MHCII glycosylation modulates Bacteroides fragilis carbohydrate antigen presentation

Journal of Experimental Medicine

Volumn 208, Issue 5, 2011, Pages 1041-1053

  Ryan, Sean O ^a   Bonomo, Jason A ^a   Zhao, Fan ^a   Cobb, Brian A ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE ANTIGEN; KIFUNENSINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL EXPERIMENT; ANTIGEN BINDING; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; BACTEROIDES FRAGILIS; CONTROLLED STUDY; FEMALE; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ALKALOIDS; ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS, BACTERIAL; BACTEROIDES FRAGILIS; GLYCOSYLATION; HEK293 CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LYMPHOCYTE ACTIVATION; MANNOSIDASES; MICE; POLYSACCHARIDES, BACTERIAL; T-LYMPHOCYTES;

EID: 79956111813     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20100508     Document Type: Article

References (45)

1. Altmann, F., E. Staudacher, I.B. Wilson, and L. März. 1999. Insect cells as hosts for the expression of recombinant glycoproteins. Glycoconj. J. 16:109-123.
2. Barrera, C., R. Espejo, and V.E. Reyes. 2002. Differential glycosylation of MHC class II molecules on gastric epithelial cells: implications in local immune responses. Hum. Immunol. 63:384-393.
3. Bergeron, J.J., A. Zapun, W.J. Ou, R. Hemming, F. Parlati, P.H. Cameron, and D.Y. Thomas. 1998. The role of the lectin calnexin in conformation independent binding to N-linked glycoproteins and quality control. Adv. Exp. Med. Biol. 435:105-116.
4. Bodger, K., J. Halfvarson, A.R. Dodson, F. Campbell, S. Wilson, R. Lee, E. Lindberg, G. Järnerot, C. Tysk, and J.M. Rhodes. 2006. Altered colonic glycoprotein expression in unaffected monozygotic twins of inflammatory bowel disease patients. Gut. 55:973-977.
5. Brown, J.H., T.S. Jardetzky, L.J. Stern, J.C. Gorga, J.L. Strominger, and D.C. Wiley. 1995. Human class II MHC molecule HLA-DR1: X-ray structure determined from three crystal forms. Acta Crystallogr. D Biol. Crystallogr. 51:946-961.
6. Brown, S.J., A.M. Miller, P.J. Cowan, J. Slavin, W.R. Connell, G.T. Moore, S. Bell, P.R. Elliott, P.V. Desmond, and A.J. d'Apice. 2004. Altered immune system glycosylation causes colitis in alpha1,2-fucosyltransferase transgenic mice. Inflamm. Bowel Dis. 10:546-556.
7. Brubaker, J.O., Q. Li, A.O. Tzianabos, D.L. Kasper, and R.W. Finberg. 1999. Mitogenic activity of purified capsular polysaccharide A from Bacteroides fragilis: differential stimulatory effect on mouse and rat lymphocytes in vitro. J. Immunol. 162:2235-2242.
8. Campbell, B.J., L.G. Yu, and J.M. Rhodes. 2001. Altered glycosylation in inflammatory bowel disease: a possible role in cancer development. Glycoconj. J. 18:851-858.
9. Choi, Y.H., M.H. Roehrl, D.L. Kasper, and J.Y. Wang. 2002. A unique structural pattern shared by T-cell-activating and abscess-regulating zwitterionic polysaccharides. Biochemistry. 41:15144-15151.
10. Cobb, B.A., and D.L. Kasper. 2008. Characteristics of carbohydrate antigen binding to the presentation protein HLA-DR. Glycobiology. 18:707-718.
11. Cobb, B.A., Q. Wang, A.O. Tzianabos, and D.L. Kasper. 2004. Polysaccharide processing and presentation by the MHCII pathway. Cell. 117:677-687.
12. Dustin, M.L., L.M. Ferguson, P.Y. Chan, T.A. Springer, and D.E. Golan. 1996. Visualization of CD2 interaction with LFA-3 and determination of the two-dimensional dissociation constant for adhesion receptors in a contact area. J. Cell Biol. 132:465-474.
