Adaptive HIV-Specific B Cell-Derived Humoral Immune Defenses of the Intestinal Mucosa in Children Exposed to HIV via Breast-Feeding

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Moussa, Sandrine ^a   Jenabian, Mohammad Ali ^b,f   Gody, Jean Chrysostome ^c,d   Léal, Josiane ^a   Grésenguet, Gérard ^d   Le Faou, Alain ^a,g   Bélec, Laurent ^b,e  

^a INSTITUT PASTEUR DE BANGUI   (Central African Republic)

^b HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^c Complexe Pédiatrique ^*  (Central African Republic)

^d Faculté des sciences de la santéde Bangui   (Central African Republic)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f MCGILL UNIVERSITY   (Canada)

^g UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 160 ANTIBODY; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; LACTOFERRIN; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ADULT; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTICLE; B LYMPHOCYTE; BREAST FEEDING; BREAST MILK; CENTRAL AFRICAN REPUBLIC; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; FECES LEVEL; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMORAL IMMUNITY; IN VITRO STUDY; INTESTINE MUCOSA; MACROPHAGE; MILK LEVEL; MOTHER; MUCOSAL IMMUNITY; NONHUMAN; PROSPECTIVE STUDY; VIRUS ATTACHMENT;

ADAPTIVE IMMUNITY; ADULT; B-LYMPHOCYTES; BREAST FEEDING; CHILD; FECES; FEMALE; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP160; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN FAB FRAGMENTS; INFANT; INTESTINAL MUCOSA; LACTOFERRIN; MILK, HUMAN; REFERENCE STANDARDS; SPECIES SPECIFICITY; YOUNG ADULT;

EID: 84878002628     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063408     Document Type: Article

References (113)

1. UNAIDS (2011) Global HIV/AIDS response. Epidemic update and health sector progress towards Universal Acces.
2. Van de Perre P, Simonon A, Hitimana DG, Dabis F, Msellati P, et al. (1993) Infective and anti-infective properties of breastmilk from HIV-1-infected women. Lancet 341: 914-918.
3. Datta P, Embree JE, Kreiss JK, Ndinya-Achola JO, Braddick M, et al. (1994) Mother-to-child transmission of human immunodeficiency virus type 1: report from the Nairobi Study. J Infect Dis 170: 1134-1140.
4. Bulterys M, Chao A, Dushimimana A, Saah A, (1995) HIV-1 seroconversion after 20 months of age in a cohort of breastfed children born to HIV-1-infected women in Rwanda. AIDS 9: 93-94.
5. Bertolli J, St Louis ME, Simonds RJ, Nieburg P, Kamenga M, et al. (1996) Estimating the timing of mother-to-child transmission of human immunodeficiency virus in a breast-feeding population in Kinshasa, Zaire. J Infect Dis 174: 722-726.
6. Bobat R, Moodley D, Coutsoudis A, Coovadia H, (1997) Breastfeeding by HIV-1-infected women and outcome in their infants: a cohort study from Durban, South Africa. AIDS 11: 1627-1633.
7. Ekpini ER, Wiktor SZ, Satten GA, AdjorloloJohnson GT, Sibailly TS, et al. (1997) Late postnatal mother-to-child transmission of HIV-1 in Abidjan, Cote d'Ivoire. Lancet 349: 1054-1059.
8. Miotti PG, Taha TET, Kumwenda NI, Broadhead R, Mtimavalye LAR, et al. (1999) HIV transmission through breastfeeding- A study in Malawi. Jama-Journal of the American Medical Association 282: 744-749.
9. Fowler MG, Newell ML, (2002) Breast-feeding and HIV-1 transmission in resource-limited settings. Journal of Acquired Immune Deficiency Syndromes 30: 230-239.
10. John-Stewart G, Mbori-Ngacha D, Ekpini R, Janoff EN, Nkengasong J, et al. (2004) Breast-feeding and Transmission of HIV-1. J Acquir Immune Defic Syndr 35: 196-202.
