Maternal broadly neutralizing antibodies can select for neutralization-resistant, infant-transmitted/founder HIV variants

mBio

Volumn 11, Issue 2, 2020, Pages

  Martinez, David R ^a,b   Tu, Joshua J ^b   Kumar, Amit ^b   Mangold, Jesse F ^b   Mangan, Riley J ^b   Goswami, Ria ^b   Giorgi, Elena E ^c   Chen, Juilin ^a,b   Mengual, Michael ^a   Douglas, Ayooluwa O ^b   Heimsath, Holly ^b   Saunders, Kevin O ^a,b   Nicely, Nathan I ^b   Eudailey, Joshua ^b   Hernandez, Giovanna ^b   Morgan Asiedu, Papa Kwadwo ^b   Wiehe, Kevin ^b   Haynes, Barton F ^a,b   Moody, M Anthony ^a,b   LaBranche, Celia ^a   Montefiori, David C ^a,b   Gao, Feng ^a   Permar, Sallie R ^a,b   more..

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

Antibody; BNAbs; HIV; Infant T F virus; Mother to child transmission; MTCT; Neutralization; Vertical transmission; Virus

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; EPITOPE; GLYCOPROTEIN GP 120; HIV ENVELOPE PROTEIN GP120 (305-321); HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; PEPTIDE FRAGMENT;

AMERICAN; ANTIBODY RESPONSE; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; FOUNDER EFFECT; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFANT; MALAWIAN; PRIORITY JOURNAL; VERTICAL TRANSMISSION; VIRUS NEUTRALIZATION; VIRUS TRANSMISSION; GENETIC VARIATION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; MALAWI; PREGNANCY; PREGNANCY COMPLICATION; SERODIAGNOSIS; VIROLOGY;

BROADLY NEUTRALIZING ANTIBODIES; COHORT STUDIES; EPITOPES; FEMALE; GENETIC VARIATION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; INFANT; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MALAWI; NEUTRALIZATION TESTS; PEPTIDE FRAGMENTS; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS;

EID: 85081652689     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00176-20     Document Type: Article

References (67)

1. UNAIDS. 2018 Global HIV & AIDS statistics-2018 fact sheet. UNAIDS, Geneva, Switzerland.
2. Fowler MG, Fiscus SA, Currier JS, Makanani B, Martinson F, Chipato T, Browning R, Shapiro D, Mofenson L. 2015. PROMISE: efficacy and safety of 2 strategies to prevent perinatal HIV transmission. Oral presentation. Conference on Retroviruses and Opportunistic Infections, Seattle, WA.
3. UNAIDS. 2015 Progress report on the global plan: towards the elimination of new HIV infections among children and keeping their mothers alive. UNAIDS, Geneva, Switzerland.
4. Saji F, Koyama M, Matsuzaki N. 1994. Current topic: human placental Fc receptors. Placenta 15: 453-466. https://doi.org/10.1016/s0143-4004(05)80 415-1.
5. Lallemant M, Le Coeur S, Samba L, Cheynier D, M’Pelé P, Nzingoula S, Essex M. 1994. Mother-to-child transmission of HIV-1 in Congo, central Africa. Congolese Research Group on Mother-to-Child Transmission of HIV. AIDS 8: 1451-1456. https://doi.org/10.1097/00002030-199410000-00012.
6. European Collaborative Study. 1991. Children born to women with HIV-1 infection: natural history and risk of transmission. Lancet 337: 253-260. https://doi.org/10.1016/0140-6736(91)90866-N.
7. Amirthalingam G, Andrews N, Campbell H, Ribeiro S, Kara E, Donegan K, Fry NK, Miller E, Ramsay M. 2014. Effectiveness of maternal pertussis vaccination in England: an observational study. Lancet 384: 1521-1528. https://doi.org/10.1016/S0140-6736(14)60686-3.
8. Khan R, Vandelaer J, Yakubu A, Raza AA, Zulu F. 2015. Maternal and neonatal tetanus elimination: from protecting women and newborns to protecting all. Int J Womens Health 7: 171-180. https://doi.org/10.2147/IJWH.S50539.
