HIV-1 Autologous Antibody Neutralization Associates with Mother to Child Transmission

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Baan, Elly ^a   de Ronde, Anthony ^a   Stax, Martijn ^a   Sanders, Rogier W ^a,b   Luchters, Stanley ^c,e,f   Vyankandondera, Joseph ^c,d   Lange, Joep M ^c   Pollakis, Georgios ^a   Paxton, William A ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c International Antiviral Therapy Evaluation Centre (IATEC)   (Netherlands)

^d Centre Hospitalier Universitaire de Kigali   (Rwanda)

^e BURNET INSTITUTE   (Australia)

^f MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD209 ANTIGEN; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; GLYCOPROTEIN GP 160; NEUTRALIZING ANTIBODY; NEUTRALIZING ANTIBODY 2F5; NEUTRALIZING ANTIBODY 2G12; NEUTRALIZING ANTIBODY 4E10; NEUTRALIZING ANTIBODY B12; UNCLASSIFIED DRUG; VIRUS RNA;

ANTIBODY RESPONSE; ARTICLE; BLOOD ANALYSIS; BREAST FEEDING; CD4 LYMPHOCYTE COUNT; CHILD; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DELIVERY; FEMALE; GESTATION PERIOD; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION RISK; MOLECULAR INTERACTION; MOTHER CHILD RELATION; NONHUMAN; PERINATAL PERIOD; PROTECTION; PROTEIN ANALYSIS; PSEUDOTYPING; VERTICAL TRANSMISSION; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS TRANSMISSION;

FEMALE; HIV ANTIBODIES; HIV-1; HUMANS; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; NEUTRALIZATION TESTS; PHYLOGENY; PREGNANCY;

EID: 84880447402     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069274     Document Type: Article

References (71)