11. Thior I, Lockman S, Smeaton LM, Shapiro RL, Wester C, et al. (2006) Breastfeeding plus infant zidovudine prophylaxis for 6 months vs formula feeding plus infant zidovudine for 1 month to reduce mother-to-child HIV transmission in Botswana: a randomized trial: the Mashi Study. JAMA 296: 794-805.
12. Kumwenda NI, Hoover DR, Mofenson LM, Thigpen MC, Kafulafula G, et al. (2008) Extended antiretroviral prophylaxis to reduce breast-milk HIV-1 transmission. N Engl J Med 359: 119-129.
13. Chasela CS, Hudgens MG, Jamieson DJ, Kayira D, Hosseinipour MC, et al. (2010) Maternal or infant antiretroviral drugs to reduce HIV-1 transmission. N Engl J Med 362: 2271-2281.
14. Shapiro RL, Hughes MD, Ogwu A, Kitch D, Lockman S, et al. (2010) Antiretroviral regimens in pregnancy and breast-feeding in Botswana. N Engl J Med 362: 2282-2294.
15. Wilson CB (2005) Developmental immunology and role of host defenses in neonatal susceptibility. In: Remington J KJ, editor. Infectious diseases of the fetus and newborn infant. Philadelphia, PA: WB Saunders Company. 37-49.
16. Lewis P, Nduati R, Kreiss JK, John GC, Richardson BA, et al. (1998) Cell-free human immunodeficiency virus type 1 in breast milk. J Infect Dis 177: 34-39.
17. Neveu D, Viljoen J, Bland RM, Nagot N, Danaviah S, et al. (2011) Cumulative exposure to cell-free HIV in breast milk, rather than feeding pattern per se, identifies postnatally infected infants. Clinical Infectious Diseases 52: 819-825.
18. Richardson BA, John-Stewart GC, Hughes JP, Nduati R, Mbori-Ngacha D, et al. (2003) Breast-milk infectivity in human immunodeficiency virus type 1-infected mothers. J Infect Dis 187: 736-740.
19. Coovadia HM, Rollins NC, Bland RM, Little K, Coutsoudis A, et al. (2007) Mother-to-child transmission of HIV-1 infection during exclusive breastfeeding in the first 6 months of life: an intervention cohort study. Lancet 369: 1107-1116.
20. Kourtis AP, Butera S, Ibegbu C, Belec L, Duerr A, (2003) Breast milk and HIV-1: vector of transmission or vehicle of protection? Lancet Infect Dis 3: 786-793.
21. Belec L, Kourtis AP, (2012) B lymphocyte-derived humoral immune defenses in breast milk transmission of the HIV-1. Adv Exp Med Biol 743: 139-160.
22. Brandtzaeg P, (2003) Mucosal immunity: integration between mother and the breast-fed infant. Vaccine 21: 3382-3388.
23. Farquhar C, John-Stewart G, (2003) The role of infant immune responses and genetic factors in preventing HIV-1 acquisition and disease progression. Clin Exp Immunol 134: 367-377.
24. Van de Perre P, (1999) Mother-to-child transmission of HIV-1: the 'all mucosal' hypothesis as a predominant mechanism of transmission. AIDS 13: 1133-1138.
25. Farquhar C, VanCott T, Bosire R, Bermudez C, Mbori-Ngacha D, et al. (2008) Salivary human immunodeficiency virus (HIV)-1-specific immunoglobulin A in HIV-1-exposed infants in Kenya. Clin Exp Immunol 153: 37-43.
26. John-Stewart GC, Mbori-Ngacha D, Payne BL, Farquhar C, Richardson BA, et al. (2009) HV-1-specific cytotoxic T lymphocytes and breast milk HIV-1 transmission. J Infect Dis 199: 889-898.
27. Gody JC, Charpentier C, Mbitikon O, Si-Mohamed A, LeGoff J, et al. (2008) High prevalence of antiretroviral drug resistance mutations in HIV-1 non-B subtype strains from African children receiving antiretroviral therapy regimen according to the 2006 revised WHO recommendations. J Acquir Immune Defic Syndr 49: 566-569.
