTICLE; BREAST MILK; CELL FUSION; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTESTINE MUCOSA PERMEABILITY; MATERNAL PLASMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PERMEABILITY BARRIER; RECEPTOR UPREGULATION; TARGET CELL; UNINDEXED SEQUENCE; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS ISOLATION; VIRUS LOAD; VIRUS NEUTRALIZATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANTIBODIES, NEUTRALIZING; BREAST FEEDING; COHORT STUDIES; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; GASTROINTESTINAL TRACT; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; INFANT; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MILK, HUMAN; NEUTRALIZATION TESTS; PHYLOGENY; SEQUENCE ANALYSIS, RNA; VIRAL LOAD;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84872117539     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-3     Document Type: Article

References (91)

1. WHO PMTCT strategic vision 2010-2015: Preventing mother-to-child transmission of HIV to reach the UNGASS and Millennium Development Goals 2010, Geneva, Switzerland: WHO Press, WHO.
2. Nduati R, John G, Mbori-Ngacha D, Richardson B, Overbaugh J, Mwatha A, Ndinya-Achola J, Bwayo J, Onyango FE, Hughes J, Kreiss J. Effect of breastfeeding and formula feeding on transmission of HIV-1: a randomized clinical trial. JAMA 2000, 283:1167-1174. 10.1001/jama.283.9.1167, 10703779.
3. Miotti PG, Taha TE, Kumwenda NI, Broadhead R, Mtimavalye LA, Van der Hoeven L, Chiphangwi JD, Liomba G, Biggar RJ. HIV transmission through breastfeeding: a study in Malawi. JAMA 1999, 282:744-749. 10.1001/jama.282.8.744, 10463709.
4. Lewis P, Nduati R, Kreiss JK, John GC, Richardson BA, Mbori-Ngacha D, Ndinya-Achola J, Overbaugh J. Cell-free human immunodeficiency virus type 1 in breast milk. J Infect Dis 1998, 177:34-39. 10.1086/513816, 3358132, 9419167.
5. Van de Perre P, Simonon A, Hitimana DG, Dabis F, Msellati P, Mukamabano B, Butera JB, Van Goethem C, Karita E, Lepage P. Infective and anti-infective properties of breastmilk from HIV-1-infected women. Lancet 1993, 341:914-918. 10.1016/0140-6736(93)91210-D, 8096264.
6. John GC, Nduati RW, Mbori-Ngacha DA, Richardson BA, Panteleeff D, Mwatha A, Overbaugh J, Bwayo J, Ndinya-Achola JO, Kreiss JK. Correlates of mother-to-child human immunodeficiency virus type 1 (HIV-1) transmission: association with maternal plasma HIV-1 RNA load, genital HIV-1 DNA shedding, and breast infections. J Infect Dis 2001, 183:206-212. 10.1086/317918, 11120927.
7. Ahmad N, Baroudy BM, Baker RC, Chappey C. Genetic analysis of human immunodeficiency virus type 1 envelope V3 region isolates from mothers and infants after perinatal transmission. J Virol 1995, 69:1001-1012. 188669, 7815476.
8. Scarlatti G, Leitner T, Halapi E, Wahlberg J, Marchisio P, Clerici-Schoeller MA, Wigzell H, Fenyo EM, Albert J, Uhlen M, et al. Comparison of variable region 3 sequences of human immunodeficiency virus type 1 from infected children with the RNA and DNA sequences of the virus populations of their mothers. Proc Natl Acad Sci USA 1993, 90:1721-1725. 10.1073/pnas.90.5.1721, 45951, 8446584.
9. Kwiek JJ, Russell ES, Dang KK, Burch CL, Mwapasa V, Meshnick SR, Swanstrom R. The molecular epidemiology of HIV-1 envelope diversity during HIV-1 subtype C vertical transmission in Malawian mother-infant pairs. AIDS 2008, 22:863-871. 10.1097/QAD.0b013e3282f51ea0, 2760232, 18427205.
10. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, Ping LH, Athreya GS, Treurnicht FK, Keele BF, Wood N, et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J Virol 2009, 83:3556-3567. 10.1128/JVI.02132-08, 2663249, 19193811.
