Cellular immunity in breast milk: Implications for postnatal transmission of HIV-1 to the infant

Advances in Experimental Medicine and Biology

Volumn 743, Issue , 2012, Pages 161-169

  Sabbaj, Steffanie ^a   Ibegbu, Chris C ^b   Kourtis, Athena P ^c  

^a University of Alabama at Birmingham   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL CENTER FOR CHRONIC DISEASE PREVENTION AND HEALTH PROMOTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE;

ADAPTIVE IMMUNITY; ARTICLE; B LYMPHOCYTE ACTIVATION; BREAST FEEDING; BREAST MILK; CELL COMPARTMENTALIZATION; CELL COMPOSITION; CELL HOMING; CELLULAR IMMUNITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INFANT; INFECTION RISK; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MOLECULAR DYNAMICS; NONHUMAN; PERINATAL PERIOD; PERIPHERAL LYMPHOCYTE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK ASSESSMENT; T LYMPHOCYTE ACTIVATION; VIRUS TRANSMISSION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84859904706     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-2251-8_11     Document Type: Article

References (86)

1. Kourtis AP, Bulterys M (2010) Mother-to-child transmission of HIV: pathogenesis, mechanisms and pathways. Clin Perinatol 37(4):721-737
2. Kourtis AP, Butera S, Ibegbu C, Beled L, Duerr A (2003) Breast milk and HIV-1: vector of transmission or vehicle of protection? Lancet Infect Dis 3(12):786-793
3. Aldrovandi GM, Kuhn L (2010) What infants and breasts can teach us about natural protection from HIV infection. J Infect Dis 202(Suppl 3):S366-S370
4. Leroy V, Newell ML, Dabis F, Peckham C, Van de Perre P, Bulterys M et al (1998) International multicentre pooled analysis of late postnatal mother-to-child transmission of HIV-1 infection. Ghent International Working Group on Mother-to-Child Transmission of HIV. Lancet 352(9128):597-600
5. Nduati R, John G, Mbori-Ngacha D, Richardson B, Overbaugh J, Mwatha A et al (2000) Effect of breastfeeding and formula feeding on transmission of HIV-1: a randomized clinical trial. JAMA 283(9):1167-1174
6. Van de Perre P, Simonon A, Hitimana DG, Dabis F, Msellati P, Mukamabano B et al (1993) Infective and antiinfective properties of breastmilk from HIV-1-infected women. Lancet 341(8850):914-918
7. Garofalo R (2010) Cytokines in human milk. J Pediatr 156(2 Suppl):S36-S40
8. Goldman AS, Chheda S, Garofalo R, Schmalstieg FC (1996) Cytokines in human milk: properties and potential effects upon the mammary gland and the neonate. J Mammary Gland Biol Neoplasia 1(3):251-258
9. Koulinska IN, Villamor E, Chaplin B, Msamanga G, Fawzi W, Renjifo B et al (2006) Transmission of cell-free and cell-associated HIV-1 through breast-feeding. J Acquir Immune Defi c Syndr 41(1):93-99
10. Rousseau CM, Nduati RW, Richardson BA, Steele MS, John-Stewart GC, Mbori-Ngacha DA et al (2003) Longitudinal analysis of human immunodefi ciency virus type 1 RNA in breast milk and of its relationship to infant infection and maternal disease. J Infect Dis 187(5):741-747
11. Toniolo A, Serra C, Conaldi PG, Basolo F, Falcone V, Dolei A (1995) Productive HIV-1 infection of normal human mammary epithelial cells. AIDS 9(8):859-866
12. Alfsen A, Yu H, Magerus-Chatinet A, Schmitt A, Bomsel M (2005) HIV-1-infected blood mononuclear cells form an integrin- and agrin-dependent viral synapse to induce effi cient HIV-1 transcytosis across epithelial cell monolayer. Mol Biol Cell 16(9):4267-4279