28. Moussa S, Pinson P, Pelembi P, Gody JC, Mbitikon O, et al. (2010) First data on HIV-1 resistance mutations to antiretroviral drugs in Central African Republic. AIDS Res Hum Retroviruses 26: 1247-1248.
29. Charpentier C, Gody JC, Mbitikon O, Moussa S, Matta M, et al. (2012) Virological response and resistance profiles after 18 to 30 months of first- or second-/third-line antiretroviral treatment: a cross-sectional evaluation in HIV type 1-infected children living in the Central African Republic. AIDS Res Hum Retroviruses 28: 87-94.
30. (WHO) WHO (2010) Antiretroviral therapy for HIV infection in babies and children: Towards universal access. Recommendations for a public health approach.
31. (WHO) WHO (2010) recommendations Antiretroviral therapy for HIV infection in adults and adolescents. Antiretroviral therapy for a public health approach.
32. Chintu C, Bhat GJ, Walker AS, Mulenga V, Sinyinza F, et al. (2004) Co-trimoxazole as prophylaxis against opportunistic infections in HIV-infected Zambian children (CHAP): a double-blind randomised placebo-controlled trial. Lancet 364: 1865-1871.
33. Becquart P, Hocini H, Garin B, Sepou A, Kazatchkine MD, et al. (1999) Compartmentalization of the IgG immune response to HIV-1 in breast milk. AIDS 13: 1323-1331.
34. Rouet F, Sakarovitch C, Msellati P, Elenga N, Montcho C, et al. (2003) Pediatric viral human immunodeficiency virus type 1 RNA levels, timing of infection, and disease progression in African HIV-1-infected children. Pediatrics 112: e289.
35. Rouet F, Chaix ML, Nerrienet E, Ngo-Giang-Huong N, Plantier JC, et al. (2007) Impact of HIV-1 genetic diversity on plasma HIV-1 RNA Quantification: usefulness of the Agence Nationale de Recherches sur le SIDA second-generation long terminal repeat-based real-time reverse transcriptase polymerase chain reaction test. J Acquir Immune Defic Syndr 45: 380-388.
36. Buchacher A, Predl R, Strutzenberger K, Steinfellner W, Trkola A, et al. (1994) Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res Hum Retroviruses 10: 359-369.
37. Becquart P, Hocini H, Levy M, Sepou A, Kazatchkine MD, et al. (2000) Secretory anti-human immunodeficiency virus (HIV) antibodies in colostrum and breast milk are not a major determinant of the protection of early postnatal transmission of HIV. J Infect Dis 181: 532-539.
38. Chomont N, Hocini H, Gody JC, Bouhlal H, Becquart P, et al. (2008) Neutralizing monoclonal antibodies to human immunodeficiency virus type 1 do not inhibit viral transcytosis through mucosal epithelial cells. Virology 370: 246-254.
39. Saidi H, Eslahpazir J, Carbonneil C, Carthagena L, Requena M, et al. (2006) Differential modulation of human lactoferrin activity against both R5 and X4-HIV-1 adsorption on epithelial cells and dendritic cells by natural antibodies. J Immunol 177: 5540-5549.
40. Saidi H, Magri G, Carbonneil C, Nasreddine N, Requena M, et al. (2007) IFN-gamma-activated monocytes weakly produce HIV-1 but induce the recruitment of HIV-sensitive T cells and enhance the viral production by these recruited T cells. J Leukoc Biol 81: 642-653.
41. Saidi H, Jenabian MA, Gombert B, Charpentier C, Mannarini A, et al. (2008) Pre-clinical development as microbicide of zinc tetra-ascorbo-camphorate, a novel terpenoid derivative: potent in vitro inhibitory activity against both R5- and X4-tropic HIV-1 strains without significant in vivo mucosal toxicity. AIDS Res Ther 5: 10.