11. Rainwater SM, Wu X, Nduati R, Nedellec R, Mosier D, John-Stewart G, Mbori-Ngacha D, Overbaugh J. Cloning and characterization of functional subtype A HIV-1 envelope variants transmitted through breastfeeding. Curr HIV Res 2007, 5:189-197. 10.2174/157016207780076986, 17346133.
12. Chohan B, Lang D, Sagar M, Korber B, Lavreys L, Richardson B, Overbaugh J. 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 2005, 79:6528-6531. 10.1128/JVI.79.10.6528-6531.2005, 1091724, 15858037.
13. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, Denham SA, Heil ML, Kasolo F, Musonda R, Hahn BH, et al. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 2004, 303:2019-2022. 10.1126/science.1093137, 15044802.
14. Russell ES, Kwiek JJ, Keys J, Barton K, Mwapasa V, Montefiori DC, Meshnick SR, Swanstrom R. The genetic bottleneck in vertical transmission of subtype C HIV-1 is not driven by selection of especially neutralization-resistant virus from the maternal viral population. J Virol 2011, 85:8253-8262. 10.1128/JVI.00197-11, 3147968, 21593171.
15. Sagar M, Wu X, Lee S, Overbaugh J. Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity. J Virol 2006, 80:9586-9598. 10.1128/JVI.00141-06, 1617272, 16973562.
16. Gnanakaran S, Bhattacharya T, Daniels M, Keele BF, Hraber PT, Lapedes AS, Shen T, Gaschen B, Krishnamoorthy M, Li H, et al. Recurrent signature patterns in HIV-1 B clade envelope glycoproteins associated with either early or chronic infections. PLoS Pathog 2011, 7:e1002209. 10.1371/journal.ppat.1002209, 3182927, 21980282.
17. Asmal M, Hellmann I, Liu W, Keele BF, Perelson AS, Bhattacharya T, Gnanakaran S, Daniels M, Haynes BF, Korber BT, et al. A signature in HIV-1 envelope leader peptide associated with transition from acute to chronic infection impacts envelope processing and infectivity. PLoS One 2011, 6:e23673. 10.1371/journal.pone.0023673, 3158090, 21876761.
18. 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.
19. 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.
20. Wilen CB, Parrish NF, Pfaff JM, Decker JM, Henning EA, Haim H, Petersen JE, Wojcechowskyj JA, Sodroski J, Haynes BF, et al. Phenotypic and immunologic comparison of clade B transmitted/founder and chronic HIV-1 envelope glycoproteins. J Virol 2011, 85:8514-8527. 10.1128/JVI.00736-11, 3165820, 21715507.
21. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliveira TY, Pietzsch J, Fenyo D, Abadir A, Velinzon K, et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 2011, 333:1633-1637. 10.1126/science.1207227, 3351836, 21764753.
22. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 2010, 329:856-861. 10.1126/science.1187659, 2965066, 20616233.
23. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL, et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 2009, 326:285-289. 10.1126/science.1178746, 3335270, 19729618.
24. Bonsignori M, Montefiori DC, Wu X, Chen X, Hwang KK, Tsao CY, Kozink DM, Parks RJ, Tomaras GD, Crump JA, et al. Two Distinct Broadly Neutralizing Antibody Specificities of Different Clonal Lineages in a Single HIV-1-Infected Donor: Implications for Vaccine Design. J Virol 2012, 86:4688-4692. 10.1128/JVI.07163-11, 3318651, 22301150.
25. Hofmann-Lehmann R, Vlasak J, Rasmussen RA, Smith BA, Baba TW, Liska V, Ferrantelli F, Montefiori DC, McClure HM, Anderson DC, et al. Postnatal passive immunization of neonatal macaques with a triple combination of human monoclonal antibodies against oral simian-human immunodeficiency virus challenge. J Virol 2001, 75:7470-7480. 10.1128/JVI.75.16.7470-7480.2001, 114982, 11462019.
