Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut

Mucosal Immunology

Volumn 4, Issue 6, 2011, Pages 603-611

  Mantis, N J ^a,b   Rol, N ^c   Corthesy B ^c  

^a WADSWORTH CENTER   (United States)

^b UNIVERSITY AT ALBANY   (United States)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; FATTY ACID BINDING PROTEIN; IMMUNOGLOBULIN A; SECRETORY COMPONENT;

ANTIGEN ANTIBODY COMPLEX; ANTIGEN ANTIBODY REACTION; ANTIGEN PRESENTING CELL; BACTERIAL CLEARANCE; BACTERIAL VIRULENCE; BIOLOGICAL ACTIVITY; CELIAC DISEASE; CELL ADHESION; CELL TRANSPORT; COMMENSAL; HOMEOSTASIS; HUMAN; IMMUNOGLOBULIN PRODUCTION; IMMUNOREGULATION; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE MUCOSA; MOLECULAR RECOGNITION; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; RECEPTOR BINDING; REVIEW; STEREOSPECIFICITY;

EID: 80054919389     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2011.41     Document Type: Review

References (91)

1. Brandtzaeg P. Function of mucosa-associated lymphoid tissue in antibody formation. Immunol. Invest. 39 303-355 ( 2010
2. He B. et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 26 812-826 ( 2007 (Pubitemid 46915505)
3. Newberry R. D. & Lorenz R. G. Organizing a mucosal defense. Immunol. Rev. 206 6-21 ( 2005 (Pubitemid 41105160)
4. Apter F. M. Lencer W. I. Finkelstein R. A. Mekalanos J. J. & Neutra M. R. Monoclonal immunoglobulin A antibodies directed against cholera toxin prevent the toxin-induced chloride secretory response and block toxin binding to intestinal epithelial cells in vitro. Infect. Immunol. 61 5271-5278 ( 1993 (Pubitemid 23353908)
5. Helander A. Miller C. L. Myers K. S. Neutra M. R. & Nibert M. L. Protective immunoglobulin A and G antibodies bind to overlapping intersubunit epitopes in the head domain of type 1 reovirus adhesion sigma1. J. Virol. 78 10695-10705 ( 2004 (Pubitemid 39258395)
6. Hutchings A. B. et al. Secretory immunoglobulin A antibodies against the sigma1 outer capsid protein of reovirus type 1 Lang prevent infection of mouse Peyer's patches. J. Virol. 78 947-957 ( 2004 (Pubitemid 38067616)
7. Mantis N. J. McGuinness C. R. Sonuyi O. Edwards G. & Farrant S. A. Immunoglobulin A antibodies against ricin A and B subunits protect epithelial cells from ricin intoxication. Infect. Immunol. 74 3455-3462 ( 2006 (Pubitemid 43794535)
8. Stubbe H. Berdoz J. Kraehenbuhl J. P. & Corthésy B. Polymeric IgA is superior to monomeric IgA and IgG carrying the same variable domain in preventing Clostridium diffi cile toxin A damaging of T84 monolayers. J. Immunol. 164 1952-1960 ( 2000 (Pubitemid 30108750)
9. Uren T. K. et al. Vaccine-induced protection against gastrointestinal bacterial infections in the absence of secretory antibodies. Eur. J. Immunol. 35 180-188 ( 2005 (Pubitemid 40123864)
10. Lycke N. Erlandsson L. Ekman L. Schon K. & Leanderson T. Lack of J chain inhibits the transport of gut gA and abrogates the development of intestinal antitoxic protection. J. Immunol. 163 913-919 ( 1999 (Pubitemid 29328102)
11. Apter F. M. et al. Analysis of the roles of antilipopolysaccharide and anticholera toxin immunoglobulin A (IgA) antibodies in protection against Vibrio cholerae and cholera toxin by use of monoclonal IgA antibodies in vivo. Infect. Immunol. 61 5279-5285 ( 1993 (Pubitemid 23353909)
12. Silvey K. J. Hutchings A. B. Vajdy M. Petzke M. M. & Neutra M. R. Role of immunoglobulin A in protection against reovirus entry into murine Peyer's patches. J. Virol. 75 10870-10879 ( 2001 (Pubitemid 33031555)
