Proinflammatory bacterial peptidoglycan as a cofactor for the development of central nervous system autoimmune disease

Journal of Immunology

Volumn 174, Issue 2, 2005, Pages 808-816

  Visser, Lizette ^a   De Heer, Hendrik Jan ^a   Boven, Leonie A ^a   Van Riel, Debby ^a   Van Meurs, Marjan ^a   Melief, Marie José ^a   Zähringer, Ulrich ^c   Van Strijp, Jos ^b   Lambrecht, Bart N ^a   Nieuwenhuis, Edward E ^a   Laman, Jon D ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c RESEARCH CENTER BORSTEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CYTOKINE; FREUND ADJUVANT; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDOGLYCAN; TOLL LIKE RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; LYMPH NODE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STIMULUS RESPONSE; T LYMPHOCYTE; TH1 CELL;

EID: 19944427519     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.2.808     Document Type: Article

References (71)

1. Compston, A., and A. Coles. 2002. Multiple sclerosis. Lancet 359:1221.
2. Martin, R., D. Jaraquemada, M. Flerlage, J. Richert, J. Whitaker, E. O. Long, D. E. McFarlin, and H. F. McFarland. 1990. Fine specificity and HLA restriction of myelin basic protein-specific cytotoxic T cell lines from multiple sclerosis patients and healthy individuals. J. Immunol. 145:540.
3. Wucherpfennig, K. W. 2001. Mechanisms for the induction of autoimmunity by infectious agents. J. Clin. Invest. 108:1097.
4. Sibley, W. A., C. R. Bamford, and K. Clark. 1985. Clinical viral infections and multiple sclerosis. Lancet 1:1313.
5. Buljevac, D., H. Z. Flach, W. C. Hop, D. Hijdra, J. D. Laman, H. F. Savelkoul, F. G. van der Meché, P. A. van Doom, and R. Q. Hintzen. 2002. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain 125:952.
6. Buljevac, D., R. P. Verkooyen, B. C. Jacobs, W. Hop, L. A. van der Zwaan, P. A. van Doorn, and R. Q. Hintzen. 2003. Chlamydia pneumoniae and the risk for exacerbation in multiple sclerosis patients. Ann. Neurol. 54:828.
7. Billiau, A., and P. Matthys. 2001. Modes of action of Freund's adjuvants in experimental models of autoimmune diseases. J. Leukocyte Biol. 70:849.
8. Heeger, P. S., T. Forsthuber, C. Shive, E. Biekert, C. Genain, H. H. Hofstetter, A. Karulin, and P. V. Lehmann. 2000. Revisiting tolerance induced by autoantigen in incomplete Freund's adjuvant. J. Immunol. 164:5771.
9. Hamada, T., B. F. Driscoll, M. W. Kies, and E. C. Alvord, Jr. 1989. LPS augments adoptive transfer of experimental allergic encephalomyelitis in the Lewis rat. Autoimmunity 2:275.
10. Segal, B. M., J. T. Chang, and E. M. Shevach. 2000. CpG oligonucleotides are potent adjuvants for the activation of autoreactive encephalitogenic T cells in vivo. J. Immunol. 164:5683.
11. Ichikawa, H. T., L. P. Williams, and B. M. Segal. 2002. Activation of APCs through CD40 or Toll-like receptor 9 overcomes tolerance and precipitates autoimmune disease. J. Immunol. 169:2781.
12. Dziarski, R. 2003. Recognition of bacterial peptidoglycan by the innate immune system. Cell. Mol. Life Sci. 60:1793.
13. Schrijver, I. A., M. J. Melief, H. M. Markusse, I. Van Aelst, G. Opdenakker, M. P. Hazenberg, and J. D. Laman. 2001. Peptidoglycan from sterile human spleen induces T-cell proliferation and inflammatory mediators in rheumatoid arthritis patients and healthy subjects. Rheumatology 40:438.
14. Schrijver, I. A., M. van Meurs, M. J. Melief, C. W. Ang, D. Buljevac, R. Ravid, M. P. Hazenberg, and J. D. Laman. 2001. Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis. Brain 124:1544.