9. Benowitz I, Esposito DB, Gracey KD, Shapiro ED, Vazquez M. 2010. Influenza vaccine given to pregnant women reduces hospitalization due to influenza in their infants. Clin Infect Dis 51: 1355-1361. https://doi.org/10.1086/657309.
10. Nunes MC, Maternal Flu Trial Team, Cutland CL, Jones S, Hugo A, Madimabe R, Simoes EA, Weinberg A, Madhi SA. 2016. Duration of infant protection against influenza illness conferred by maternal immunization: secondary analysis of a randomized clinical trial. JAMA Pediatr 170: 840-847. https://doi.org/10.1001/jamapediatrics.2016.0921.
11. Zaman K, Roy E, Arifeen SE, Rahman M, Raqib R, Wilson E, Omer SB, Shahid NS, Breiman RF, Breiman RE, Steinhoff MC. 2008. Effectiveness of maternal influenza immunization in mothers and infants. N Engl J Med 359: 1555-1564. https://doi.org/10.1056/NEJMoa0708630.
12. Seppälä EM, López-Perea N, Torres de Mier M. d V, Echevarría JE, Fernández-García A, Masa-Calles J. 2019. Last cases of rubella and congenital rubella syndrome in Spain, 1997-2016: the success of a vaccination program. Vaccine 37: 169-175. https://doi.org/10.1016/j.vaccine.2018.11.017.
13. Pou C, Nkulikiyimfura D, Henckel E, Olin A, Lakshmikanth T, Mikes J, Wang J, Chen Y, Bernhardsson AK, Gustafsson A, Bohlin K, Brodin P. 2019. The repertoire of maternal anti-viral antibodies in human newborns. Nat Med 25: 591-596. https://doi.org/10.1038/s41591-019-0392-8.
14. Martinez DR, Fong Y, Li SH, Yang F, Jennewein MF, Weiner JA, Harrell EA, Mangold JF, Goswami R, Seage GR, III, Alter G, Ackerman ME, Peng X, Fouda GG, Permar SR. 2019. Fc characteristics mediate selective placental transfer of IgG in HIV-infected women. Cell 178: 190-201.e11. https://doi.org/10.1016/j.cell.2019.05.046.
15. Ahmad N, Baroudy BM, Baker RC, Chappey C. 1995. Genetic analysis of human immunodeficiency virus type 1 envelope V3 region isolates from mothers and infants after perinatal transmission. J Virol 69: 1001-1012. https://doi.org/10.1128/JVI.69.2.1001-1012.1995.
16. Martinez DR, Vandergrift N, Douglas AO, McGuire E, Bainbridge J, Nicely NI, Montefiori DC, Tomaras GD, Fouda GG, Permar SR. 2017. Maternal binding and neutralizing IgG responses targeting the C-terminal region of the V3 loop are predictive of reduced peripartum HIV-1 transmission risk. J Virol 91: e2422-16. https://doi.org/10.1128/JVI.02422-16.
17. Permar SR, Fong Y, Vandergrift N, Fouda GG, Gilbert P, Parks R, Jaeger FH, Pollara J, Martelli A, Liebl BE, Lloyd K, Yates NL, Overman RG, Shen X, Whitaker K, Chen H, Pritchett J, Solomon E, Friberg E, Marshall DJ, Whitesides JF, Gurley TC, Von Holle T, Martinez DR, Cai F, Kumar A, Xia SM, Lu X, Louzao R, Wilkes S, Datta S, Sarzotti-Kelsoe M, Liao HX, Ferrari G, Alam SM, Montefiori DC, Denny TN, Moody MA, Tomaras GD, Gao F, Haynes BF. 2015. Maternal HIV-1 envelope-specific antibody responses and reduced risk of perinatal transmission. J Clin Invest 125: 2702-2706. https://doi.org/10.1172/JCI81593.