13. Helander A. et al. The viral sigma1 protein and glycoconjugates containing alpha2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. J. Virol. 77 7964-7977 ( 2003 (Pubitemid 36792793)
14. Deplancke B. & Gaskins H. R. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr. 73 1131S - 1141S ( 2001 (Pubitemid 32496957)
15. Lievin-Le Moal V. & Servin A. L. The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucinsantimicrobial peptidesand microbiota. Clin. Microbiol. Rev. 19 315-337 ( 2006
16. Mantis N. J. & Forbes S. J. Secretory IgA: arresting microbial pathogens at epithelial borders. Immunol. Invest. 39 383-406 ( 2010
17. Stokes C. R. Soothill J. F. & Turner M. W. Immune exclusion is a function of IgA. Nature 255 745-746 ( 1975
18. Brandtzaeg P. Mucosal immunity: inductiondisseminationand effector functions. Scand. J. Immunol. 70 505-515 ( 2009
19. Forbes S. J. Eschmann M. & Mantis N. J. Inhibition of Salmonella enterica serovar typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immunol. 76 4137-4144 ( 2008
20. Michetti P. Mahan M. J. Slauch J. M. Mekalanos J. J. & Neutra M. R. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immunol. 60 1786-1792 ( 1992
21. Boullier S. et al. Secretory IgA-mediated neutralization of Shigella fl exneri prevents intestinal tissue destruction by down-regulating infl amatory circuits. J. Immunol. 183 5879-5885 ( 2009
22. Phalipon A. et al. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo. Immunity 17 107-115 ( 2002 (Pubitemid 34874623)
23. McGuckin M. A. Linden S. K. Sutton P. & Florin T. H. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9 265-278 ( 2011
24. Kraehenbuhl J. P. & Neutra M. R. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol. Rev. 72 853-879 ( 1992
25. Corthésy B. et al. Rotavirus anti-VP6 secretory immunoglobulin A contributes to protection via intracellular neutralization but not via immune exclusion. J. Virol. 80 10692-10699 ( 2006 (Pubitemid 44628915)
26. Iankov I. D. et al. Protective effi cacy of IgA monoclonal antibodies to O and H antigens in a mouse model of intranasal challenge with Salmonella enterica serotype Enteritidis. Microbes Infect. 6 901-910 ( 2004 (Pubitemid 39061211)
27. Michetti P. et al. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 107 915-923 ( 1994 (Pubitemid 24294552)
28. Forbes S. J. Bumpus T. McCarthy E. A. Corthésy B. & Mantis N. J. Transient suppression of Shigella fl exneri Type 3 secretion by a protective O-antigen-specifi c monoclonal IgA. MBio 2 e00042-11 ( 2011
29. Dallas S. D. & Rolfe R. D. Binding of Clostridium diffi cile toxin A to human milk secretory component. J. Med. Microbiol. 47 879-888 ( 1998 (Pubitemid 28484379)
30. Mantis N. J. Farrant S. A. & Mehta S. Oligosaccharide side chains on human secretory IgA serve as receptors for ricin. J. Immunol. 172 6838-6845 ( 2004 (Pubitemid 38669122)
31. Mestecky J. & Russell M. W. Specifi c antibody activityglycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces. Immunol. Lett. 124 57-62 ( 2009
32. Perrier C. Sprenger N. & Corthésy B. Glycans on secretory component participate in innate protection against mucosal pathogens. J. Biol. Chem. 281 14280-14287 ( 2006 (Pubitemid 43848356)
33. Royle L. et al. Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J. Biol. Chem. 278 20140-20153 ( 2003 (Pubitemid 36799209)