15. Schrijver, I. A., M. J. Melief, P. P. Tak, M. P. Hazenberg, and J. D. Laman. 2000. Antigen-presenting cells containing bacterial peptidoglycan in synovial tissues of rheumatoid arthritis patients coexpress costimulatory molecules and cytokines. Arthritis Rheum. 43:2160.
16. van der Heijden, I. M., B. Wilbrink, I. Tchetverikov, I. A. Schrijver, L. M. Schouls, M. P. Hazenberg, F. C. Breedveld, and P. P. Tak. 2000. Presence of bacterial DNA and bacterial peptidoglycans in joints of patients with rheumatoid arthritis and other arthritides. Arthritis Rheum. 43:593.
17. Girardin, S. E., P. J. Sansonetti, and D. J. Philpott. 2002. Intracellular vs extracellular recognition of pathogens - common concepts in mammals and flies. Trends Microbiol. 10:193.
18. Underhill, D. M., A. Ozinsky, A. M. Hajjar, A. Stevens, C. B. Wilson, M. Bassetti, and A. Aderem. 1999. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401:811.
19. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11:443.
20. Ozinsky, A., D. M. Underhill, J. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA 97:13766.
21. Girardin, S. E., L. H. Travassos, M. Herve, D. Blanot, I. G. Boneca, D. J. Philpott, P. J. Sansonetti, and D. Mengin-Lecreulx. 2003. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278:41702.
22. Girardin, S. E., I. G. Boneca, L. A. Carneiro, A. Antignac, M. Jehanno, J. Viala, K. Tedin, M. K. Taha, A. Labigne, U. Zahringer, et al. 2003. Nod1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan. Science 300:1584.
23. Inohara, N., Y. Ogura, A. Fontalba, O. Gutierrez, F. Pons, J. Crespo, K. Fukase, S. Inamura, S. Kusumoto, M. Hashimoto, et al. 2003. Host recognition of bacterial muramyl dipeptide mediated through NOD2: implications for Crohn's disease. J. Biol. Chem. 278:5509.
24. Girardin, S. E., I. G. Boneca, J. Viala, M. Chamaillard, A. Labigne, G. Thomas, D. J. Philpott, and P. J. Sansonetti. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278:8869.
25. Rosenthal, R. S., and R. Dziarski. 1994. Isolation of peptidoglycan and soluble peptidoglycan fragments. Methods Enzymol. 235:253.
26. Travassos, L. H., S. E. Girardin, D. J. Philpott, D. Blanot, M. A. Nahori, C. Werts, and I. G. Boneca. 2004. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep. 5:1000.
27. Dmitriev, B. A., F. V. Toukach, K. J. Schaper, O. Holst, E. T. Rietschel, and S. Ehlers. 2003. Tertiary structure of bacterial murein: the scaffold model. J. Bacteriol. 185:3458.
28. Wang, Z. M., X. Li, R. R. Cocklin, M. Wang, K. Fukase, S. Inamura, S. Kusumoto, D. Gupta, and R. Dziarski. 2003. Human peptidoglycan recognition protein-L is an N-acetylmuramoyl-L-alanine amidase. J. Biol. Chem. 278:49044.
29. Gelius, E., C. Persson, J. Karlsson, and H. Steiner. 2003. A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-L-alanine amidase activity. Biochem. Biophys. Res. Commun. 306:988.
30. Laman, J. D., M. van Meurs, M. M. Schellekens, M. de Boer, B. Melchers, L. Massacesi, H. Lassmann, E. Claassen, and B. A. 't Hart. 1998. Expression of accessory molecules and cytokines in acute EAE in marmoset monkeys (Callithrix jacchus). J. Neuroimmunol. 86:30.
31. Claassen, E., K. Gerritse, J. D. Laman, and W. J. Boersma. 1992. New immunoenzyme-cytochemical stainings for the in situ detection of epitope specificity and isotype of antibody forming B cells in experimental and natural (auto) immune responses in animals and man. J. Immunol. Methods 150:207.
32. Hammad, H., H. J. de Heer, T. Souille, V. Angeli, F. Trottein, H. C. Hoogsteden, and B. N. Lambrecht. 2004. Activation of peroxisome proliferator-activated receptor-γ in dendritic cells inhibits the development of eosinophilic airway inflammation in a mouse model of asthma. Am. J. Pathol. 164:263.
