Mannan-binding lectin deficiency results in unusual antibody production and excessive experimental colitis in response to mannose-expressing mild gut pathogens

Gut

Volumn 59, Issue 11, 2010, Pages 1493-1500

  Müller, Stefan ^a   Schaffer, Thomas ^a   Flogerzi, Beatrice ^a   Seibold Schmid, Beatrice ^a   Schnider, Jasmin ^a   Takahashi, Kazue ^b   Darfeuille Michaud, Arlette ^c   Vazeille, Emilie ^c   Schoepfer, Alain M ^a,d   Seibold, Frank ^a,e  

^a UNIVERSITY OF BERN   (Switzerland)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

^d MCMASTER UNIVERSITY   (Canada)

^e UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; EPITOPE; FUNGUS ANTIBODY; IMMUNOGLOBULIN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; MANNAN BINDING LECTIN; MANNOSE; MANNOSE BINDING LECTIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CANDIDA ALBICANS; COLITIS; CONTROLLED STUDY; CROHN DISEASE; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; INFLAMMATION; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE INJURY; INTESTINE MUCOSA; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RISK REDUCTION; SACCHAROMYCES CEREVISIAE; WILD TYPE; ADOLESCENT; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CANDIDIASIS; IMMUNOLOGY; INNATE IMMUNITY; ISOLATION AND PURIFICATION; KIDNEY; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MOUSE MUTANT; MUCOSAL IMMUNITY; PATHOGENICITY; ULCERATIVE COLITIS;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODIES, FUNGAL; CANDIDA ALBICANS; CANDIDIASIS; COLITIS; COLITIS, ULCERATIVE; CROHN DISEASE; ESCHERICHIA COLI; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; KIDNEY; MANNOSE; MANNOSE-BINDING LECTIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; PHENOTYPE; SACCHAROMYCES CEREVISIAE; YOUNG ADULT;

EID: 78049515838     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gut.2010.208348     Document Type: Article

References (48)