26. Ferrantelli F, Rasmussen RA, Buckley KA, Li PL, Wang T, Montefiori DC, Katinger H, Stiegler G, Anderson DC, McClure HM, Ruprecht RM. Complete protection of neonatal rhesus macaques against oral exposure to pathogenic simian-human immunodeficiency virus by human anti-HIV monoclonal antibodies. J Infect Dis 2004, 189:2167-2173. 10.1086/420833, 15181562.
27. Wu X, Parast AB, Richardson BA, Nduati R, John-Stewart G, Mbori-Ngacha D, Rainwater SM, Overbaugh J. Neutralization escape variants of human immunodeficiency virus type 1 are transmitted from mother to infant. J Virol 2006, 80:835-844. 10.1128/JVI.80.2.835-844.2006, 1346878, 16378985.
28. Zhang H, Rola M, West JT, Tully DC, Kubis P, He J, Kankasa C, Wood C. Functional properties of the HIV-1 subtype C envelope glycoprotein associated with mother-to-child transmission. Virology 2010, 400:164-174. 10.1016/j.virol.2009.12.019, 2844456, 20096914.
29. Goo L, Milligan C, Simonich CA, Nduati R, Overbaugh J. Neutralizing Antibody Escape during HIV-1 Mother-to-Child Transmission Involves Conformational Masking of Distal Epitopes in Envelope. J Virol 2012,
30. Lynch JB, Nduati R, Blish CA, Richardson BA, Mabuka JM, Jalalian-Lechak Z, John-Stewart G, Overbaugh J. The breadth and potency of passively acquired human immunodeficiency virus type 1-specific neutralizing antibodies do not correlate with the risk of infant infection. J Virol 2011, 85:5252-5261. 10.1128/JVI.02216-10, 3094986, 21411521.
31. Fouda GG, Yates NL, Pollara J, Shen X, Overman GR, Mahlokozera T, Wilks AB, Kang HH, Salazar-Gonzalez JF, Salazar MG, et al. HIV-specific functional antibody responses in breast milk mirror those in plasma and are primarily mediated by IgG antibodies. J Virol 2011, 85:9555-9567. 10.1128/JVI.05174-11, 3165739, 21734046.
32. Dickover R, Garratty E, Yusim K, Miller C, Korber B, Bryson Y. Role of maternal autologous neutralizing antibody in selective perinatal transmission of human immunodeficiency virus type 1 escape variants. J Virol 2006, 80:6525-6533. 10.1128/JVI.02658-05, 1488973, 16775339.
33. Salazar-Gonzalez JF, Salazar MG, Learn GH, Fouda GG, Kang HH, Mahlokozera T, Wilks AB, Lovingood RV, Stacey A, Kalilani L, et al. Origin and evolution of HIV-1 in breast milk determined by single-genome amplification and sequencing. J Virol 2011, 85:2751-2763. 10.1128/JVI.02316-10, 3067940, 21191008.
34. Aizire J, McConnell MS, Mudiope P, Mubiru M, Matovu F, Parsons TL, Elbireer A, Nolan M, Janoff EN, Fowler MG. Kinetics of nevirapine and its impact on HIV-1 RNA levels in maternal plasma and breast milk over time after perinatal single-dose nevirapine. J Acquir Immune Defic Syndr 2012, 60:483-488. 10.1097/QAI.0b013e318246bf9e, 22217678.
35. Russell ES, Ojeda S, Fouda G, Meshnick SR, Montefiori D, Permar SR, Swanstrom R. HIV-1 subtype C variants transmitted through the bottleneck of breastfeeding are sensitive to new generation broadly-neutralizing antibodies directed against quaternary and CD4-binding site epitopes. AIDS Res Hum Retroviruses 2012,
36. Rolland M, Edlefsen PT, Larsen BB, Tovanabutra S, Sanders-Buell E, Hertz T, Decamp AC, Carrico C, Menis S, Magaret CA, et al. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 2012,
37. Kumar SB, Handelman SK, Voronkin I, Mwapasa V, Janies D, Rogerson SJ, Meshnick SR, Kwiek JJ. Different regions of HIV-1 subtype C env are associated with placental localization and in utero mother-to-child transmission. J Virol 2011, 85:7142-7152. 10.1128/JVI.01955-10, 3126595, 21543508.