34. Schroten H. et al. Fab-independent antiadhesion effects of secretory immunoglobulin A on S-fi mbriated Escherichia coli are mediated by sialyloligosaccharides. Infect. Immunol. 66 3971-3973 ( 1998 (Pubitemid 28347864)
35. Wold A. E. et al. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fi mbrial lectin. Infect. Immunol. 58 3073-3077 ( 1990 (Pubitemid 20267705)
36. Lu L. Lamm M. E. Li H. Corthésy B. & Zhang J. R. The human polymeric immunoglobulin receptor binds to Streptococcus pneumoniae via domains 3 and 4. J. Biol. Chem. 278 48178-48187 ( 2003 (Pubitemid 37523271)
37. Murthy A. K. et al. Mannose-containing oligosaccharides of non-specifi c human secretory immunoglobulin A mediate inhibition of Vibrio cholerae biofi lm formation. PLoS One 6 e16847 ( 2011
38. Mathias A. & Corthésy B. Recognition of Gram-positive intestinal bacteria by Hybridoma- and Colostrum-derived secretory immunoglobulin a is mediated by carbohydrates. J. Biol. Chem. 286 17239-17247 ( 2011
39. Mathias A. et al. Potentiation of polarized intestinal Caco-2 cell responsiveness to probiotics complexed with secretory IgA. J. Biol. Chem. 285 33906-33913 ( 2010
40. Sekirov I. Russell S. L. Antunes L. C. & Finlay B. B. Gut microbiota in health and disease. Physiol. Rev. 90 859-904 ( 2010
41. Walter J. & Ley R. E. The human gut microbiome: ecology and recent evolutionary changes. Annu. Rev. Microbiol. ( 2011
42. Cebra J. J. Infl uences of microbiota on intestinal immune system development. Am. J. Clin. Nutr. 69 1046S - 1051S ( 1999 (Pubitemid 29205083)
43. Jiang H. Q. et al. Interactions of commensal gut microbes with subsets of B- and T-cells in the murine host. Vaccine 22 805-811 ( 2004
44. Stoel M. et al. Restricted IgA repertoire in both B-1 and B-2 cell-derived gut plasmablasts. J. Immunol. 174 1046-1054 ( 2005 (Pubitemid 40094301)
45. + T cells on intestinal IgA immune responses. Dev. Immunol. 6 53-60 ( 1998 (Pubitemid 28409864)
46. Macpherson A. J. et al. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288 2222-2226 ( 2000 (Pubitemid 30429609)
47. Macpherson A. J. & Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303 1662-1665 ( 2004 (Pubitemid 38338323)
48. Hapfelmeier S. et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 328 1705-1709 ( 2010
49. Fagarasan S. et al. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut fl ora. Science 298 1424-1427 ( 2002 (Pubitemid 35346143)
50. Yel L. Selective IgA defi ciency. J. Clin. Immunol. 30 10-16 ( 2010
51. Meini A. et al. Prevalence and diagnosis of celiac disease in IgA-defi cient children. Ann. Allergy Asthma Immunol. 77 333-336 ( 1996 (Pubitemid 27014591)
52. Janzi M. et al. Selective IgA defi ciency in early life: association to infections and allergic diseases during childhood. Clin. Immunol. 133 78-85 ( 2009
53. Brandtzaeg P. et al. The clinical condition of IgA-defi cient patients is related to the proportion of IgD- and IgM-producing cells in their nasal mucosa. Clin. Exp. Immunol. 67 626-636 ( 1987 (Pubitemid 17031806)
54. Corthésy B. Roundtrip ticket for secretory IgA: role in mucosal homeostasis? J. Immunol. 178 27-32 ( 2007 (Pubitemid 46033584)
55. van der Waaij L. A. Limburg P. C. Mesander G. & van der Waaij D. In vivo IgA coating of anaerobic bacteria in human faeces. Gut 38 348-354 ( 1996 (Pubitemid 26074314)