42. Saidi H, Nasreddine N, Jenabian MA, Lecerf M, Schols D, et al. (2007) Differential in vitro inhibitory activity against HIV-1 of alpha-(1-3)- and alpha-(1-6)-D-mannose specific plant lectins: implication for microbicide development. J Transl Med 5: 28.
43. Kimpton J, Emerman M, (1992) Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated beta-galactosidase gene. J Virol 66: 2232-2239.
44. Becquart P, Courgnaud V, Willumsen J, Van de Perre P, (2007) Diversity of HIV-1 RNA and DNA in breast milk from HIV-1-infected mothers. Virology 363: 256-260.
45. Salazar-Gonzalez JF, Salazar MG, Learn GH, Fouda GG, Kang HH, et al. (2011) Origin and evolution of HIV-1 in breast milk determined by single-genome amplification and sequencing. J Virol 85: 2751-2763.
46. Hocini H, Barra A, Belec L, Iscaki S, Preud'homme JL, et al. (1995) Systemic and secretory humoral immunity in the normal human vaginal tract. Scand J Immunol 42: 269-274.
47. Pfefferkorn MD, Boone JH, Nguyen JT, Juliar BE, Davis MA, et al. (2010) Utility of fecal lactoferrin in identifying Crohn disease activity in children. J Pediatr Gastroenterol Nutr 51: 425-428.
48. Brock JH, (1980) Lactoferrin in human milk: its role in iron absorption and protection against enteric infection in the newborn infant. Arch Dis Child 55: 417-421.
49. Spik G, Brunet B, Mazurier-Dehaine C, Fontaine G, Montreuil J, (1982) Characterization and properties of the human and bovine lactotransferrins extracted from the faeces of newborn infants. Acta Paediatr Scand 71: 979-985.
50. Levay PF, Viljoen M, (1995) Lactoferrin: a general review. Haematologica 80: 252-267.
51. Langhorst J, Boone J, (2012) Fecal lactoferrin as a noninvasive biomarker in inflammatory bowel diseases. Drugs Today (Barc) 48: 149-161.
52. Goldman AS, Garza C, Schanler RJ, Goldblum RM, (1990) Molecular forms of lactoferrin in stool and urine from infants fed human milk. Pediatr Res 27: 252-255.
53. Eslahpazir J, Jenabian MA, Bouhlal H, Hocini H, Carbonneil C, et al. (2008) Infection of macrophages and dendritic cells with primary R5-tropic human immunodeficiency virus type 1 inhibited by natural polyreactive anti-CCR5 antibodies purified from cervicovaginal secretions. Clin Vaccine Immunol 15: 872-884.
54. Carthagena L, Becquart P, Hocini H, Kazatchkine MD, Bouhlal H, et al. (2011) 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 5: 27-34.
55. Creek TL, Sherman GG, Nkengasong J, Lu L, Finkbeiner T, et al. (2007) Infant human immunodeficiency virus diagnosis in resource-limited settings: issues, technologies, and country experiences. Am J Obstet Gynecol 197: S64-71.
56. Sherman GG, Cooper PA, Coovadia AH, Puren AJ, Jones SA, et al. (2005) Polymerase chain reaction for diagnosis of human immunodeficiency virus infection in infancy in low resource settings. Pediatr Infect Dis J 24: 993-997.
57. Lehman DA, Farquhar C, (2007) Biological mechanisms of vertical human immunodeficiency virus (HIV-1) transmission. Rev Med Virol 17: 381-403.
58. C W (2005) Developmental immunology and role of host defenses in neonatal susceptibility. In: Remington J, Klein J, ed. Infectious diseases of the fetus and newborn infant, 6th edition. Philadelphia, PA: WB Saunders Company: 37-49.
59. Ballan WM, Vu BA, Long BR, Loo CP, Michaelsson J, et al. (2007) Natural killer cells in perinatally HIV-1-infected children exhibit less degranulation compared to HIV-1-exposed uninfected children and their expression of KIR2DL3, NKG2C, and NKp46 correlates with disease severity. J Immunol 179: 3362-3370.