18. Wu X, Parast AB, Richardson BA, Nduati R, John-Stewart G, Mbori-Ngacha D, Rainwater SM, Overbaugh J. 2006. Neutralization escape variants of human immunodeficiency virus type 1 are transmitted from mother to infant. J Virol 80: 835-844. https://doi.org/10.1128/JVI.80.2.835-844.2006.
19. Ghulam-Smith M, Olson A, White LF, Chasela CS, Ellington SR, Kourtis AP, Jamieson DJ, Tegha G, van der Horst CM, Sagar M. 2017. Maternal but not infant anti-HIV-1 neutralizing antibody response associates with enhanced transmission and infant morbidity. mBio 8: e01373-17. https://doi.org/10.1128/mBio.01373-17.
20. Markham RB, Coberly J, Ruff AJ, Hoover D, Gomez J, Holt E, Desormeaux J, Boulos R, Quinn TC, Halsey NA. 1994. Maternal IgG1 and IgA antibody to V3 loop consensus sequence and maternal-infant HIV-1 transmission. Lancet 343: 390-391. https://doi.org/10.1016/s0140-6736(94)91225-4.
21. Pancino G, Leste-Lasserre T, Burgard M, Costagliola D, Ivanoff S, Blanche S, Rouzioux C, Sonigo P. 1998. Apparent enhancement of perinatal transmission of human immunodeficiency virus type 1 by high maternal anti-gp160 antibody titer. J Infect Dis 177: 1737-1741. https://doi.org/10.1086/517435.
22. Moody MA, Gao F, Gurley TC, Amos JD, Kumar A, Hora B, Marshall DJ, Whitesides JF, Xia SM, Parks R, Lloyd KE, Hwang KK, Lu X, Bonsignori M, Finzi A, Vandergrift NA, Alam SM, Ferrari G, Shen X, Tomaras GD, Kamanga G, Cohen MS, Sam NE, Kapiga S, Gray ES, Tumba NL, Morris L, Zolla-Pazner S, Gorny MK, Mascola JR, Hahn BH, Shaw GM, Sodroski JG, Liao HX, Montefiori DC, Hraber PT, Korber BT, Haynes BF. 2015. Strainspecific V3 and CD4 binding site autologous HIV-1 neutralizing antibodies select neutralization-resistant viruses. Cell Host Microbe 18: 354-362. https://doi.org/10.1016/j.chom.2015.08.006.
23. Rong R, Li B, Lynch RM, Haaland RE, Murphy MK, Mulenga J, Allen SA, Pinter A, Shaw GM, Hunter E, Robinson JE, Gnanakaran S, Derdeyn CA. 2009. Escape from autologous neutralizing antibodies in acute/early subtype C HIV-1 infection requires multiple pathways. PLoS Pathog 5: e1000594. https://doi.org/10.1371/journal.ppat.1000594.
24. Lynch RM, Rong R, Li B, Shen T, Honnen W, Mulenga J, Allen S, Pinter A, Gnanakaran S, Derdeyn CA. 2010. Subtype-specific conservation of isoleucine 309 in the envelope V3 domain is linked to immune evasion in subtype C HIV-1 infection. Virology 404: 59-70. https://doi.org/10.1016/j.virol.2010.04.010.
25. Kumar A, Smith CEP, Giorgi EE, Eudailey J, Martinez DR, Yusim K, Douglas AO, Stamper L, McGuire E, LaBranche CC, Montefiori DC, Fouda GG, Gao F, Permar SR. 2018. Infant transmitted/founder HIV-1 viruses from peripartum transmission are neutralization resistant to paired maternal plasma. PLoS Pathog 14: e1006944. https://doi.org/10.1371/journal.ppat. 1006944.
26. Hraber P, Seaman MS, Bailer RT, Mascola JR, Montefiori DC, Korber BT. 2014. Prevalence of broadly neutralizing antibody responses during chronic HIV-1 infection. AIDS 28: 163-169. https://doi.org/10.1097/QAD. 0000000000000106.