13. Bulek K, Swaidani S, Aronica M, Li X (2010) Epithelium: the interplay between innate and Th2 immunity. Immunol Cell Biol 88(3):257-268
14. Dorosko SM, Connor RI (2010) Primary human mammary epithelial cells endocytose HIV-1 and facilitate viral infection of CD4+ T lymphocytes. J Virol 84(20):10533-10542
15. Lyimo MA, Howell AL, Balandya E, Eszterhas SK, Connor RI (2009) Innate factors in human breast milk inhibit cell-free HIV-1 but not cell-associated HIV-1 infection of CD4+ cells. J Acquir Immune Defi c Syndr 51(2): 117-124
16. Bertotto A, Castellucci G, Radicioni M, Bartolucci M, Vaccaro R (1996) CD40 ligand expression on the surface of colostral T cells. Arch Dis Child Fetal Neonatal Ed 74(2):F135-F136
17. Bertotto A, Gerli R, Fabietti G, Crupi S, Arcangeli C, Scalise F et al (1990) Human breast milk T lymphocytes display the phenotype and functional characteristics of memory T cells. Eur J Immunol 20(8):1877-1880
18. Bertotto A, Spinozzi F, Gerli R, Castellucci G, Bassotti G, Crupi S et al (1995) CD26 and CD31 surface antigen expression on human colostral T cells. Biol Neonate 68(4):259-263
19. Crago SS, Prince SJ, Pretlow TG, McGhee JR, Mestecky J (1979) Human colostral cells. I. Separation and characterization. Clin Exp Immunol 38(3):585-597
20. Davis MK (1991) Human milk and HIV infection: epidemiologic and laboratory data. Adv Exp Med Biol 310:271-280
21. Eglinton BA, Roberton DM, Cummins AG (1994) Phenotype of T cells, their soluble receptor levels, and cytokine profi le of human breast milk. Immunol Cell Biol 72(4):306-313
22. Goldman AS, Chheda S, Garofalo R (1998) Evolution of immunologic functions of the mammary gland and the postnatal development of immunity. Pediatr Res 43(2):155-162
23. Jarvinen KM, Suomalainen H (2002) Leucocytes in human milk and lymphocyte subsets in cows milk-allergic infants. Pediatr Allergy Immunol 13(4):243-254
24. Lindstrand A, Smedman L, Gunnlaugsson G, Troye-Blomberg M (1997) Selective compartmentalization of gammadelta-T lymphocytes in human breastmilk. Acta Paediatr 86(8):890-891
25. Moro I, Abo T, Crago SS, Komiyama K, Mestecky J (1985) Natural killer cells in human colostrum. Cell Immunol 93(2):467-474
26. Ogra SS, Ogra PL (1978) Immunologic aspects of human colostrum and milk. II. Characteristics of lymphocyte reactivity and distribution of E-rosette forming cells at different times after the onset of lactation. J Pediatr 92(4):550-555
27. Ogra SS, Weintraub D, Ogra PL (1977) Immunologic aspects of human colostrum and milk. III. Fate and absorption of cellular and soluble components in the gastrointestinal tract of the newborn. J Immunol 119(1):245-248
28. Xanthou M (1997) Human milk cells. Acta Paediatr 86(12):1288-1290
29. Parmely MJ, Beer AE, Billingham RE (1976) In vitro studies on the T-lymphocyte population of human milk. J Exp Med 144(2):358-370
30. Thorpe LW, Rudloff HE, Powell LC, Goldman AS (1986) Decreased response of human milk leukocytes to chemoattractant peptides. Pediatr Res 20(4):373-377
31. Williamson MT, Murti PK (1996) Effects of storage, time, temperature, and composition of containers on biologic components of human milk. J Hum Lact 12(1):31-35
32. Ho FC, Wong RL, Lawton JW (1979) Human colostral and breast milk cells. A light and electron microscopic study. Acta Paediatr Scand 68(3):389-396
33. Keller MA, Turner JL, Stratton JA, Miller ME (1980) Breast milk lymphocyte response to K1 antigen of Escherichia coli . Infect Immun 27(3):903-909