60. Tiemessen CT, Shalekoff S, Meddows-Taylor S, Schramm DB, Papathanasopoulos MA, et al. (2009) Cutting Edge: Unusual NK cell responses to HIV-1 peptides are associated with protection against maternal-infant transmission of HIV-1. J Immunol 182: 5914-5918.
61. De Milito A, Nilsson A, Titanji K, Thorstensson R, Reizenstein E, et al. (2004) Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood 103: 2180-2186.
62. Titanji K, Chiodi F, Bellocco R, Schepis D, Osorio L, et al. (2005) Primary HIV-1 infection sets the stage for important B lymphocyte dysfunctions. AIDS 19: 1947-1955.
63. D'Orsogna LJ, Krueger RG, McKinnon EJ, French MA, (2007) Circulating memory B-cell subpopulations are affected differently by HIV infection and antiretroviral therapy. AIDS 21: 1747-1752.
64. Chong Y, Ikematsu H, Kikuchi K, Yamamoto M, Murata M, et al. (2004) Selective CD27+ (memory) B cell reduction and characteristic B cell alteration in drug-naive and HAART-treated HIV type 1-infected patients. AIDS Res Hum Retroviruses 20: 219-226.
65. Chong Y, Ikematsu H, Yamamoto M, Murata M, Yamaji K, et al. (2004) Increased frequency of CD27- (naive) B cells and their phenotypic alteration in HIV type 1-infected patients. AIDS Res Hum Retroviruses 20: 621-629.
66. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, et al. (1983) Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med 309: 453-458.
67. Agarwal S, Karmaus W, Davis S, Gangur V, (2011) Immune markers in breast milk and fetal and maternal body fluids: a systematic review of perinatal concentrations. J Hum Lact 27: 171-186.
68. Cummins AG, Thompson FM, (1997) Postnatal changes in mucosal immune response: a physiological perspective of breast feeding and weaning. Immunol Cell Biol 75: 419-429.
69. Filipp D, Alizadeh-Khiavi K, Richardson C, Palma A, Paredes N, et al. (2001) Soluble CD14 enriched in colostrum and milk induces B cell growth and differentiation. Proc Natl Acad Sci U S A 98: 603-608.
70. Lepage P, Van de Perre P, (2012) The immune system of breast milk: antimicrobial and anti-inflammatory properties. Adv Exp Med Biol 743: 121-137.
71. Bunders M, Pembrey L, Kuijpers T, Newell ML, (2010) Evidence of impact of maternal HIV infection on immunoglobulin levels in HIV-exposed uninfected children. AIDS Res Hum Retroviruses 26: 967-975.
72. Filteau S, (2009) The HIV-exposed, uninfected African child. Trop Med Int Health 14: 276-287.
73. Van de Perre P, (2000) Breast milk transmission of HIV-1. Laboratory and clinical studies. Ann N Y Acad Sci 918: 122-127.
74. Van de Perre P, Hitimana DG, Lepage P, (1988) Human immunodeficiency virus antibodies of IgG, IgA, and IgM subclasses in milk of seropositive mothers. J Pediatr 113: 1039-1041.
75. Belec L, Bouquety JC, Georges AJ, Siopathis MR, Martin PM, (1990) Antibodies to human immunodeficiency virus in the breast milk of healthy, seropositive women. Pediatrics 85: 1022-1026.
76. Duprat C, Mohammed Z, Datta P, Stackiw W, Ndinya-Achola JO, et al. (1994) Human immunodeficiency virus type 1 IgA antibody in breast milk and serum. Pediatr Infect Dis J 13: 603-608.
77. Lu FX, (2000) Predominate HIV1-specific IgG activity in various mucosal compartments of HIV1-infected individuals. Clin Immunol 97: 59-68.
78. Mestecky J, Jackson S, Moldoveanu Z, Nesbit LR, Kulhavy R, et al. (2004) Paucity of antigen-specific IgA responses in sera and external secretions of HIV-type 1-infected individuals. AIDS Res Hum Retroviruses 20: 972-988.