1. European collaborative Study, (1992) Risk factors for mother-to-child transmission of HIV-1. Lancet 339: 1007-1012.
2. Kourtis AP, Lee FK, Abrams EJ, Jamieson DJ, Bulterys M, (2006) Mother-to-child transmission of HIV-1: timing and implications for prevention. Lancet Infect Dis 6: 726-732.
3. Bobkov AF, Kazennova EV, Selimova LM, Khanina TA, Ryabov GS, et al. (2004) Temporal trends in the HIV-1 epidemic in Russia: predominance of subtype A. J Med Virol. 74: 191-196.
4. Huang W, Eshleman SH, Toma J, Stawiski E, Whitcomb JM, et al. (2009) Vertical transmission of X4-tropic and dual-tropic HIV-1 in five Ugandan mother-infant pairs. AIDS 23: 1903-1908.
5. Raymond S, Delobel P, Mavigner M, Cazabat M, Encinas S, et al. (2010) CXCR4-using viruses in plasma and peripheral blood mononuclear cells during primary HIV-1 infection and impact on disease progression. AIDS 24: 2305-2312.
6. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82: 3952-3970.
7. Wolinsky SM, Wike CM, Korber BT, Hutto C, Parks WP, et al. (1992) Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 255: 1134-1137.
8. Chen W, Ying T, Dimitrov DS, (2013) Antibody-based candidate therapeutics against HIV-1: implications for virus eradication and vaccine design. Expert Opin Biol Ther 13: 657-671.
9. Sapsutthipas S, Tsuchiya N, Pathipavanich P, Ariyoshi K, Sawanpanyalert P, et al. (2013) CRF01_AE-Specific Neutralizing Activity Observed in Plasma Derived from HIV-1-Infected Thai Patients Residing in Northern Thailand: Comparison of Neutralizing Breadth and Potency between Plasma Derived from Rapid and Slow Progressors. PLoS One 8: e53920.
10. Weiss RA, Clapham PR, McClure MO, McKeating JA, McKnight A, et al. (1988) Human immunodeficiency viruses: neutralization and receptors. J Acquir Immune Defic Syndr 1: 536-541.
11. Kliks SC, Wara DW, Landers DV, Levy JA, (1994) Features of HIV-1 that could influence maternal-child transmission. JAMA 272: 467-474.
12. Kittinunvorakoon C, Morris MK, Neeyapun K, Jetsawang B, Buehring GC, et al. (2009) Mother to child transmission of HIV-1 in a Thai population: role of virus characteristics and maternal humoral immune response. J Med Virol 81: 768-778.
13. Thenin S, Samleerat T, Tavernier E, Ngo-Giang-Huong N, Jourdain G, et al. (2012) Envelope glycoproteins of human immunodeficiency virus type 1 variants issued from mother-infant pairs display a wide spectrum of biological properties. Virology 426: 12-21.
14. Kishko M, Somasundaran M, Brewster F, Sullivan JL, Clapham PR, et al. (2011) Genotypic and functional properties of early infant HIV-1 envelopes. Retrovirology 8: 67.
15. Kong X, West JT, Zhang H, Shea DM, M'soka TJ, et al. (2008) The human immunodeficiency virus type 1 envelope confers higher rates of replicative fitness to perinatally transmitted viruses than to nontransmitted viruses. J Virol 82: 11609-11618.
16. Alexander M, Lynch R, Mulenga J, Allen S, Derdeyn CA, 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: 4100-4104.
17. Keele BF, Derdeyn CA, (2009) Genetic and antigenic features of the transmitted virus. Current Opinion in HIV and AIDS 4: 352-327.
18. Wu X, Parast AB, Richardson BA, Nduati R, John-Stewart G, et al. (2006) Neutralization escape variants of human immunodeficiency virus type 1 are transmitted from mother to infant. J Virol 80: 835-844.
19. Samleerat T, Braibant M, Jourdain G, Moreau A, Ngo-Giang-Huong N, et al. (2008) Characteristics of HIV type 1 (HIV-1) glycoprotein 120 env sequences in mother-infant pairs infected with HIV-1 subtype CRF01_AE. J Infect Dis 198: 868-876.
20. Baan E, de Ronde A, Luchters S, Vyankandondera J, Lange JM, et al. (2012) HIV Type 1 Mother-to-Child Transmission Facilitated by Distinctive Glycosylation Sites in the gp120 Envelope Glycoprotein. AIDS Res Hum Retroviruses. 28: 715-724.
21. Emini EA, Schleif WA, Nunberg JH, Conley AJ, Eda Y, et al. (1992) Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature 355: 728-730.
22. Ferrantelli F, Rasmussen RA, Buckley KA, Li PL, Wang T, et al. (2004) Complete protection of neonatal rhesus macaques against oral exposure to pathogenic simian-human immunodeficiency virus by human anti-HIV monoclonal antibodies. J Infect Dis 189: 2167-2173.
23. Girard M, Meignier B, Barre-Sinoussi F, Kieny MP, Matthews T, et al. (1995) Vaccine-induced protection of chimpanzees against infection by a heterologous human immunodeficiency virus type 1. J Virol 69: 6239-6248.