38. Yahi N, Baghdiguian S, Moreau H, Fantini J. Galactosyl ceramide (or a closely related molecule) is the receptor for human immunodeficiency virus type 1 on human colon epithelial HT29 cells. J Virol 1992, 66:4848-4854. 241313, 1378511.
39. Shattock RJ, Moore JP. Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol 2003, 1:25-34. 10.1038/nrmicro729, 15040177.
40. Friedman J, Alam SM, Shen X, Xia S, Stewart S, Anasti K, Pollara J, Fouda GG, Yang G, Kelsoe G, Ferrari G, Tomaras GD, Haynes BF, Liao H, Moody MA, Permar SR. Isolation of HIV-1-neutralizing mucosal monoclonal antibodies from human colostrum. PLoS One 2012, in press.
41. Newburg DS. Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans. J Anim Sci 2009, 87:26-34.
42. Nwosu CC, Aldredge DL, Lee H, Lerno LA, Zivkovic AM, German JB, Lebrilla CB. Comparison of the human and bovine milk N-glycome via high-performance microfluidic chip liquid chromatography and tandem mass spectrometry. J Proteome Res 2012, 11:2912-2924. 10.1021/pr300008u, 22439776.
43. Carthagena L, Becquart P, Hocini H, Kazatchkine MD, Bouhlal H, Belec L. Modulation of HIV Binding to Epithelial Cells and HIV Transfer from Immature Dendritic Cells to CD4 T Lymphocytes by Human Lactoferrin and its Major Exposed LF-33 Peptide. Open Virol J 2011, 5:27-34. 10.2174/1874357901105010027, 3109640, 21660187.
44. Holla A, Skerra A. Comparative analysis reveals selective recognition of glycans by the dendritic cell receptors DC-SIGN and Langerin. Protein Eng Des Sel 2011, 24:659-669. 10.1093/protein/gzr016, 21540232.
45. de Ferrer PA R, Baroni A, Sambucetti ME, Lopez NE, Ceriani Cernadas JM. Lactoferrin levels in term and preterm milk. J Am Coll Nutr 2000, 19:370-373.
46. Cavalli C, Teng C, Battaglia FC, Bevilacqua G. Free sugar and sugar alcohol concentrations in human breast milk. J Pediatr Gastroenterol Nutr 2006, 42:215-221. 10.1097/01.mpg.0000189341.38634.77, 16456418.
47. Lin G, Simmons G, Pohlmann S, Baribaud F, Ni H, Leslie GJ, Haggarty BS, Bates P, Weissman D, Hoxie JA, Doms RW. Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR. J Virol 2003, 77:1337-1346. 10.1128/JVI.77.2.1337-1346.2003, 140807, 12502850.
48. Parrish NF, Wilen CB, Banks LB, Iyer SS, Pfaff JM, Salazar-Gonzalez JF, Salazar MG, Decker JM, Parrish EH, Berg A, et al. Transmitted/founder and chronic subtype C HIV-1 use CD4 and CCR5 receptors with equal efficiency and are not inhibited by blocking the integrin alpha4beta7. PLoS Pathog 2012, 8:e1002686. 10.1371/journal.ppat.1002686, 3364951, 22693444.
49. Harmsen MC, Swart PJ, de Bethune MP, Pauwels R, De Clercq E, The TH, Meijer DK. Antiviral effects of plasma and milk proteins: lactoferrin shows potent activity against both human immunodeficiency virus and human cytomegalovirus replication in vitro. J Infect Dis 1995, 172:380-388. 10.1093/infdis/172.2.380, 7622881.
50. Wahl A, Swanson MD, Nochi T, Olesen R, Denton PW, Chateau M, Garcia JV. Human Breast Milk and Antiretrovirals Dramatically Reduce Oral HIV-1 Transmission in BLT Humanized Mice. PLoS Pathog 2012, 8:e1002732. 10.1371/journal.ppat.1002732, 3380612, 22737068.
51. Li M, Salazar-Gonzalez JF, Derdeyn CA, Morris L, Williamson C, Robinson JE, Decker JM, Li Y, Salazar MG, Polonis VR, et al. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J Virol 2006, 80:11776-11790. 10.1128/JVI.01730-06, 1642599, 16971434.