13. Dustin, M.L., D.E. Golan, D.M. Zhu, J.M. Miller, W. Meier, E.A. Davies, and P.A. van der Merwe. 1997. Low affinity interaction of human or rat T cell adhesion molecule CD2 with its ligand aligns adhering membranes to achieve high physiological affinity. J. Biol. Chem. 272:30889-30898.
14. Frayser, M., A.K. Sato, L. Xu, and L.J. Stern. 1999. Empty and peptide-loaded class II major histocompatibility complex proteins produced by expression in Escherichia coli and folding in vitro. Protein Expr. Purif. 15:105-114.
15. Gauthier, L., K.J. Smith, J. Pyrdol, A. Kalandadze, J.L. Strominger, D.C. Wiley, and K.W. Wucherpfennig. 1998. Expression and crystallization of the complex of HLA-DR2 (DRA, DRB1*1501) and an immunodominant peptide of human myelin basic protein. Proc. Natl. Acad. Sci. USA. 95:11828-11833.
16. Guerra, C.B., R. Busch, R.C. Doebele, W. Liu, T. Sawada, W.W. Kwok, M.D. Chang, and E.D. Mellins. 1998. Novel glycosylation of HLA-DRalpha disrupts antigen presentation without altering endosomal localization. J. Immunol. 160:4289-4297.
17. Hart, G.W. 1982. The role of asparagine-linked oligosaccharides in cellular recognition by thymic lymphocytes. Effects of tunicamycin on the mixed lymphocyte reaction. J. Biol. Chem. 257:151-158.
18. Ishikawa, S., C. Kowal, B. Cole, C. Thomson, and B. Diamond. 1995. Replacement of N-glycosylation sites on the MHC class II E alpha chain. Effect on thymic selection and peripheral T cell activation. J. Immunol. 154: 5023-5029.
19. Kreisman, L.S., J.H. Friedman, A. Neaga, and B.A. Cobb. 2007. Structure and function relations with a T-cell-activating polysaccharide antigen using circular dichroism. Glycobiology. 17:46-55.
20. Krinos, C.M., M.J. Coyne, K.G. Weinacht, A.O. Tzianabos, D.L. Kasper, and L.E. Comstock. 2001. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature. 414:555-558.
21. Lewis, C.J., and B.A. Cobb. 2010. Carbohydrate oxidation acidifies endosomes, regulating antigen processing and TLR9 signaling. J. Immunol. 184:3789-3800.
22. Li, Y., H. Li, R. Martin, and R.A. Mariuzza. 2000. Structural basis for the binding of an immunodominant peptide from myelin basic protein in different registers by two HLA-DR2 proteins. J. Mol. Biol. 304:177-188.
23. Li, Y., H. Li, N. Dimasi, J.K. McCormick, R. Martin, P. Schuck, P.M. Schlievert, and R.A. Mariuzza. 2001. Crystal structure of a superantigen bound to the high-affinity, zinc-dependent site on MHC class II. Immunity. 14:93- 104.
24. Matsuda, T., and C.L. Cepko. 2007. Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA. 104:1027-1032.
25. Mazmanian, S.K., C.H. Liu, A.O. Tzianabos, and D.L. Kasper. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 122:107-118.
26. Mazmanian, S.K., J.L. Round, and D.L. Kasper. 2008. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 453:620-625.
27. Néel, D., B. Merlu, E. Turpin, C. Rabourdin-Combe, B. Mach, Y. Goussault, and D.J. Charron. 1987. Characterization of N-linked oligosaccharides of an HLA-DR molecule expressed in different cell lines. Biochem. J. 244:433-442.
28. Paulson, J.C., O. Blixt, and B.E. Collins. 2006. Sweet spots in functional glycomics. Nat. Chem. Biol. 2:238-248.
29. Rudd, P.M., M.R. Wormald, R.L. Stanfield, M. Huang, N. Mattsson, J.A. Speir, J.A. DiGennaro, J.S. Fetrow, R.A. Dwek, and I.A. Wilson. 1999. Roles for glycosylation of cell surface receptors involved in cellular immune recognition. J. Mol. Biol. 293:351-366.