34. Wirt DP, Adkins LT, Palkowetz KH, Schmalstieg FC, Goldman AS (1992) Activated and memory T lymphocytes in human milk. Cytometry 13(3):282-290
35. Satomi M, Shimizu M, Shinya E, Watari E, Owaki A, Hidaka C et al (2005) Transmission of macrophage-tropic HIV-1 by breast-milk macrophages via DC-SIGN. J Infect Dis 191(2):174-181
36. Yagi Y, Watanabe E, Watari E, Shinya E, Satomi M, Takeshita T et al (2010) Inhibition of DC-SIGN-mediated transmission of human immunodefi ciency virus type 1 by Toll-like receptor 3 signalling in breast milk macrophages. Immunology 130(4):597-607
37. Kourtis AP, Ibegbu CC, Theiler R, Xu YX, Bansil P, Jamieson DJ et al (2007) Breast milk CD4+ T cells express high levels of C chemokine receptor 5 and CXC chemokine receptor 4 and are preserved in HIV-infected mothers receiving highly active antiretroviral therapy. J Infect Dis 195(7):965-972
38. Tuaillon E, Valea D, Becquart P, Al Tabaa Y, Meda N, Bollore K et al (2009) Human milk-derived B cells: a highly activated switched memory cell population primed to secrete antibodies. J Immunol 182(11):7155-7162
39. Ichikawa M, Sugita M, Takahashi M, Satomi M, Takeshita T, Araki T et al (2003) Breast milk macrophages spontaneously produce granulocyte-macrophage colony-stimulating factor and differentiate into dendritic cells in the presence of exogenous interleukin-4 alone. Immunology 108(2):189-195
40. Sabbaj S, Ghosh MK, Edwards BH, Leeth R, Decker WD, Goepfert PA et al (2005) Breast milk-derived antigenspecifi c CD8+ T cells: an extralymphoid effector memory cell population in humans. J Immunol 174(5): 2951-2956
41. Rivas RA, el-Mohandes AA, Katona IM (1994) Mononuclear phagocytic cells in human milk: HLA-DR and Fc gamma R ligand expression. Biol Neonate 66(4):195-204
42. Farstad IN, Halstensen TS, Lien B, Kilshaw PJ, Lazarovits AI, Brandtzaeg P (1996) Distribution of beta 7 integrins in human intestinal mucosa and organized gut-associated lymphoid tissue. Immunology 89(2):227-237
43. Hladik F, Lentz G, Delpit E, McElroy A, McElrath MJ (1999) Coexpression of CCR5 and IL-2 in human genital but not blood T cells: implications for the ontogeny of the CCR5+ Th1 phenotype. J Immunol 163(4):2306-2313
44. Hussain LA, Kelly CG, Fellowes R, Hecht EM, Wilson J, Chapman M et al (1992) Expression and gene transcript of Fc receptors for IgG, HLA class II antigens and Langerhans cells in human cervico-vaginal epithelium. Clin Exp Immunol 90(3):530-538
45. Johansson EL, Rudin A, Wassen L, Holmgren J (1999) Distribution of lymphocytes and adhesion molecules in human cervix and vagina. Immunology 96(2):272-277
46. Quayle AJ, Kourtis AP, Cu-Uvin S, Politch JA, Yang H, Bowman FP et al (2007) T-lymphocyte profi le and total and virus-specifi c immunoglobulin concentrations in the cervix of HIV-1-infected women. J Acquir Immune Defi c Syndr 44(3):292-298
47. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL et al (1998) Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280(5362):427-431
48. Zabel BA, Agace WW, Campbell JJ, Heath HM, Parent D, Roberts AI et al (1999) Human G protein-coupled receptor GPR-9-6/CC chemokine receptor 9 is selectively expressed on intestinal homing T lymphocytes, mucosal lymphocytes, and thymocytes and is required for thymus-expressed chemokine-mediated chemotaxis. J Exp Med 190(9):1241-1256
49. Bush JF, Beer AE (1979) Analysis of complement receptors on B-lymphocytes in human milk. Am J Obstet Gynecol 133(6):708-712
50. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ et al (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200(6):749-759
51. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M (2005) Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434(7037):1093-1097
52. Permar SR, Kang HH, Carville A, Wilks AB, Mansfield KG, Rao SS et al (2010) Preservation of memory CD4(+) T lymphocytes in breast milk of lactating rhesus monkeys during acute simian immunodefi ciency virus infection. J Infect Dis 201(2):302-310
53. Alkhatib G (2009) The biology of CCR5 and CXCR4. Curr Opin HIV AIDS 4(2):96-103
54. Wu Y, Yoder A (2009) Chemokine coreceptor signaling in HIV-1 infection and pathogenesis. PLoS Pathog 5(12):e1000520
55. Veazey RS, Marx PA, Lackner AA (2003) Vaginal CD4+ T cells express high levels of CCR5 and are rapidly depleted in simian immunodefi ciency virus infection. J Infect Dis 187(5):769-776
56. Petitjean G, Becquart P, Tuaillon E, Al Tabaa Y, Valea D, Huguet MF et al (2007) Isolation and characterization of HIV-1-infected resting CD4+ T lymphocytes in breast milk. J Clin Virol 39(1):1-8
57. Brenchley JM, Karandikar NJ, Betts MR, Ambrozak DR, Hill BJ, Crotty LE et al (2003) Expression of CD57 defi nes replicative senescence and antigen-induced apoptotic death of CD8+ T cells. Blood 101(7):2711-2720
58. Lewis P, Nduati R, Kreiss JK, John GC, Richardson BA, Mbori-Ngacha D et al (1998) Cell-free human immunodefi ciency virus type 1 in breast milk. J Infect Dis 177(1):34-39
59. Smith CW, Goldman AS (1968) The cells of human colostrum. I. In vitro studies of morphology and functions. Pediatr Res 2(2):103-109
60. Allison JP, McIntyre BW, Bloch D (1982) Tumor-specifi c antigen of murine T-lymphoma defi ned with monoclonal antibody. J Immunol 129(5):2293-2300
61. Haskins K, Kubo R, White J, Pigeon M, Kappler J, Marrack P (1983) The major histocompatibility complexrestricted antigen receptor on T cells. I. Isolation with a monoclonal antibody. J Exp Med 157(4):1149-1169
62. Hedrick SM, Cohen DI, Nielsen EA, Davis MM (1984) Isolation of cDNA clones encoding T cell-specifi c membrane-associated proteins. Nature 308(5955):149-153
63. Hedrick SM, Nielsen EA, Kavaler J, Cohen DI, Davis MM (1984) Sequence relationships between putative T-cell receptor polypeptides and immunoglobulins. Nature 308(5955):153-158
64. Meuer SC, Fitzgerald KA, Hussey RE, Hodgdon JC, Schlossman SF, Reinherz EL (1983) Clonotypic structures involved in antigen-specifi c human T cell function. Relationship to the T3 molecular complex. J Exp Med 157(2):705-719
65. Yanagi Y, Yoshikai Y, Leggett K, Clark SP, Aleksander I, Mak TW (1984) A human T cell-specifi c cDNA clone encodes a protein having extensive homology to immunoglobulin chains. Nature 308(5955):145-149
66. Ruben FL, Holzman IR, Fireman P (1982) Responses of lymphocytes from human colostrum or milk to infl uenza antigens. Am J Obstet Gynecol 143(5):518-522
67. Totterdell BM, Patel S, Banatvala JE, Chrystie IL (1988) Development of a lymphocyte transformation assay for rotavirus in whole blood and breast milk. J Med Virol 25(1):27-36
68. Scott R, Scott M, Toms GL (1985) Cellular reactivity to respiratory syncytial virus in human colostrum and breast milk. J Med Virol 17(1):83-93
69. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB (1994) Virus-specifi c CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodefi ciency virus type 1 infection. J Virol 68(9):6103-6110
70. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W et al (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodefi ciency virus type 1 syndrome. J Virol 68(7):4650-4655
71. Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, Goedert JJ et al (1999) HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283(5408):1748-1752
72. Hendel H, Caillat-Zucman S, Lebuanec H, Carrington M, OBrien S, Andrieu JM et al (1999) New class I and II HLA alleles strongly associated with opposite patterns of progression to AIDS. J Immunol 162(11):6942-6946
73. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ et al (1996) Infl uence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 2(4):405-411
74. Keet IP, Tang J, Klein MR, LeBlanc S, Enger C, Rivers C et al (1999) Consistent associations of HLA class I and II and transporter gene products with progression of human immunodefi ciency virus type 1 infection in homosexual men. J Infect Dis 180(2):299-309
75. Nelson GW, Kaslow R, Mann DL (1997) Frequency of HLA allele-specifi c peptide motifs in HIV-1 proteins correlates with the alleles association with relative rates of disease progression after HIV-1 infection. Proc Natl Acad Sci USA 94(18):9802-9807
76. Lohman BL, Slyker J, Mbori-Ngacha D, Bosire R, Farquhar C, Obimbo E et al (2003) Prevalence and magnitude of human immunodefi ciency virus (HIV) type 1-specifi c lymphocyte responses in breast milk from HIV-1- seropositive women. J Infect Dis 188(11):1666-1674
77. Sabbaj S, Edwards BH, Ghosh MK, Semrau K, Cheelo S, Thea DM et al (2002) Human immunodefi ciency virusspecifi c CD8(+) T cells in human breast milk. J Virol 76(15):7365-7373
78. Diaz-Jouanen E, Williams RC Jr (1974) T and B lymphocytes in human colostrum. Clin Immunol Immunopathol 3(2):248-255
79. Becquart P, Chomont N, Roques P, Ayouba A, Kazatchkine MD, Belec L et al (2002) Compartmentalization of HIV-1 between breast milk and blood of HIV-infected mothers. Virology 300(1):109-117
80. Losonsky GA, Fishaut JM, Strussenberg J, Ogra PL (1982) Effect of immunization against rubella on lactation products. I. Development and characterization of specifi c immunologic reactivity in breast milk. J Infect Dis 145(5):654-660
81. Permar SR, Kang HH, Carville A, Mansfield KG, Gelman RS, Rao SS et al (2008) Potent simian immunodefi ciency virus-specifi c cellular immune responses in the breast milk of simian immunodefi ciency virus-infected, lactating rhesus monkeys. J Immunol 181(5):3643-3650
82. Wilks AB, Christian EC, Seaman MS, Sircar P, Carville A, Gomez CE et al (2010) Robust vaccine-elicited cellular immune responses in breast milk following systemic simian immunodefi ciency virus DNA prime and live virus vector boost vaccination of lactating rhesus monkeys. J Immunol 185(11):7097-7106
83. Kunkel EJ, Campbell JJ, Haraldsen G, Pan J, Boisvert J, Roberts AI et al (2000) Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specifi c chemokines as an organizing principle in regional immunity. J Exp Med 192(5):761-768
84. Jain L, Vidyasagar D, Xanthou M, Ghai V, Shimada S, Blend M (1989) In vivo distribution of human milk leucocytes after ingestion by newborn baboons. Arch Dis Child 64(7 Spec No):930-933
85. Manning LS, Parmely MJ (1980) Cellular determinants of mammary cell-mediated immunity in the rat. I. The migration of radioisotopically labeled T lymphocytes. J Immunol 125(6):2508-2514
86. Schnorr KL, Pearson LD (1984) Intestinal absorption of maternal leucocytes by newborn lambs. J Reprod Immunol 6(5):329-337