52. Gray ES, Meyers T, Gray G, Montefiori DC, Morris L. Insensitivity of paediatric HIV-1 subtype C viruses to broadly neutralising monoclonal antibodies raised against subtype B. PLoS Med 2006, 3:e255. 10.1371/journal.pmed.0030255, 1502151, 16834457.
53. Falkowska E, Ramos A, Feng Y, Zhou T, Moquin S, Walker LM, Wu X, Seaman MS, Wrin T, Kwong PD, et al. PG V04, an HIV-1 gp120 CD4 binding site antibody, is broad and potent in neutralization but does not induce conformational changes characteristic of CD4. J Virol 2012,
54. Wolinsky SM, Wike CM, Korber BT, Hutto C, Parks WP, Rosenblum LL, Kunstman KJ, Furtado MR, Munoz JL. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 1992, 255:1134-1137. 10.1126/science.1546316, 1546316.
55. Hocini H, Belec L, Iscaki S, Garin B, Pillot J, Becquart P, Bomsel M. High-level ability of secretory IgA to block HIV type 1 transcytosis: contrasting secretory IgA and IgG responses to glycoprotein 160. AIDS Res Hum Retroviruses 1997, 13:1179-1185. 10.1089/aid.1997.13.1179, 9310284.
56. Bomsel M. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat Med 1997, 3:42-47. 10.1038/nm0197-42, 8986739.
57. Bobardt MD, Chatterji U, Selvarajah S, Van der Schueren B, David G, Kahn B, Gallay PA. Cell-free human immunodeficiency virus type 1 transcytosis through primary genital epithelial cells. J Virol 2007, 81:395-405. 10.1128/JVI.01303-06, 1797244, 17050597.
58. Alfsen A, Bomsel M. HIV-1 gp41 envelope residues 650-685 exposed on native virus act as a lectin to bind epithelial cell galactosyl ceramide. J Biol Chem 2002, 277:25649-25659. 10.1074/jbc.M200554200, 11940580.
59. Fantini J, Cook DG, Nathanson N, Spitalnik SL, Gonzalez-Scarano F. Infection of colonic epithelial cell lines by type 1 human immunodeficiency virus is associated with cell surface expression of galactosylceramide, a potential alternative gp120 receptor. Proc Natl Acad Sci USA 1993, 90:2700-2704. 10.1073/pnas.90.7.2700, 46163, 8464878.
60. Yu H, Alfsen A, Tudor D, Bomsel M. The binding of HIV-1 gp41 membrane proximal domain to its mucosal receptor, galactosyl ceramide, is structure-dependent. Cell Calcium 2008, 43:73-82. 10.1016/j.ceca.2007.04.011, 17553560.
61. Tugizov SM, Herrera R, Veluppillai P, Greenspan D, Soros V, Greene WC, Levy JA, Palefsky JM. Differential transmission of HIV traversing fetal oral/intestinal epithelia and adult oral epithelia. J Virol 2012, 86:2556-2570. 10.1128/JVI.06578-11, 3302289, 22205732.
62. Groot F, Geijtenbeek TB, Sanders RW, Baldwin CE, Sanchez-Hernandez M, Floris R, van Kooyk Y, de Jong EC, Berkhout B. Lactoferrin prevents dendritic cell-mediated human immunodeficiency virus type 1 transmission by blocking the DC-SIGN-gp120 interaction. J Virol 2005, 79:3009-3015. 10.1128/JVI.79.5.3009-3015.2005, 548463, 15709021.
63. Kishko M, Somasundaran M, Brewster F, Sullivan JL, Clapham PR, Luzuriaga K. Genotypic and functional properties of early infant HIV-1 envelopes. Retrovirology 2011, 8:67. 10.1186/1742-4690-8-67, 3189118, 21843318.
64. Diomede L, Nyoka S, Pastori C, Scotti L, Zambon A, Sherman G, Gray CM, Sarzotti-Kelsoe M, Lopalco L. Passively Transmitted gp41 Antibodies in Babies Born from HIV-1 Subtype C-Seropositive Women: Correlation between Fine Specificity and Protection. J Virol 2012, 86:4129-4138. 10.1128/JVI.06359-11, 3318605, 22301151.