27. Walker LM, Simek MD, Priddy F, Gach JS, Wagner D, Zwick MB, Phogat SK, Poignard P, Burton DR. 2010. A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog 6: e1001028. https://doi.org/10.1371/journal.ppat.1001028.
28. Scheid JF, Mouquet H, Feldhahn N, Seaman MS, Velinzon K, Pietzsch J, Ott RG, Anthony RM, Zebroski H, Hurley A, Phogat A, Chakrabarti B, Li Y, Connors M, Pereyra F, Walker BD, Wardemann H, Ho D, Wyatt RT, Mascola JR, Ravetch JV, Nussenzweig MC. 2009. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458: 636-640. https://doi.org/10.1038/nature07930.
29. Liao H-X, NISC Comparative Sequencing Program, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, Fire AZ, Roskin KM, Schramm CA, Zhang Z, Zhu J, Shapiro L, Mullikin JC, Gnanakaran S, Hraber P, Wiehe K, Kelsoe G, Yang G, Xia S-M, Montefiori DC, Parks R, Lloyd KE, Scearce RM, Soderberg KA, Cohen M, Kamanga G, Louder MK, Tran LM, Chen Y, Cai F, Chen S, Moquin S, Du X, Joyce MG, Srivatsan S, Zhang B, Zheng A, Shaw GM, Hahn BH, Kepler TB, Korber BTM, Kwong PD, Mascola JR, Haynes BF. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469-476. https://doi.org/10.1038/nature12053.
30. Gao F, Bonsignori M, Liao HX, Kumar A, Xia SM, Lu X, Cai F, Hwang KK, Song H, Zhou T, Lynch RM, Alam SM, Moody MA, Ferrari G, Berrong M, Kelsoe G, Shaw GM, Hahn BH, Montefiori DC, Kamanga G, Cohen MS, Hraber P, Kwong PD, Korber BT, Mascola JR, Kepler TB, Haynes BF. 2014. Cooperation of B cell lineages in induction of HIV-1-broadly neutralizing antibodies. Cell 158: 481-491. https://doi.org/10.1016/j.cell.2014.06.022.
31. Derdeyn CA, Moore PL, Morris L. 2014. Development of broadly neutralizing antibodies from autologous neutralizing antibody responses in HIV infection. Curr Opin HIV AIDS 9: 210-216. https://doi.org/10.1097/COH. 0000000000000057.
32. Moore PL, Gray ES, Wibmer CK, Bhiman JN, Nonyane M, Sheward DJ, Hermanus T, Bajimaya S, Tumba NL, Abrahams MR, Lambson BE, Ranchobe N, Ping L, Ngandu N, Abdool Karim Q, Abdool Karim SS, Swan-strom RI, Seaman MS, Williamson C, Morris L. 2012. Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat Med 18: 1688-1692. https://doi.org/10.1038/nm.2985.
33. Bar-On Y, Gruell H, Schoofs T, Pai JA, Nogueira L, Butler AL, Millard K, Lehmann C, Suárez I, Oliveira TY, Karagounis T, Cohen YZ, Wyen C, Scholten S, Handl L, Belblidia S, Dizon JP, Vehreschild JJ, Witmer-Pack M, Shimeliovich I, Jain K, Fiddike K, Seaton KE, Yates NL, Horowitz J, Gulick RM, Pfeifer N, Tomaras GD, Seaman MS, Fätkenheuer G, Caskey M, Klein F, Nussenzweig MC. 2018. Safety and antiviral activity of combination HIV-1 broadly neutralizing antibodies in viremic individuals. Nat Med 24: 1701-1707. https://doi.org/10.1038/s41591-018-0186-4.