30. Rudd, P.M., T. Elliott, P. Cresswell, I.A. Wilson, and R.A. Dwek. 2001. Glycosylation and the immune system. Science. 291:2370-2376.
31. Saito, Y., Y. Ihara, M.R. Leach, M.F. Cohen-Doyle, and D.B. Williams. 1999. Calreticulin functions in vitro as a molecular chaperone for both glycosylated and non-glycosylated proteins. EMBO J. 18:6718-6729.
32. Stephen, T.L., M. Niemeyer, A.O. Tzianabos, M. Kroenke, D.L. Kasper, and W.M. Kalka-Moll. 2005. Effect of B7-2 and CD40 signals from activated antigen-presenting cells on the ability of zwitterionic polysaccharides to induce T-Cell stimulation. Infect. Immun. 73:2184-2189.
33. Stingele, F., B. Corthésy, N. Kusy, S.A. Porcelli, D.L. Kasper, and A.O. Tzianabos. 2004. Zwitterionic polysaccharides stimulate T cells with no preferential V beta usage and promote anergy, resulting in protection against experimental abscess formation. J. Immunol. 172:1483-1490.
34. Trombetta, E.S., and A. Helenius. 1998. Lectins as chaperones in glycoprotein folding. Curr. Opin. Struct. Biol. 8:587-592.
35. Tzianabos, A.O., A. Pantosti, H. Baumann, J.R. Brisson, H.J. Jennings, and D.L. Kasper. 1992. The capsular polysaccharide of Bacteroides fragilis comprises two ionically linked polysaccharides. J. Biol. Chem. 267: 18230-18235.
36. Tzianabos, A.O., A.B. Onderdonk, B. Rosner, R.L. Cisneros, and D.L. Kasper. 1993. Structural features of polysaccharides that induce intraabdominal abscesses. Science. 262:416-419.
37. Tzianabos, A.O., D.L. Kasper, and A.B. Onderdonk. 1995. Structure and function of Bacteroides fragilis capsular polysaccharides: relationship to induction and prevention of abscesses. Clin. Infect. Dis. 20:S132-S140.
38. Tzianabos, A.O., J.Y. Wang, and J.C. Lee. 2001. Structural rationale for the modulation of abscess formation by Staphylococcus aureus capsular polysaccharides. Proc. Natl. Acad. Sci. USA. 98:9365-9370.
39. Velez, C.D., C.J. Lewis, D.L. Kasper, and B.A. Cobb. 2009. Type I Streptococcus pneumoniae carbohydrate utilizes a nitric oxide and MHC II-dependent pathway for antigen presentation. Immunology. 127:73-82.
40. von Gunten, S., D.F. Smith, R.D. Cummings, S. Riedel, S. Miescher, A. Schaub, R.G. Hamilton, and B.S. Bochner. 2009. Intravenous immunoglobulin contains a broad repertoire of anticarbohydrate antibodies that is not restricted to the IgG2 subclass. J. Allergy Clin. Immunol. 123:1268- 1276: e15.
41. Wang, Y., W.M. Kalka-Moll, M.H. Roehrl, and D.L. Kasper. 2000. Structural basis of the abscess-modulating polysaccharide A2 from Bacteroides fragilis. Proc. Natl. Acad. Sci. USA. 97:13478-13483.
42. Wang, Y., J. Tan, M. Sutton-Smith, D. Ditto, M. Panico, R.M. Campbell, N.M. Varki, J.M. Long, J. Jaeken, S.R. Levinson, et al. 2001. Modeling human congenital disorder of glycosylation type IIa in the mouse: conservation of asparagine-linked glycan-dependent functions in mammalian physiology and insights into disease pathogenesis. Glycobiology. 11:1051-1070.
43. Wang, Q., R.M. McLoughlin, B.A. Cobb, M. Charrel-Dennis, K.J. Zaleski, D. Golenbock, A.O. Tzianabos, and D.L. Kasper. 2006. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J. Exp. Med. 203:2853-2863.
44. Wiman, K., L. Claesson, L. Rask, L. Trägårdh, and P.A. Peterson. 1982. Purification and partial amino acid sequence of papain-solubilized class II transplantation antigens. Biochemistry. 21:5351-5358.
45. Wormald, M.R., and R.A. Dwek. 1999. Glycoproteins: glycan presentation and protein-fold stability. Structure. 7:R155-R160.