24. Dickover R, Garratty E, Yusim K, Miller C, Korber B, et al. (2006) Role of maternal autologous neutralizing antibody in selective perinatal transmission of human immunodeficiency virus type 1 escape variants. J Virol 80: 6525-6533.
25. Samleerat T, Thenin S, Jourdain G, Ngo-Giang-Huong N, Moreau A, et al. (2009) Maternal neutralizing antibodies against a CRF01_AE primary isolate are associated with a low rate of intrapartum HIV-1 transmission. Virology 387: 388-394.
26. Lynch JB, Nduati R, Blish CA, Richardson BA, Mabuka JM, et al. (2011) 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 85: 5252-5261.
27. Russell ES, Kwiek JJ, Keys J, Barton K, Mwapasa V, et al. (2011) 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 85: 8253-8262.
28. Scarlatti G, Albert J, Rossi P, Hodara V, Biraghi P, et al. (1993) Mother-to-child transmission of human immunodeficiency virus type 1: correlation with neutralizing antibodies against primary isolates. J Infect Dis 168: 207-210.
29. Chaillon A, Wack T, Braibant M, Mandelbrot L, Blanche S, et al. (2012) The Breadth and Titer of Maternal HIV-1-Specific Heterologous Neutralizing Antibodies Are Not Associated with a Lower Rate of Mother-to-Child Transmission of HIV-1. J Virol 86: 10540-10546.
30. Husson RN, Lan Y, Kojima E, Venzon D, Mitsuya H, et al. (1995) Vertical transmission of human immunodeficiency virus type 1: autologous neutralizing antibody, virus load, and virus phenotype. J Pediatr 126: 865-871.
31. Zhang H, Rola M, West JT, Tully DC, Kubis P, et al. (2010) Functional properties of the HIV-1 subtype C envelope glycoprotein associated with mother-to-child transmission. Virology 400: 164-174.
32. Guay LA, Musoke P, Hom DL, Nakabiito C, Bagenda D, et al. (2002) Phase I/II trial of HIV-1 hyperimmune globulin for the prevention of HIV-1 vertical transmission in Uganda. Aids 16: 1391-1400.
33. Onyango-Makumbi C, Omer SB, Mubiru M, Moulton LH, Nakabiito C, et al. (2011) Safety and efficacy of HIV hyperimmune globulin for prevention of mother-to-child HIV transmission in HIV-1-infected pregnant women and their infants in Kampala, Uganda (HIVIGLOB/NVP STUDY). J Acquir Immune Defic Syndr 58: 399-407.
34. Simister NE, (2003) Placental transport of immunoglobulin G. Vaccine. 21: 3365-3369.
35. Lagaye S, Derrien M, Menu E, Coito C, Tresoldi E, et al. (2001) Cell-to-cell contact results in a selective translocation of maternal human immunodeficiency virus type 1 quasispecies across a trophoblastic barrier by both transcytosis and infection. J Virol 75: 4780-4791.
36. Barin F, Jourdain G, Brunet S, Ngo-Giang-Huong N, Weerawatgoompa S, et al. (2006) Revisiting the role of neutralizing antibodies in mother-to-child transmission of HIV-1. J Infect Dis 193: 1504-1511.
37. Lallemant M, Baillou A, Lallemant-Le CS, Nzingoula S, Mampaka M, et al. (1994) Maternal antibody response at delivery and perinatal transmission of human immunodeficiency virus type 1 in African women. Lancet 343: 1001-1005.
38. Pancino G, Leste-Lasserre T, Burgard M, Costagliola D, Ivanoff S, et al. (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.
39. Vidricaire G, Imbeault M, Tremblay MJ, (2004) Endocytic host cell machinery plays a dominant role in intracellular trafficking of incoming human immunodeficiency virus type 1 in human placental trophoblasts. J Virol 78: 11904-11915.
40. Tugizov SM, Herrera R, Veluppillai P, Greenspan D, Soros V, et al. (2012) Differential transmission of HIV traversing fetal oral/intestinal epithelia and adult oral epithelia. J Virol 86: 2556-2570.
41. Geijtenbeek TBH, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GCF, et al. (2000) DC-SIGN, a Dendritic Cell-Specific HIV-1-Binding Protein that Enhances trans-Infection of T Cells. Cell 100: 587-597.
42. Haase AT, (2005) Perils at mucosal front lines for HIV and SIV and their hosts. Nat Rev Immunol 5: 783-792.
43. Hladik F, McElrath MJ, (2008) Setting the stage: host invasion by HIV. Nat Rev Immunol 8: 447-457.
44. Boily-Larouche G, Milev MP, Zijenah LS, Labbe AC, Zannou DM, et al. (2012) Naturally-occurring genetic variants in human DC-SIGN increase HIV-1 capture, cell-transfer and risk of mother-to-child transmission. PLoS One 7: e40706.
45. van Montfort T, Nabatov AA, Geijtenbeek TB, Pollakis G, Paxton WA, (2007) Efficient capture of antibody neutralized HIV-1 by cells expressing DC-SIGN and transfer to CD4+ T lymphocytes. J Immunol 178: 3177-3185.
46. Stax MJ, van Montfort T, Sprenger RR, Melchers M, Sanders RW, et al. (2009) Mucin 6 in seminal plasma binds DC-SIGN and potently blocks dendritic cell mediated transfer of HIV-1 to CD4(+) T-lymphocytes. Virology 391: 203-211.