34. Caskey M, Schoofs T, Gruell H, Settler A, Karagounis T, Kreider EF, Murrell B, Pfeifer N, Nogueira L, Oliveira TY, Learn GH, Cohen YZ, Lehmann C, Gillor D, Shimeliovich I, Unson-O’Brien C, Weiland D, Robles A, Kümmerle T, Wyen C, Levin R, Witmer-Pack M, Eren K, Ignacio C, Kiss S, West AP, Mouquet H, Zingman BS, Gulick RM, Keler T, Bjorkman PJ, Seaman MS, Hahn BH, Fätkenheuer G, Schlesinger SJ, Nussenzweig MC, Klein F. 2017. Antibody 10-1074 suppresses viremia in HIV-1-infected individuals. Nat Med 23: 185-191. https://doi.org/10.1038/nm.4268.
35. Mendoza P, Gruell H, Nogueira L, Pai JA, Butler AL, Millard K, Lehmann C, Suárez I, Oliveira TY, Lorenzi JCC, Cohen YZ, Wyen C, Kümmerle T, Karagounis T, Lu C-L, Handl L, Unson-O’Brien C, Patel R, Ruping C, Schlotz M, Witmer-Pack M, Shimeliovich I, Kremer G, Thomas E, Seaton KE, Horowitz J, West AP, Bjorkman PJ, Tomaras GD, Gulick RM, Pfeifer N, Fätkenheuer G, Seaman MS, Klein F, Caskey M, Nussenzweig MC. 2018. Combination therapy with anti-HIV-1 antibodies maintains viral suppression. Nature 561: 479-484. https://doi.org/10.1038/s41586-018-0531-2.
36. Scheid JF, Horwitz JA, Bar-On Y, Kreider EF, Lu CL, Lorenzi JC, Feldmann A, Braunschweig M, Nogueira L, Oliveira T, Shimeliovich I, Patel R, Burke L, Cohen YZ, Hadrigan S, Settler A, Witmer-Pack M, West AP, Jr, Juelg B, Keler T, Hawthorne T, Zingman B, Gulick RM, Pfeifer N, Learn GH, Seaman MS, Bjorkman PJ, Klein F, Schlesinger SJ, Walker BD, Hahn BH, Nussenzweig MC, Caskey M. 2016. HIV-1 antibody 3BNC117 suppresses viral rebound in humans during treatment interruption. Nature 535: 556-560. https://doi.org/10.1038/nature18929.
37. Alam SM, Aussedat B, Vohra Y, Meyerhoff RR, Cale EM, Walkowicz WE, Radakovich NA, Anasti K, Armand L, Parks R, Sutherland L, Scearce R, Joyce MG, Pancera M, Druz A, Georgiev IS, Van Holle T, Eaton A, Fox C, Reed SG, Louder M, Bailer RT, Morris L, Abdool-Karim SS, Cohen M, Liao HX, Montefiori DC, Park PK, Fernandez-Tejada A, Wiehe K, Santra S, Kepler TB, Saunders KO, Sodroski J, Kwong PD, Mascola JR, Bonsignori M, Moody MA, Danishefsky S, Haynes BF. 2017. Mimicry of an HIV broadly neutralizing antibody epitope with a synthetic glycopeptide. Sci Transl Med 9: eaai7521. https://doi.org/10.1126/scitranslmed.aai7521.
38. Bonsignori M, Kreider EF, Fera D, Meyerhoff RR, Bradley T, Wiehe K, Alam SM, Aussedat B, Walkowicz WE, Hwang KK, Saunders KO, Zhang R, Gladden MA, Monroe A, Kumar A, Xia SM, Cooper M, Louder MK, McKee K, Bailer RT, Pier BW, Jette CA, Kelsoe G, Williams WB, Morris L, Kappes J, Wagh K, Kamanga G, Cohen MS, Hraber PT, Montefiori DC, Trama A, Liao HX, Kepler TB, Moody MA, Gao F, Danishefsky SJ, Mascola JR, Shaw GM, Hahn BH, Harrison SC, Korber BT, Haynes BF. 2017. Staged induction of HIV-1 glycan-dependent broadly neutralizing antibodies. Sci Transl Med 9: eaai7514. https://doi.org/10.1126/scitranslmed.aai7514.
