Salmonella regulates polyubiquitination and surface expression of MHC class II antigens

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 33, 2009, Pages 14052-14057

  Lapaque, Nicolas ^a   Hutchinson, James L ^a   Jones, Des C ^a   Méresse, Stéphane ^b   Holden, David W ^c   Trowsdale, John ^a   Kelly, Adrian P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CNRS   (France)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HLA DP ANTIGEN; HLA DQ ANTIGEN; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ARTICLE; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SALMONELLA; SALMONELLOSIS; UBIQUITINATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CELL MEMBRANE; CELL SEPARATION; CYTOPLASM; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; SALMONELLA; SALMONELLA INFECTIONS; UBIQUITIN;

SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 69549126588     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906735106     Document Type: Article

References (35)

1. Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bull World Health Organ 82:346-353.
2. Hess J, Ladel C, Miko D, Kaufmann SH (1996) Salmonella typhimurium aroA- infection in gene-targeted immunodeficient mice: major role of CD4+ TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J Immunol 156:3321-3326. (Pubitemid 26123548)
3. Dunstan SJ, et al. (2001) Genes of the class II and class III major histocompatibility complex are associated with typhoid fever in Vietnam. J Infect Dis 183:261-268. (Pubitemid 32066028)
4. Cheminay C, Mohlenbrink A, Hensel M (2005) Intracellular Salmonella inhibit antigen presentation by dendritic cells. J Immunol 174:2892-2899. (Pubitemid 40279707)
5. Bryant PW, Lennon-Dumenil AM, Fiebiger E, Lagaudriere-Gesbert C, Ploegh HL (2002) Proteolysis and antigen presentation by MHC class II molecules. Adv Immunol 80:71-114. (Pubitemid 34625621)
6. Cresswell P (1994) Assembly, transport, and function of MHC class II molecules. Annu Rev Immunol 12:259-293. (Pubitemid 24140416)
7. Bakke O, Dobberstein B (1990) MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63:707-716. (Pubitemid 120035044)
8. Watts C (2004) The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat Immunol 5:685-692. (Pubitemid 39023297)
9. Hiltbold EM, Roche PA (2002) Trafficking of MHC class II molecules in the late secretory pathway. Curr Opin Immunol 14:30-35.
10. McCormick PJ, Martina JA, Bonifacino JS (2005) Involvement of clathrin and AP-2 in the trafficking of MHC class II molecules to antigen-processing compartments. Proc Natl Acad Sci USA 102:7910-7915.
11. Cresswell P (1992) Chemistry and functional role of the invariant chain. Curr Opin Immunol 4:87-92.
12. Denzin LK, Cresswell P (1995) HLA-DM induces CLIP dissociation fromMHCclass II alpha beta dimers and facilitates peptide loading. Cell 82:155-165.
13. Denzin LK, Sant'Angelo DB, Hammond C, Surman MJ, Cresswell P (1997) Negative regulation by HLA-DO of MHC class II-restricted antigen processing. Science 278:106-109. (Pubitemid 27446286)
14. Brodsky FM, Lem L, Solache A, Bennett EM (1999) Human pathogen subversion of antigen presentation. Immunol Rev 168:199-215. (Pubitemid 29276684)
15. Shin JS, Ebersold M, Pypaert M, Delamarre L, Hartley A, Mellman I (2006) Surface expression of MHC class II in dendritic cells is controlled by regulated ubiquitination. Nature 444:115-118. (Pubitemid 44684767)
16. van Niel G, et al. (2006) Dendritic cells regulate exposure of MHC class II at their plasma membrane by oligoubiquitination. Immunity 25:885-894. (Pubitemid 44894949)
17. Goto E, et al. (2003) c-MIR, a human E3 ubiquitin ligase, is a functional homolog of herpesvirus proteins MIR1 and MIR2 and has similar activity. J Biol Chem 278:14657-14668. (Pubitemid 36799788)
18. Mitchell EK, Mastroeni P, Kelly AP, Trowsdale J (2004) Inhibition of cell surface MHC class II expression by Salmonella. Eur J Immunol 34:2559-2567. (Pubitemid 39302813)
19. Roche PA, Cresswell P (1991) Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc Natl Acad Sci USA 88:3150-3154.
20. Stumptner-Cuvelette P, et al. (2001) HIV-1 Nef impairs MHC class II antigen presentation and surface expression. Proc Natl Acad Sci USA 98:12144-12149. (Pubitemid 32959841)
21. Dugast M, Toussaint H, Dousset C, Benaroch P (2005) AP2 clathrin adaptor complex, but not AP1, controls the access of the major histocompatibility complex (MHC) class II to endosomes. J Biol Chem 280:19656-19664. (Pubitemid 41379489)
22. Lapaque N, Jahnke M, Trowsdale J, Kelly AP (2009) The HLA-DRalpha chain is modified by poly-ubiquitination. J Biol Chem 284:7007-7016.
23. Ohmura-Hoshino M, et al. (2006) Inhibition of MHC class II expression and immune responses by c-MIR. J Immunol 177:341-354. (Pubitemid 43939146)
24. Matsuki Y, et al. (2007) Novel regulation of MHC class II function in B cells. EMBO J 26:846-854. (Pubitemid 46253856)
25. De Gassart A, et al. (2008) MHC class II stabilization at the surface of human dendritic cells is the result of maturation-dependent MARCH I down-regulation. Proc Natl Acad Sci USA 105:3491-3496. (Pubitemid 351723580)
26. Zhang Y, Higashide WM, McCormick BA, Chen J, Zhou D (2006) The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol Microbiol 62:786-793. (Pubitemid 44571602)
27. Rytkonen A, et al. (2007) SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci USA 104:3502-3507 (Pubitemid 46364188)
28. Quezada CM, Hicks SW, Galan JE, Stebbins CE (2009) A family of Salmonella virulence factors functions as a distinct class of autoregulated E3 ubiquitin ligases. Proc Natl Acad Sci USA 106:4864-4869.
29. Zhou H, et al. (2005) Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 202:1327-1332. (Pubitemid 41668735)
30. Misaghi S, Balsara ZR, Catic A, Spooner E, Ploegh HL, Starnbach MN (2006) Chlamydia trachomatis-derived deubiquitinating enzymes in mammalian cells during infection. Mol Microbiol 61:142-150. (Pubitemid 43911504)
31. Walseng E, Bakke O, Roche PA (2008) Major histocompatibility complex class II-peptide complexes internalize using a clathrin- and dynamin-independent endocytosis pathway. J Biol Chem 283:14717-14727.
32. Pinet V, Vergelli M, Martin R, Bakke O, Long EO (1995) Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature 375:603-606.
33. Zhong G, Romagnoli P, Germain RN (1997) Related leucine-based cytoplasmic targeting signals in invariant chain and major histocompatibility complex class II molecules control endocytic presentation of distinct determinants in a single protein. J Exp Med 185:429-438. (Pubitemid 27078361)
34. Boyer L, Lemichez E (2004) Targeting of host-cell ubiquitin and ubiquitin-like pathways by bacterial factors. Nat Rev Microbiol 2:779-788. (Pubitemid 39317459)
35. Neish AS, et al. (2000) Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 289:1560-1563.