47. Saeland E, de Jong MA, Nabatov AA, Kalay H, Geijtenbeek TB, et al. (2009) MUC1 in human milk blocks transmission of human immunodeficiency virus from dendritic cells to T cells. Mol Immunol 46: 2309-2316.
48. Sabatte J, Faigle W, Ceballos A, Morelle W, Rodriguez RC, et al. (2011) Semen clusterin is a novel DC-SIGN ligand. J Immunol 187: 5299-5309.
49. Naarding MA, Dirac AM, Ludwig IS, Speijer D, Lindquist S, et al. (2006) Bile salt-stimulated lipase from human milk binds DC-SIGN and inhibits human immunodeficiency virus type 1 transfer to CD4+ T cells. Antimicrob Agents Chemother 50: 3367-3374.
50. Mann AM, Rusert P, Berlinger L, Kuster H, Gunthard HF, et al. (2009) HIV sensitivity to neutralization is determined by target and virus producer cell properties. Aids 23: 1659-1667.
51. Provine NM, Puryear WB, Wu X, Overbaugh J, Haigwood NL, (2009) The infectious molecular clone and pseudotyped virus models of human immunodeficiency virus type 1 exhibit significant differences in virion composition with only moderate differences in infectivity and inhibition sensitivity. J Virol 83: 9002-9007.
52. Derdeyn CA, Hunter E, (2008) Viral characteristics of transmitted HIV. Curr Opin HIV AIDS 3: 16-21.
53. van't Wout AB, Kootstra NA, Mulder-Kampinga GA, Albrecht-van LN, Scherpbier HJ, et al. (1994) Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J Clin Invest 94: 2060-2067.
54. Chalmet K, Dauwe K, Foquet L, Baatz F, Seguin-Devaux C, et al. (2012) Presence of CXCR4-using HIV-1 in patients with recently diagnosed infection: correlates and evidence for transmission. J Infect Dis 205: 174-184.
55. Hedskog C, Mild M, Albert J, (2012) Transmission of the X4 phenotype of HIV-1: is there evidence against the "random transmission" hypothesis? J Infect Dis 205: 163-165.
56. Rieder P, Joos B, Scherrer AU, Kuster H, Braun D, et al. (2011) Characterization of human immunodeficiency virus type 1 (HIV-1) diversity and tropism in 145 patients with primary HIV-1 infection. Clin Infect Dis 53: 1271-1279.
57. Pollakis G, Kang S, Kliphuis A, Chalaby MI, Goudsmit J, et al. (2001) N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J Biol Chem 276: 13433-13441.
58. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (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.
59. Chohan B, Lang D, Sagar M, Korber B, Lavreys L, 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: 6528-6531.
60. Frost SD, Liu Y, Pond SL, Chappey C, Wrin T, et al. (2005) Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. J Virol. 79: 6523-6527.
61. Frost SD, Wrin T, Smith DM, Kosakovsky Pond SL, et al. (2005) Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci U S A 102: 18514-18519.
62. Moore PL, Gray ES, Wibmer CK, Bhiman JN, Nonyane M, et al. (2012) Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat Med 18: 1688-1692.
63. Pereira L, Maidji E, McDonagh S, Tabata T, (2005) Insights into viral transmission at the uterine-placental interface. Trends Microbiol 13: 164-174.
64. Homsy J, Meyer M, Tateno M, Clarkson S, Levy JA, (1989) The Fc and not CD4 receptor mediates antibody enhancement of HIV infection in human cells. Science 244: 1357-1360.
65. Robinson WE Jr, Montefiori DC, Mitchell WM, (1988) Antibody-dependent enhancement of human immunodeficiency virus type 1 infection. Lancet 1: 790-794.
66. Wigzell H, (1988) Immunopathogenesis of HIV infection. J Acquir Immune Defic Syndr 1: 559-565.
67. Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM, et al. (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28: 495-503.
68. Ruijter JM, Thygesen HH, Schoneveld OJ, Das AT, Berkhout B, et al. (2006) Factor correction as a tool to eliminate between-session variation in replicate experiments: application to molecular biology and retrovirology. Retrovirology 3: 2.
69. Willey R, Nason MC, Nishimura Y, Follmann DA, Martin MA, (2010) Neutralizing antibody titers conferring protection to macaques from a simian/human immunodeficiency virus challenge using the TZM-bl assay. AIDS Res Hum Retroviruses 26: 89-98.
70. Binley JM, Sanders RW, Clas B, Schuelke N, Master A, et al. (2000) A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J Virol 74: 627-643.
71. Eggink D, Melchers M, Wuhrer M, van Montfort T, Dey AK, et al. (2010) Lack of complex N-glycans on HIV-1 envelope glycoproteins preserves protein conformation and entry function. Virology 401: 236-247.