1. Duchmann R, Kaiser I, Hermann E, et al. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol 1995;102:448-55.
2. Landers CJ, Cohavy O, Misra R, et al. Selected loss of tolerance evidenced by Crohn's disease-associated immune responses to auto- and microbial antigens. Gastroenterology 2002;123:689-99.
3. Sartor RB. Bacteria in Crohn's disease: mechanisms of inflammation and therapeutic implications. J Clin Gastroenterol 2007;41:S37-43.
4. Sutton CL, Kim J, Yamane A, et al. Identification of a novel bacterial sequence associated with Crohn's disease. Gastroenterology 2000;119:23-31.
5. Main J, McKenzie H, Yeaman GR, et al. Antibody to Saccharomyces cerevisiae (bakers' yeast) in Crohn's disease. BMJ 1988;297:1105-6.
6. Seibold F, Stich O, Hufnagl R, et al. Anti-Saccharomyces cerevisiae antibodies in inflammatory bowel disease: a family study. Scand J Gastroenterol 2001;36:196-201.
7. Konrad A, Rutten C, Flogerzi B, et al. Immune sensitization to yeast antigens in ASCA-positive patients with Crohn's disease. Inflamm Bowel Dis 2004;10:97-105.
8. Standaert-Vitse A, Jouault T, Vandewalle P, et al. Candida albicans is an immunogen for anti-Saccharomyces cerevisiae antibody markers of Crohn's disease. Gastroenterology 2006;130:1764-75.
9. Schaffer T, Müller S, Flogerzi B, et al. Anti-Saccharomyces cerevisiae mannan antibodies (ASCA) of Crohn's patients crossreact with mannan from other yeast strains, and murine ASCA IgM can be experimentally induced with Candida albicans. Inflamm Bowel Dis 2007;13:1339-46.
10. Müller S, Schaffer T, Schoepfer AM, et al. Partial overlap of anti-mycobacterial, and anti-Saccharomyces cerevisiae mannan antibodies in Crohn's disease. World J Gastroenterol 2008;14:3650-61.
11. Sendid B, Colombel JF, Jacquinot PM, et al. Specific antibody response to oligomannosidic epitopes in Crohn's disease. Clin Diagn Lab Immunol 1996;3:219-26.
12. Young M, Davies MJ, Bailey D, et al. Characterization of oligosaccharides from an antigenic mannan of Saccharomyces cerevisiae. Glycoconj J 1998;15:815-22.
13. Ballou CE, Lipke PN, Raschke WC. Structure and immunochemistry of the cell wall mannans from Saccharomyces chevalieri, Saccharomyces italicus, Saccharomyces diastaticus, and Saccharomyces carlsbergensis. J Bacteriol 1974;117:461-7.
14. Dommett RM, Klein N, Turner MW. Mannose-binding lectin in innate immunity: past, present and future. Tissue Antigens 2006;68:193-209.
15. Takahashi K, Ezekowitz RA. The role of the mannose-binding lectin in innate immunity. Clin Infect Dis 2005;41(Suppl 7):S440-4.
16. Takahashi K, Ip WE, Michelow IC, et al. The mannose-binding lectin: a prototypic pattern recognition molecule. Curr Opin Immunol 2006;18:16-23.
17. Thiel S. Complement activating soluble pattern recognition molecules with collagen-like regions, mannan-binding lectin, ficolins and associated proteins. Mol Immunol 2007;44:3875-88.
18. Jack DL, Turner MW. Anti-microbial activities of mannose-binding lectin. Biochem Soc Trans 2003;31:753-7.
19. Shi L, Takahashi K, Dundee J, et al. Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J Exp Med 2004;199:1379-90.
20. Ip WK, Takahashi K, Moore KJ, et al. Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J Exp Med 2008;205:169-81.
21. Turner MW. Mannose-binding lectin (MBL) in health and disease. Immunobiology 1998;199:327-39.
22. Bouwman LH, Roep BO, Roos A. Mannose-binding lectin: clinical implications for infection, transplantation, and autoimmunity. Hum Immunol 2006;67:247-56.
23. Thiel S, Frederiksen PD, Jensenius JC. Clinical manifestations of mannan-binding lectin deficiency. Mol Immunol 2006;43:86-96.
24. Møller-Kristensen M, Ip WK, Shi L, et al. Deficiency of mannose-binding lectin greatly increases susceptibility to postburn infection with Pseudomonas aeruginosa. J Immunol 2006;176:1769-75.
25. Gadjeva M, Paludan SR, Thiel S, et al. Mannan-binding lectin modulates the response to HSV-2 infection. Clin Exp Immunol 2004;138:304-11.
26. Guttormsen HK, Stuart LM, Shi L, et al. Deficiency of mannose-binding lectin greatly increases antibody response in a mouse model of vaccination. Clin Immunol 2009;130:264-71.
27. Ruseva M, Kolev M, Dagnaes-Hansen F, et al. Mannan-binding lectin deficiency modulates the humoral immune response dependent on the genetic environment. Immunology 2009;127:279-88.
28. Seibold F, Boldt AB, Seibold-Schmid B, et al. Deficiency for mannan-binding lectin is associated with antibodies to Saccharomyces cerevisiae in patients with Crohn's disease and their relatives. Gut 2007;56:152.
29. Seibold F, Konrad A, Flogerzi B, et al. Genetic variants of the mannan-binding lectin are associated with immune reactivity to mannans in Crohn's disease. Gastroenterology 2004;127:1076-84.
30. Schoepfer AM, Flogerzi B, Seibold-Schmid B, et al. Low mannan-binding lectin serum levels are associated with complicated Crohn's disease and reactivity to oligomannan (ASCA). Am J Gastroenterol 2009;104:2508-16.
31. Kuhlman M, Joiner K, Ezekowitz RA. The human mannose-binding protein functions as an opsonin. J Exp Med 1989;169:1733-45.
32. Martin HM, Campbell BJ, Hart CA, et al. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 2004;127:80-93.
33. Rolhion N, Darfeuille-Michaud A. Adherent-invasive Escherichia coli in inflammatory bowel disease. Inflamm Bowel Dis 2007;13:1277-83.
34. Boudeau J, Glasser AL, Masseret E, et al. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 1999;67:4499-509.
35. Müller S, Styner M, Seibold-Schmid B, et al. Anti-Saccharomyces cerevisiae antibody titers are stable over time in Crohn's patients and are not inducible in murine models of colitis. World J Gastroenterol 2005;11:6988-94.
36. Møller-Kristensen M, Hamblin MR, Thiel S, et al. Burn injury reveals altered phenotype in mannan-binding lectin-deficient mice. J Invest Dermatol 2007;127:1524-31.
37. Konrad A, Mahler M, Arni S, et al. Ameliorative effect of IDS 30, a stinging nettle leaf extract, on chronic colitis. Int J Colorectal Dis 2005;20:9-17.
38. Seyfarth J, Garred P, Madsen HO. Extra-hepatic transcription of the human mannose-binding lectin gene (mbl2) and the MBL-associated serine protease 1-3 genes. Mol Immunol 2006;43:962-71.
39. Darfeuille-Michaud A, Neut C, Barnich N, et al. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 1998;115:1405-13.
40. Slack E, Hapfelmeier S, Stecher B, et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 2009;325:617-20.
41. Schweinle JE, Ezekowitz RA, Tenner AJ, et al. Human mannose-binding protein activates the alternative complement pathway and enhances serum bactericidal activity on a mannose-rich isolate of Salmonella. J Clin Invest 1989;84:1821-9.
42. van Emmerik LC, Kuijper EJ, Fijen CA, et al. Binding of mannan-binding protein to various bacterial pathogens of meningitis. Clin Exp Immunol 1994;97:411-16.
43. Jawhara S, Thuru X, Standaert-Vitse A, et al. Colonization of mice by Candida albicans is promoted by chemically induced colitis and augments inflammatory responses through galectin-3. J Infect Dis 2008;197:972-80.
44. Faux JA, Agbarakwe AE, Misbah SA, et al. A comparison of specific IgG antibody levels to the cell wall mannan of Candida albicans in normal individuals and in patients with primary antibody deficiency. J Immunol Methods 1992;153:167-72.
45. Held K, Thiel S, Loos M, et al. Increased susceptibility of complement factor B/C2 double knockout mice and mannan-binding lectin knockout mice to systemic infection with Candida albicans. Mol Immunol 2008;45:3934-41.
46. Lillegard JB, Sim RB, Thorkildson P, et al. Recognition of Candida albicans by mannan-binding lectin in vitro and in vivo. J Infect Dis 2006;193:1589-97.
47. Brouwer N, Dolman KM, van Houdt M, et al. Mannose-binding lectin (MBL) facilitates opsonophagocytosis of yeasts but not of bacteria despite MBL binding. J Immunol 2008;180:4124-32.
48. Tahara T, Shibata T, Wang FY, et al. Mannan-binding lectin B allele is associated with a risk of developing more severe gastric mucosal atrophy in Helicobacter pylori-infected Japanese patients. Eur J Gastroenterol Hepatol 2009;21:781-6.