39. Saunders KO, Nicely NI, Wiehe K, Bonsignori M, Meyerhoff RR, Parks R, Walkowicz WE, Aussedat B, Wu NR, Cai F, Vohra Y, Park PK, Eaton A, Go EP, Sutherland LL, Scearce RM, Barouch DH, Zhang R, Von Holle T, Overman RG, Anasti K, Sanders RW, Moody MA, Kepler TB, Korber B, Desaire H, Santra S, Letvin NL, Nabel GJ, Montefiori DC, Tomaras GD, Liao HX, Alam SM, Danishefsky SJ, Haynes BF. 2017. Vaccine Elicitation of High Mannose-Dependent Neutralizing Antibodies against the V3-Glycan Broadly Neutralizing Epitope in Nonhuman Primates. Cell Rep 18: 2175-2188. https://doi.org/10.1016/j.celrep.2017.02.003.
40. Burton DR, Ahmed R, Barouch DH, Butera ST, Crotty S, Godzik A, Kaufmann DE, McElrath MJ, Nussenzweig MC, Pulendran B, Scanlan CN, Schief WR, Silvestri G, Streeck H, Walker BD, Walker LM, Ward AB, Wilson IA, Wyatt R. 2012. A blueprint for HIV vaccine discovery. Cell Host Microbe 12: 396-407. https://doi.org/10.1016/j.chom.2012.09.008.
41. Escolano A, Steichen JM, Dosenovic P, Kulp DW, Golijanin J, Sok D, Freund NT, Gitlin AD, Oliveira T, Araki T, Lowe S, Chen ST, Heinemann J, Yao KH, Georgeson E, Saye-Francisco KL, Gazumyan A, Adachi Y, Kubitz M, Burton DR, Schief WR, Nussenzweig MC. 2016. Sequential immunization elicits broadly neutralizing anti-HIV-1 antibodies in Ig knockin mice. Cell 166: 1445-1458.e12. https://doi.org/10.1016/j.cell.2016.07.030.
42. Giorgi EE, Funkhouser B, Athreya G, Perelson AS, Korber BT, Bhattacharya T. 2010. Estimating time since infection in early homogeneous HIV-1 samples using a Poisson model. BMC Bioinformatics 11: 532. https://doi. org/10.1186/1471-2105-11-532.
43. Martinez DR, Vandergrift N, Douglas AO, McGuire E, Bainbridge J, Nicely NI, Montefiori DC, Tomaras GD, Fouda GG, Permar SR. 2017. Maternal binding and neutralizing IgG responses targeting the C-terminal region of the V3 loop are predictive of reduced peripartum HIV-1 transmission risk. J Virol 91: e02422-16. https://doi.org/10.1128/JVI.02422-16.
44. Scarlatti G, Albert J, Rossi P, Hodara V, Biraghi P, Muggiasca L, Fenyo EM. 1993. Mother-to-child transmission of human immunodeficiency virus type 1: correlation with neutralizing antibodies against primary isolates. J Infect Dis 168: 207-210. https://doi.org/10.1093/infdis/168.1.207.
45. deCamp A, Hraber P, Bailer RT, Seaman MS, Ochsenbauer C, Kappes J, Gottardo R, Edlefsen P, Self S, Tang H, Greene K, Gao H, Daniell X, Sarzotti-Kelsoe M, Gorny MK, Zolla-Pazner S, LaBranche CC, Mascola JR, Korber BT, Montefiori DC. 2014. Global panel of HIV-1 Env reference strains for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol 88: 2489-2507. https://doi.org/10.1128/JVI.02853-13.
46. West AP, Jr, Scharf L, Horwitz J, Klein F, Nussenzweig MC, Bjorkman PJ. 2013. Computational analysis of anti-HIV-1 antibody neutralization panel data to identify potential functional epitope residues. Proc Natl Acad Sci U S A 110: 10598-10603. https://doi.org/10.1073/pnas.1309215110.