33. Eisenbarth, S. C., D. A. Piggott, J. W. Huleatt, I. Visintin, C. A. Herrick, and K. Bottomly. 2002. Lipopolysaccharide-enhanced, Toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J. Exp. Med. 196:1645.
34. Zamvil, S. S., and L. Steinman. 1990. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol. 8:579.
35. Kool, J., H. De Visser, M. Y. Gerrits-Boeye, I. S. Klasen, M. J. Melief, C. G. Van Helden-Meeuwsen, L. M. Van Lieshout, J. G. Ruseler-Van Embden, W. B. Van den Berg, G. M. Bahr, et al. 1994. Detection of intestinal flora-derived bacterial antigen complexes in splenic macrophages of rats. J. Histochem. Cytochem. 42:1435.
36. Schrijver, I. A., M. J. Melief, F. Eulderink, M. P. Hazenberg, and J. D. Laman. 1999. Bacterial peptidoglycan polysaccharides in sterile human spleen induce proinflammatory cytokine production by human blood cells. J. Infect. Dis. 179:1459.
37. Kraehenbuhl, J. P., S. A. Hopkins, S. Kernels, and E. Pringault. 1997. Antigen sampling by epithelial tissues: implication for vaccine design. Behring Inst. Mitt. 24.
38. Rescigno, M., M. Urbano, B. Valzasina, M. Francolini, G. Rotta, R. Bonasio, F. Granucci, J. P. Kraehenbuhl, and P. Ricciardi-Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2:361.
39. 125I-labeled peptidoglycan-polysaccharide fragments from group A and group D streptococci. Infect. Immun. 52:390.
40. Gilbart, J., and A. Fox. 1987. Elimination of group A streptococcal cell walls from mammalian tissues. Infect. Immun. 55:1526.
41. Park, H., A. R. Zeiger, and H. R. Schumacher. 1984. Detection of soluble peptidoglycan in urine after penicillin administration. Infect. Immun. 43:139.
42. Lehtonen, L., P. Kortekangas, P. Oksman, E. Eerola, H. Aro, and A. Toivanen. 1994. Synovial fluid muramic acid in acute inflammatory arthritis. Br. J. Rheumatol. 33:1127.
43. Lehtonen, L., E. Eerola, P. Oksman, and P. Toivanen. 1995. Muramic acid in peripheral blood leukocytes of healthy human subjects. J. Infect. Dis. 171:1060.
44. Melief, M. J., M. A. Hoijer, H. C. Van Paassen, and M. P. Hazenberg. 1995. Presence of bacterial flora-derived antigen in synovial tissue macrophages and dendritic cells. Br. J. Rheumatol. 34:1112.
45. Hoijer, M. A., M. J. Melief, C. G. van Helden-Meeuwsen, F. Eulderink, and M. P. Hazenberg. 1995. Detection of muramic acid in a carbohydrate fraction of human spleen. Infect. Immun. 63:1652.
46. Fukui, M., R. Imamura, M. Umemura, T. Kawabe, and T. Suda. 2003. Pathogenassociated molecular patterns sensitize macrophages to Fas ligand-induced apoptosis and IL-1β release. J. Immunol. 171:1868.
47. Hou, W. S., and L. Van Parijs. 2004. A Bcl-2-dependent molecular timer regulates the lifespan and immunogenicity of dendritic cells. Nat. Immunol. 5:583.
48. Moser, M. 2004. Balancing life and death. Nat. Immunol. 5:559.
49. Dziarski, R. 2004. Peptidoglycan recognition proteins (PGRPs). Mol. Immunol. 40:877.
50. Girardin, S. E., and D. J. Philpott. 2004. Mini-review: the role of peptidoglycan recognition in innate immunity. Eur. J. Immunol. 34:1777.
51. Šimelyte, E., M. Rimpilainen, X. Zhang, and P. Toivanen. 2003. Role of peptidoglycan subtypes in the pathogenesis of bacterial cell wall arthritis. Ann. Rheum. Dis. 62:976.
52. Majcherczyk, P. A., H. Langen, D. Heumann, M. Fountoulakis, M. P. Glauser, and P. Moreillon. 1999. Digestion of Streptococcus pneumoniae cell walls with its major peptidoglycan hydrolase releases branched stem peptides carrying proinflammatory activity. J. Biol. Chem. 274:12537.