56. Tsuruta T. et al. The amount of secreted IgA may not determine the secretory IgA coating ratio of gastrointestinal bacteria. FEMS Immunol. Med. Microbiol. 56 185-189 ( 2009
57. Peterson D. A. McNulty N. P. Guruge J. L. & Gordon J. I. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2 328-339 ( 2007 (Pubitemid 350056397)
58. Zitomersky N. L. Coyne M. J. & Comstock L. E. Longitudinal analysis of the prevalencemaintenanceand IgA response to species of the order bacteroidales in the human gut. Infect. Immunol. 79 2012-2020 ( 2011
59. Friman V. et al. Decreased expression of mannose-specifi c adhesins by Escherichia coli in the colonic microfl ora of immunoglobulin A-defi cient individuals. Infect. Immunol. 64 2794-2798 ( 1996 (Pubitemid 26226848)
60. Bollinger R. R. et al. Human secretory immunoglobulin A may contribute to biofi lm formation in the gut. Immunology 109 580-587 ( 2003
61. Bollinger R. R. et al. Secretory IgA and mucin-mediated biofi lm formation by environmental strains of Escherichia coli: role of type 1 pili. Mol. Immunol. 43 378-387 ( 2006 (Pubitemid 41668846)
62. Costerton J. W. Lewandowski Z. Caldwell D. E. Korber D. R. & Lappin- Scott H. M. Microbial biofi lms. Annu. Rev. Microbiol. 49 711-745 ( 1995
63. Palestrant D. et al. Microbial biofi lms in the gut: visualization by electron microscopy and by acridine orange staining. Ultrastruct. Pathol. 28 23-27 ( 2004 (Pubitemid 38299721)
64. Lebeer S. Claes I. J. Verhoeven T. L. Vanderleyden J. & De Keersmaecker S. C. Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb. Biotechnol. 4 368-374 ( 2011
65. Mantis N. J. et al. Selective adherence of IgA to murine Peyer's patch M cells: evidence for a novel IgA receptor. J. Immunol. 169 1844-1851 ( 2002 (Pubitemid 34857646)
66. Weltzin R. et al. Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral proteins. J. Cell Biol. 108 1673-1685 ( 1989 (Pubitemid 19130500)
67. Duc M. Johansen F. E. & Corthésy B. Antigen binding to secretory immunoglobulin A results in decreased sensitivity to intestinal proteases and increased binding to cellular Fc receptors. J. Biol. Chem. 285 953 - 960 ( 2010
68. Favre L. Spertini F. & Corthésy B. Secretory IgA possesses intrinsic modulatory properties stimulating mucosal and systemic immune responses. J. Immunol. 175 2793-2800 ( 2005 (Pubitemid 41170495)
69. Sansonetti P. J. Arondel J. Cantey J. R. Prevost M. C. & Huerre M. Infection of rabbit Peyer's patches by Shigella fl exneri: effect of adhesive or invasive bacterial phenotypes on follicle-associated epithelium. Infect. Immunol. 64 2752-2764 ( 1996 (Pubitemid 26226843)
70. Smits H. H. et al. Cholera toxin B suppresses allergic infl ammation trough induction of secretory IgA. Mucosal Immunol. 2 331-339 ( 2009
71. Schwarze J. et al. Antigen-specifi c immunoglobulin-A prevents increased airway responsiveness and lung eosinophilia after airway challenge in sensitized mice. Am. J. Respir. Crit. Care Med. 158 519-525 ( 1998 (Pubitemid 28378182)
72. Heikkinen T. et al. Intranasally administered immunoglobulin for the prevention of rhinitis in children. Pediatr. Infect. Dis. J. 17 367-372 ( 1998 (Pubitemid 28232857)
73. Bottcher M. F. Haggstrom P. Bjorksten B. & Jenmalm M. C. Total and allergen-specifi c immunoglobulin A levels in saliva in relation to the development of allergy in infants up to 2 years of age. Clin. Exp. Allergy 32 1293-1298 ( 2002 (Pubitemid 35024954)