79. Fouda GG, Yates NL, Pollara J, Shen X, Overman GR, et al. (2011) HIV-specific functional antibody responses in breast milk mirror those in plasma and are primarily mediated by IgG antibodies. J Virol 85: 9555-9567.
80. Kuhn L, Trabattoni D, Kankasa C, Sinkala M, Lissoni F, et al. (2006) Hiv-specific secretory IgA in breast milk of HIV-positive mothers is not associated with protection against HIV transmission among breast-fed infants. J Pediatr 149: 611-616.
81. Belec L, Georges AJ, Steenman G, Martin PM, (1989) Antibodies to human immunodeficiency virus in vaginal secretions of heterosexual women. J Infect Dis 160: 385-391.
82. Belec L, Dupre T, Prazuck T, Tevi-Benissan C, Kanga JM, et al. (1995) Cervicovaginal overproduction of specific IgG to human immunodeficiency virus (HIV) contrasts with normal or impaired IgA local response in HIV infection. J Infect Dis 172: 691-697.
83. Wolff H, Mayer K, Seage G, Politch J, Horsburgh CR, et al. (1992) A comparison of HIV-1 antibody classes, titers, and specificities in paired semen and blood samples from HIV-1 seropositive men. J Acquir Immune Defic Syndr 5: 65-69.
84. Artenstein AW, VanCott TC, Sitz KV, Robb ML, Wagner KF, et al. (1997) Mucosal immune responses in four distinct compartments of women infected with human immunodeficiency virus type 1: a comparison by site and correlation with clinical information. J Infect Dis 175: 265-271.
85. Haimovici F, Mayer KH, Anderson DJ, (1997) Quantitation of HIV-1-specific IgG, IgA, and IgM antibodies in human genital tract secretions. J Acquir Immune Defic Syndr Hum Retrovirol 15: 185-191.
86. Raux M, Finkielsztejn L, Salmon-Ceron D, Bouchez H, Excler JL, et al. (1999) Comparison of the distribution of IgG and IgA antibodies in serum and various mucosal fluids of HIV type 1-infected subjects. AIDS Res Hum Retroviruses 15: 1365-1376.
87. Wright PF, Kozlowski PA, Rybczyk GK, Goepfert P, Staats HF, et al. (2002) Detection of mucosal antibodies in HIV type 1-infected individuals. AIDS Res Hum Retroviruses 18: 1291-1300.
88. Alexander R, Mestecky J, (2007) Neutralizing antibodies in mucosal secretions: IgG or IgA? Curr HIV Res 5: 588-593.
89. Goldman AS, (1993) The immune system of human milk: antimicrobial, antiinflammatory and immunomodulating properties. Pediatr Infect Dis J 12: 664-671.
90. Israel ZR, Marx PA, (1995) Nonclassical mucosal antibodies predominate in genital secretions of HIV-1 infected chimpanzees. J Med Primatol 24: 53-60.
91. Permar SR, Wilks AB, Ehlinger EP, Kang HH, Mahlokozera T, et al. (2010) Limited contribution of mucosal IgA to Simian immunodeficiency virus (SIV)-specific neutralizing antibody response and virus envelope evolution in breast milk of SIV-infected, lactating rhesus monkeys. J Virol 84: 8209-8218.
92. Schafer F, Kewenig S, Stolte N, Stahl-Hennig C, Stallmach A, et al. (2002) Lack of simian immunodeficiency virus (SIV) specific IgA response in the intestine of SIV infected rhesus macaques. Gut 50: 608-614.
93. Hanson LA, Ahlstedt S, Andersson B, Cruz JR, Dahlgren U, et al. (1984) The immune response of the mammary gland and its significance for the neonate. Ann Allergy 53: 576-582.
94. Jonard PP, Rambaud JC, Dive C, Vaerman JP, Galian A, et al. (1984) Secretion of immunoglobulins and plasma proteins from the jejunal mucosa. Transport rate and origin of polymeric immunoglobulin A. J Clin Invest 74: 525-535.