53. Burroughs, M., E. Rozdzinski, S. Geelen, and E. Tuomanen. 1993. A structure-activity relationship for induction of meningeal inflammation by muramyl peptides. J. Clin. Invest. 92:297.
54. Zhang, X., M. Rimpilainen, E. Šimelyte, and P. Toivanen. 2001. Enzyme degradation and pro inflammatory activity in arthritogenic and nonarthritogenic Eubacterium aerofaciens cell walls. Infect. Immun. 69:7277.
55. Hoijer, M. A., M. J. Melief, W. Keck, and M. P. Hazenberg. 1996. Purification and characterization of N-acetylmuramyl-L-alanine amidase from human plasma using monoclonal antibodies. Biochim. Biophys. Acta 1289:57.
56. Hoijer, M. A., M. J. Melief, R. Debets, and M. P. Hazenberg. 1997. Inflammatory properties of peptidoglycan are decreased after degradation by human N-acetylmuramyl-L-alanine amidase. Eur. Cytokine Netw. 8:375.
57. Rescigno, M., F. Granucci, S. Citterio, M. Foti, and P. Ricciardi-Castagnoli. 1999. Coordinated events during bacteria-induced DC maturation. Immunol. Today 20:200.
58. Shirota, H., K. Sano, N. Hirasawa, T. Terui, K. Ohuchi, T. Hattori, K. Shirato, and G. Tamura. 2001. Novel roles of CpG oligodeoxynucleotides as a leader for the sampling and presentation of CpG-tagged antigen by dendritic cells. J. Immunol. 167:66.
59. Maurer, T., A. Heit, H. Hochrein, F. Ampenberger, M. O'Keeffe, S. Bauer, G. B. Lipford, R. M. Vabulas, and H. Wagner. 2002. CpG-DNA aided cross-presentation of soluble antigens by dendritic cells. Eur. J. Immunol. 32:2356.
60. Heit, A., T. Maurer, H. Hochrein, S. Bauer, K. M. Huster, D. H. Busch, and H. Wagner. 2003. Cutting edge: Toll-like receptor 9 expression is not required for CpG DNA-aided cross-presentation of DNA-conjugated antigens but essential for cross-priming of CD8 T cells. J. Immunol. 170:2802.
61. Michelsen, K. S., A. Aicher, M. Mohaupt, T. Hartung, S. Dimmeler, C. J. Kirschning, and R. R. Schumann. 2001. The role of Toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCS): peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J. Biol. Chem. 276:25680.
62. Lawrence, C., and C. Nauciel. 1998. Production of interleukin-12 by murine macrophages in response to bacterial peptidoglycan. Infect. Immun. 66:4947.
63. Wang, Z. M., C. Liu, and R. Dziarski. 2000. Chemokines are the main proinflammatory mediators in human monocytes activated by Staphylococcus aureus, peptidoglycan, and endotoxin. J. Biol. Chem. 275:20260.
64. Dabbagh, K., and D. B. Lewis. 2003. Toll-like receptors and T-helper-1/T-helper-2 responses. Curr. Opin. Infect. Dis. 16:199.
65. Kapsenberg, M. L. 2003. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 3:984.
66. + T cell-mediated suppression by dendritic cells. Science 299:1033.
67. Noseworthy, J. H., C. Lucchinetti, M. Rodriguez, and B. G. Weinshenker. 2000. Multiple sclerosis. N. Engl. J. Med. 343:938.
68. Hill, N., and N. Sarvetnick. 2002. Cytokines: promoters and dampeners of autoimmunity. Curr. Opin. Immunol. 14:791.
69. Lock, C., G. Hermans, R. Pedotti, A. Brendolan, E. Schadt, H. Garren, A. Langer-Gould, S. Strober, B. Cannella, J. Allard, et al. 2002. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8:500.
70. Boonstra, A., C. Asselin-Paturel, M. Gilliet, C. Crain, G. Trinchieri, Y. J. Liu, and A. O'Garra. 2003. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential Toll-like receptor ligation. J. Exp. Med. 197:101.
71. Qi, H., T. L. Denning, and L. Soong. 2003. Differential induction of interleukin-10 and interleukin-12 in dendritic cells by microbial Toll-like receptor activators and skewing of T-cell cytokine profiles. Infect. Immun. 71:3337.