47. Bricault CA, Yusim K, Seaman MS, Yoon H, Theiler J, Giorgi EE, Wagh K, Theiler M, Hraber P, Macke JP, Kreider EF, Learn GH, Hahn BH, Scheid JF, Kovacs JM, Shields JL, Lavine CL, Ghantous F, Rist M, Bayne MG, Neubauer GH, McMahan K, Peng H, Cheneau C, Jones JJ, Zeng J, Ochsenbauer C, Nkolola JP, Stephenson KE, Chen B, Gnanakaran S, Bonsignori M, Williams LD, Haynes BF, Doria-Rose N, Mascola JR, Montefiori DC, Barouch DH, Korber B. 2019. HIV-1 neutralizing antibody signatures and application to epitope-targeted vaccine design. Cell Host Microbe 25: 59-72.e8. https://doi.org/10.1016/j.chom.2018.12.001.
48. Kishko M, Somasundaran M, Brewster F, Sullivan JL, Clapham PR, Luzuriaga K. 2011. Genotypic and functional properties of early infant HIV-1 envelopes. Retrovirology 8: 67. https://doi.org/10.1186/1742-4690-8-67.
49. Fouda G, Mahlokozera T, Salazar-Gonzalez J, Salazar M, Learn G, Kumar S, Dennison S, Russell E, Rizzolo K, Jaeger F, Cai F, Vandergrift N, Gao F, Hahn B, Shaw G, Ochsenbauer C, Swanstrom R, Meshnick S, Mwapasa V, Kalilani L, Fiscus S, Montefiori D, Haynes B, Kwiek J, Alam S, Permar S. 2013. Postnatally-transmitted HIV-1 Envelope variants have similar neutralizationsensitivity and function to that of nontransmitted breast milk variants. Retrovirology 10: 3-4690. https://doi.org/10.1186/1742-4690-10-3.
50. Chohan B, Lang D, Sagar M, Korber B, Lavreys L, Richardson B, Overbaugh J. 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: 6528-6531. https://doi.org/10.1128/JVI.79.10.6528-6531.2005.
51. Bar KJ, Tsao CY, Iyer SS, Decker JM, Yang Y, Bonsignori M, Chen X, Hwang KK, Montefiori DC, Liao HX, Hraber P, Fischer W, Li H, Wang S, Sterrett S, Keele BF, Ganusov VV, Perelson AS, Korber BT, Georgiev I, McLellan JS, Pavlicek JW, Gao F, Haynes BF, Hahn BH, Kwong PD, Shaw GM. 2012. Early low-titer neutralizing antibodies impede HIV-1 replication and select for virus escape. PLoS Pathog 8: e1002721. https://doi.org/10.1371/journal.ppat.1002721.
52. Fera D, Lee MS, Wiehe K, Meyerhoff RR, Piai A, Bonsignori M, Aussedat B, Walkowicz WE, Ton T, Zhou JO, Danishefsky S, Haynes BF, Harrison SC. 2018. HIV envelope V3 region mimic embodies key features of a broadly neutralizing antibody lineage epitope. Nat Commun 9: 1111. https://doi. org/10.1038/s41467-018-03565-6.
53. Wolinsky SM, Wike CM, Korber BT, Hutto C, Parks WP, Rosenblum LL, Kunstman KJ, Furtado MR, Munoz JL. 1992. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 255: 1134-1137. https://doi.org/10.1126/science.1546316.
54. Braibant M, Barin F. 2013. The role of neutralizing antibodies in prevention of HIV-1 infection: what can we learn from the mother-to-child transmission context? Retrovirology 10: 103. https://doi.org/10.1186/1742-4690-10-103.
55. Andrabi R, Williams C, Wang XH, Li L, Choudhary AK, Wig N, Biswas A, Luthra K, Nadas A, Seaman MS, Nyambi P, Zolla-Pazner S, Gorny MK. 2013. Cross-neutralizing activity of human anti-V3 monoclonal antibodies derived from non-B clade HIV-1 infected individuals. Virology 439: 81-88. https://doi.org/10.1016/j.virol.2012.12.010.