65. Mabuka J, Nduati R, Odem-Davis K, Peterson D, Overbaugh J. HIV-specific antibodies capable of ADCC are common in breastmilk and are associated with reduced risk of transmission in women with high viral loads. PLoS Pathog 2012, 8:e1002739. 10.1371/journal.ppat.1002739, 3375288, 22719248.
66. Barin F, Jourdain G, Brunet S, Ngo-Giang-Huong N, Weerawatgoompa S, Karnchanamayul W, Ariyadej S, Hansudewechakul R, Achalapong J, Yuthavisuthi P, et al. Revisiting the role of neutralizing antibodies in mother-to-child transmission of HIV-1. J Infect Dis 2006, 193:1504-1511. 10.1086/503778, 16652277.
67. Scarlatti G, Albert J, Rossi P, Hodara V, Biraghi P, Muggiasca L, Fenyo EM. Mother-to-child transmission of human immunodeficiency virus type 1: correlation with neutralizing antibodies against primary isolates. J Infect Dis 1993, 168:207-210. 10.1093/infdis/168.1.207, 8515110.
68. Samleerat T, Thenin S, Jourdain G, Ngo-Giang-Huong N, Moreau A, Leechanachai P, Ithisuknanth J, Pagdi K, Wannarit P, Sangsawang S, et al. Maternal neutralizing antibodies against a CRF01_AE primary isolate are associated with a low rate of intrapartum HIV-1 transmission. Virology 2009, 387:388-394. 10.1016/j.virol.2009.02.024, 19303619.
69. Thenin S, Samleerat T, Tavernier E, Ngo-Giang-Huong N, Jourdain G, Lallemant M, Barin F, Braibant M. Envelope glycoproteins of human immunodeficiency virus type 1 variants issued from mother-infant pairs display a wide spectrum of biological properties. Virology 2012, 426:12-21. 10.1016/j.virol.2012.01.017, 22310702.
70. Kittinunvorakoon C, Morris MK, Neeyapun K, Jetsawang B, Buehring GC, Hanson CV. Mother to child transmission of HIV-1 in a Thai population: role of virus characteristics and maternal humoral immune response. J Med Virol 2009, 81:768-778. 10.1002/jmv.21465, 19319941.
71. McFarland EJ, Johnson DC, Muresan P, Fenton T, Tomaras GD, McNamara J, Read JS, Douglas SD, Deville J, Gurwith M, et al. HIV-1 vaccine induced immune responses in newborns of HIV-1 infected mothers. AIDS 2006, 20:1481-1489. 10.1097/01.aids.0000237363.33994.45, 16847402.
72. Ng CT, Jaworski JP, Jayaraman P, Sutton WF, Delio P, Kuller L, Anderson D, Landucci G, Richardson BA, Burton DR, et al. Passive neutralizing antibody controls SHIV viremia and enhances B cell responses in infant macaques. Nat Med 2010, 16:1117-1119. 10.1038/nm.2233, 2952052, 20890292.
73. Kwiek JJ, Mwapasa V, Milner DA, Alker AP, Miller WC, Tadesse E, Molyneux ME, Rogerson SJ, Meshnick SR. Maternal-fetal microtransfusions and HIV-1 mother-to-child transmission in Malawi. PLoS Med 2006, 3:e10. 10.1371/journal.pmed.0030010, 1285069, 16287342.
74. Mwapasa V, Rogerson SJ, Kwiek JJ, Wilson PE, Milner D, Molyneux ME, Kamwendo DD, Tadesse E, Chaluluka E, Meshnick SR. Maternal syphilis infection is associated with increased risk of mother-to-child transmission of HIV in Malawi. AIDS 2006, 20:1869-1877. 10.1097/01.aids.0000244206.41500.27, 16954728.
75. Mwapasa V, Rogerson SJ, Molyneux ME, Abrams ET, Kamwendo DD, Lema VM, Tadesse E, Chaluluka E, Wilson PE, Meshnick SR. The effect of Plasmodium falciparum malaria on peripheral and placental HIV-1 RNA concentrations in pregnant Malawian women. AIDS 2004, 18:1051-1059. 10.1097/00002030-200404300-00014, 15096809.