74. Frossard C. P. Hauser C. & Eigenmann P. A. Antigen-specifi c secretory IgA antibodies in the gut are decreased in a mouse model of food allergy. J. Allergy Clin. Immunol. 114 377-382 ( 2004 (Pubitemid 39119040)
75. Mosconi E. et al. Breast milk immune complexes are potent inducers of oral tolerance in neonates and prevent asthma development. Mucosal Immunol. 3 461-474 ( 2010
76. Johansen F. E. et al. Absence of epithelial immunoglobulin A transportwith increased mucosal leakinessin polymeric immunoglobulin receptor/ secretory component-defi cient mice. J. Exp. Med. 190 915-922 ( 1999
77. Sait L. C. et al. Secretory antibodies reduce systemic antibody responses against the gastrointestinal commensal fl ora. Int. Immunol. 19 257-265 ( 2007 (Pubitemid 46344690)
78. Karlsson M. R. Johansen F. E. Kahu H. Macpherson A. & Brandtzaeg P. Hypersensitivity and oral tolerance in the absence of a secretory immune system. Allergy 65 561-570 ( 2010
79. Pilette C. et al. Grass pollen immunotherapy induces an allergen-specifi c IgA2 antibody response associated with mucosal TGF-beta expression. J. Immunol. 178 4658-4666 ( 2007 (Pubitemid 46492419)
80. Pasquier B. et al. Identifi cation of FcalphaRI as an inhibitory receptor that controls infl ammation: dual role of FcRgamma ITAM. Immunity 22 31-42 ( 2005 (Pubitemid 40143449)
81. Roth-Walter F. et al. Pasteurization of milk proteins promotes allergic sensitization by enhancing uptake through Peyer's patches. Allergy 63 882-890 ( 2008 (Pubitemid 351832791)
82. Perrier C. Thierry A. C. Mercenier A. & Corthésy B. Allergen-specifi c antibody and cytokine responsesmast cell reactivity and intestinal permeability upon oral challenge of sensitized and tolerized mice. Clin. Exp. Allergy 40 153-162 ( 2010
83. Aghamohammadi A. et al. IgA defi ciency: correlation between clinical and immunological phenotypes. J. Clin. Immunol. 29 130-136 ( 2009
84. Matysiak-Budnik T. et al. Secretory IgA mediates retrotranscytosis of intact gliadin peptides via the transferrin receptor in celiac disease. J. Exp. Med. 205 143-154 ( 2008 (Pubitemid 351185722)
85. Rey J. Garin N. Spertini F. & Corthésy B. Targeting of secretory IgA to Peyer's patch dendritic and T cells after transport by intestinal M cells. J Immunol. 172 3026-3033 ( 2004 (Pubitemid 38263691)
86. Heystek H. C. Moulon C. Woltman A. M. Garonne P. & van Kooten C. Human immature dendritic cells effi ciently bind and take up secretory IgA without the induction of maturation. J. Immunol. 168 102-107 ( 2002 (Pubitemid 34014108)
87. Baumann J. Park C. G. & Mantis N. J. Recognition of secretory IgA by DC-SIGN: implications for immune surveillance in the intestine. Immunol. Lett. 131 59-66 ( 2010
88. Jameson B. et al. Expression of DC-SIGN by dendritic cells of intestinal and genital mucosae in humans and rhesus macaques. J. Virol. 76 1866-1875 ( 2002 (Pubitemid 34094633)
89. Galustian C. et al. High and low affi nity carbohydrate ligands revealed for murine SIGN-R1 by carbohydrate array and cell binding approachesand differing specifi cities for SIGN-R3 and langerin. Int. Immunol. 16 853-866 ( 2004 (Pubitemid 38786526)
90. Zhou Y. et al. Oral tolerance to food-induced systemic anaphylaxis mediated by the C-type lectin SIGNR1. Nat. Med. 16 1128-1133 ( 2010
91. Kadaoui K. A. & Corthésy B. Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer's patches with restriction to mucosal compartment. J. Immunol. 179 7751-7757 ( 2007