56. Han Q, Jones JA, Nicely NI, Reed RK, Shen X, Mansouri K, Louder M, Trama AM, Alam SM, Edwards RJ, Bonsignori M, Tomaras GD, Korber B, Montefiori DC, Mascola JR, Seaman MS, Haynes BF, Saunders KO. 2019. Difficult-to-neutralize global HIV-1 isolates are neutralized by antibodies targeting open envelope conformations. Nat Commun 10: 2898. https://doi.org/10.1038/s41467-019-10899-2.
57. Zolla-Pazner S, Edlefsen PT, Rolland M, Kong X-P, deCamp A, Gottardo R, Williams C, Tovanabutra S, Sharpe-Cohen S, Mullins JI, deSouza MS, Karasavvas N, Nitayaphan S, Rerks-Ngarm S, Pitisuttihum P, Kaewkungwal J, O’Connell RJ, Robb ML, Michael NL, Kim JH, Gilbert P. 2014. Vaccine-induced human antibodies specific for the third variable region of HIV-1 gp120 impose immune pressure on infecting viruses. EBioMedicine 1: 37-45. https://doi.org/10.1016/j.ebiom.2014.10.022.
58. Sacha CR, Vandergrift N, Jeffries TL, Jr, McGuire E, Fouda GG, Liebl B, Marshall DJ, Gurley TC, Stiegel L, Whitesides JF, Friedman J, Badiabo A, Foulger A, Yates NL, Tomaras GD, Kepler TB, Liao HX, Haynes BF, Moody MA, Permar SR. 2015. Restricted isotype, distinct variable gene usage, and high rate of gp120 specificity of HIV-1 envelope-specific B cells in colostrum compared with those in blood of HIV-1-infected, lactating African women. Mucosal Immunol 8: 316-326. https://doi.org/10.1038/mi.2014.69.
59. Rich KC, Fowler MG, Mofenson LM, Abboud R, Pitt J, Diaz C, Hanson IC, Cooper E, Mendez H. 2000. Maternal and infant factors predicting disease progression in human immunodeficiency virus type 1-infected infants. Women and Infants Transmission Study Group. Pediatrics 105: e8. https://doi.org/10.1542/peds.105.1.e8.
60. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224. https://doi.org/10.1093/molbev/msp259.
61. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7557. https://doi.org/10.1073/pnas.0802203105.
62. Louder MK, Sambor A, Chertova E, Hunte T, Barrett S, Ojong F, Sanders-Buell E, Zolla-Pazner S, McCutchan FE, Roser JD, Gabuzda D, Lifson JD, Mascola JR. 2005. HIV-1 envelope pseudotyped viral vectors and infectious molecular clones expressing the same envelope glycoprotein have a similar neutralization phenotype, but culture in peripheral blood mononuclear cells is associated with decreased neutralization sensitivity. Virology 339: 226-238. https://doi.org/10.1016/j.virol.2005.06.003.
63. Volpe JM, Cowell LG, Kepler TB. 2006. SoDA: implementation of a 3D alignment algorithm for inference of antigen receptor recombinations. Bioinformatics 22: 438-444. https://doi.org/10.1093/bioinformatics/btk004.
64. Liao HX, Levesque MC, Nagel A, Dixon A, Zhang R, Walter E, Parks R, Whitesides J, Marshall DJ, Hwang KK, Yang Y, Chen X, Gao F, Munshaw S, Kepler TB, Denny T, Moody MA, Haynes BF. 2009. High-throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J Virol Methods 158: 171-179. https://doi.org/10.1016/j.jviromet.2009.02.014.
65. Seaman MS, Janes H, Hawkins N, Grandpre LE, Devoy C, Giri A, Coffey RT, Harris L, Wood B, Daniels MG, Bhattacharya T, Lapedes A, Polonis VR, McCutchan FE, Gilbert PB, Self SG, Korber BT, Montefiori DC, Mascola JR. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J Virol 84: 1439-1452. https://doi.org/10.1128/JVI.02108-09.
66. Montefiori DC. 2009. Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol Biol 485: 395-405. https://doi.org/10.1007/978-1-59745-170-3_26.
67. R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.