95. Laibe S, Bard E, Biichle S, Vielle J, Millon L, et al. (2003) New sensitive method for the measurement of lysozyme and lactoferrin to explore mucosal innate immunity. Part II: time-resolved immunofluorometric assay used in HIV patients with oral candidiasis. Clin Chem Lab Med 41: 134-138.
96. Brandtzaeg P FI (1994) The human mucosal B-cell system. In Mucosal Immunology. In: Ogra PL MJ, Lamm ME, Strober W, Bienenstock J, McGhee editor. Second Edition ed: Academic Press. 439-468.
97. Ruggeri FM, Johansen K, Basile G, Kraehenbuhl JP, Svensson L, (1998) Antirotavirus immunoglobulin A neutralizes virus in vitro after transcytosis through epithelial cells and protects infant mice from diarrhea. J Virol 72: 2708-2714.
98. Long KZ, Garcia C, Ko G, Santos JI, Al Mamun A, et al. (2011) Vitamin A modifies the intestinal chemokine and cytokine responses to norovirus infection in Mexican children. J Nutr 141: 957-963.
99. Ogra PL, (1995) Comparative evaluation of immunization with live attenuated and inactivated poliovirus vaccines. Ann N Y Acad Sci 754: 97-107.
100. Hird TR, Grassly NC, (2012) Systematic review of mucosal immunity induced by oral and inactivated poliovirus vaccines against virus shedding following oral poliovirus challenge. PLoS Pathog 8: e1002599.
101. Fantini J, Yahi N, Baghdiguian S, Chermann JC, (1992) Human colon epithelial cells productively infected with human immunodeficiency virus show impaired differentiation and altered secretion. J Virol 66: 580-585.
102. Bouhlal H, Chomont N, Haeffner-Cavaillon N, Kazatchkine MD, Belec L, et al. (2002) Opsonization of HIV-1 by semen complement enhances infection of human epithelial cells. J Immunol 169: 3301-3306.
103. Smith PD, Meng G, Salazar-Gonzalez JF, Shaw GM, (2003) Macrophage HIV-1 infection and the gastrointestinal tract reservoir. J Leukoc Biol 74: 642-649.
104. Margolis L, Shattock R, (2006) Selective transmission of CCR5-utilizing HIV-1: the 'gatekeeper' problem resolved? Nat Rev Microbiol 4: 312-317.
105. 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.
106. Hocini H, Becquart P, Bouhlal H, Chomont N, Ancuta P, et al. (2001) Active and selective transcytosis of cell-free human immunodeficiency virus through a tight polarized monolayer of human endometrial cells. J Virol 75: 5370-5374.
107. Moog C, (2008) Immune responses that correlate with HIV-1 protection? AIDS 22: 1461-1462.
108. Shearer G, Clerici M, (2010) Historical perspective on HIV-exposed seronegative individuals: has nature done the experiment for us? J Infect Dis 202Suppl 3: S329-332.
109. Belec L, Ghys PD, Hocini H, Nkengasong JN, Tranchot-Diallo J, et al. (2001) Cervicovaginal secretory antibodies to human immunodeficiency virus type 1 (HIV-1) that block viral transcytosis through tight epithelial barriers in highly exposed HIV-1-seronegative African women. J Infect Dis 184: 1412-1422.
110. Hirbod T, Broliden K, (2007) Mucosal immune responses in the genital tract of HIV-1-exposed uninfected women. J Intern Med 262: 44-58.
111. Hasselrot K, (2009) Genital and oral mucosal immune response against HIV-1 in exposed uninfected individuals. Crit Rev Immunol 29: 369-377.
112. Mestecky J, Wright PF, Lopalco L, Staats HF, Kozlowski PA, et al. (2011) Scarcity or absence of humoral immune responses in the plasma and cervicovaginal lavage fluids of heavily HIV-1-exposed but persistently seronegative women. AIDS Res Hum Retroviruses 27: 469-486.
113. Semba RD, Neville MC, (1999) Breast-feeding, mastitis, and HIV transmission: nutritional implications. Nutr Rev 57: 146-153.