76. Kwiek JJ, Arney LA, Harawa V, Pedersen B, Mwapasa V, Rogerson SJ, Meshnick SR. Maternal-fetal DNA admixture is associated with intrapartum mother-to-child transmission of HIV-1 in Blantyre. Malawi. J Infect Dis 2008, 197:1378-1381.
77. Rose PP, Korber BT. Detecting hypermutations in viral sequences with an emphasis on G A hypermutation. Bioinformatics 2000, 16:400-401. 10.1093/bioinformatics/16.4.400, 10869039.
78. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. 10.1093/bioinformatics/btm404, 17846036.
79. Guindon S, Delsuc F, Dufayard JF, Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 2009, 537:113-137. 10.1007/978-1-59745-251-9_6, 19378142.
80. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006, 55:539-552. 10.1080/10635150600755453, 16785212.
81. Johnson RE. Infectivity assay (virus yield assay) 1990, New York, NY: Stockton Press, Techniques in HIV research (A. Aldovani aBDW.
82. Mantis NJ, Palaia J, Hessell AJ, Mehta S, Zhu Z, Corthesy B, Neutra MR, Burton DR, Janoff EN. Inhibition of HIV-1 infectivity and epithelial cell transfer by human monoclonal IgG and IgA antibodies carrying the b12 V region. J Immunol 2007, 179:3144-3152. 2881690, 17709529.
83. Dennison SM, Stewart SM, Stempel KC, Liao HX, Haynes BF, Alam SM. Stable docking of neutralizing human immunodeficiency virus type 1 gp41 membrane-proximal external region monoclonal antibodies 2 F5 and 4E10 is dependent on the membrane immersion depth of their epitope regions. J Virol 2009, 83:10211-10223. 10.1128/JVI.00571-09, 2748034, 19640992.
84. Alam SM, McAdams M, Boren D, Rak M, Scearce RM, Gao F, Camacho ZT, Gewirth D, Kelsoe G, Chen P, Haynes BF. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2 F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J Immunol 2007, 178:4424-4435. 2262928, 17372000.
85. Edmonds TG, Ding H, Yuan X, Wei Q, Smith KS, Conway JA, Wieczorek L, Brown B, Polonis V, West JT, et al. Replication competent molecular clones of HIV-1 expressing Renilla luciferase facilitate the analysis of antibody inhibition in PBMC. Virology 2010, 408:1-13. 10.1016/j.virol.2010.08.028, 2993081, 20863545.
86. Binley JM, Ngo-Abdalla S, Moore P, Bobardt M, Chatterji U, Gallay P, Burton DR, Wilson IA, Elder JH, de Parseval A. Inhibition of HIV Env binding to cellular receptors by monoclonal antibody 2 G12 as probed by Fc-tagged gp120. Retrovirology 2006, 3:39. 10.1186/1742-4690-3-39, 1543650, 16817962.
87. Wu L, Martin TD, Vazeux R, Unutmaz D, KewalRamani VN. Functional evaluation of DC-SIGN monoclonal antibodies reveals DC-SIGN interactions with ICAM-3 do not promote human immunodeficiency virus type 1 transmission. J Virol 2002, 76:5905-5914. 10.1128/JVI.76.12.5905-5914.2002, 136240, 12021323.
88. Emmelkamp JM, Rockstroh JK. CCR5 antagonists: comparison of efficacy, side effects, pharmacokinetics and interactions-review of the literature. Eur J Med Res 2007, 12:409-417.
89. Lawless MK, Barney S, Guthrie KI, Bucy TB, Petteway SR, Merutka G. HIV-1 membrane fusion mechanism: structural studies of the interactions between biologically-active peptides from gp41. Biochemistry 1996, 35:13697-13708. 10.1021/bi9606962, 8885850.
90. Montefiori DC. Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol Biol 2009, 485:395-405. 10.1007/978-1-59745-170-3_26, 19020839.
91. Storey JD, Taylor JE, Siegmund D. Strong Control, Conservative Point Estimation, and Simultaneous Conservative Consistency of False Discovery Rates: A Unified Approach. JRSS-B 2004, 66:187-205.