Proteinase-activated receptor 2 modulates neuroinflammation in experimental autoimmune encephalomyelitis and multiple sclerosis

Journal of Experimental Medicine

Volumn 203, Issue 2, 2006, Pages 425-435

  Noorbakhsh, Farshid ^a,c,e   Tsutsui, Shigeki ^b,c   Vergnolle, Nathalie ^c   Boven, Leonie A ^d   Shariat, Neda ^a   Vodjgani, Mohammed ^e   Warren, Kenneth G ^a   Andrade Gordon, Patricia ^f   Hollenberg, Morley D ^c   Power, Christopher ^a,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d ERASMUS MEDICAL CENTER   (Netherlands)

^e TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^f JOHNSON AND JOHNSON PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; CYTOTOXIN; GAMMA INTERFERON; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROTEINASE ACTIVATED RECEPTOR 2;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AXONAL INJURY; CELL ACTIVATION; CELL INFILTRATION; CELL SECRETION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEMYELINATION; DISEASE COURSE; DISEASE SEVERITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOGENETICS; IMMUNOSTIMULATION; KNOCKOUT MOUSE; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RELAPSE; T LYMPHOCYTE; WILD TYPE;

ANIMALS; ASTROCYTES; CELL PROLIFERATION; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FRONTAL LOBE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERFERON TYPE II; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; MULTIPLE SCLEROSIS; OLIGODENDROGLIA; RECEPTOR, PAR-2; T-LYMPHOCYTES;

EID: 33344473933     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20052148     Document Type: Article

References (57)

1. Ossovskaya, V.S., and N.W. Bunnett. 2004. Protease-activated receptors: contribution to physiology and disease. Physiol. Rev. 84:579-621.
2. Hollenberg, M.D., and S.J. Compton. 2002. International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol. Rev. 54:203-217.
3. Steinhoff, M., J. Buddenkotte, V. Shpacovitch, A. Rattenholl, C. Moormann, N. Vergnolle, T.A. Luger, and M.D. Hollenberg. 2005. Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr. Rev. 26:1-43.
4. Macfarlane, S.R., M.J. Seatter, T. Kanke, G.D. Hunter, and R. Plevin. 2001. Proteinase-activated receptors. Pharmacol. Rev. 53:245-282.
5. Noorbakhsh, F., N. Vergnolle, M.D. Hollenberg, and C. Power. 2003. Proteinase-activated receptors in the nervous system. Nat. Rev. Neurosci. 4:981-990.
6. Cottrell, G.S., S. Amadesi, F. Schmidlin, and N. Bunnett. 2003. Protease-activated receptor 2: activation, signalling and function. Biochem. Soc. Trans. 31:1191-1197.
7. Vergnolle, N., M. Ferazzini, M.R. D'Andrea, J. Buddenkotte, and M. Steinhoff. 2003. Proteinase-activated receptors: novel signals for peripheral nerves. Trends Neurosci. 26:496-500.
8. Smith-Swintosky, V.L., C.T. Cheo-Isaacs, M.R. D'Andrea, R.J. Santulli, A.L. Darrow, and P. Andrade-Gordon. 1997. Protease-activated receptor-2 (PAR-2) is present in the rat hippocampus and is associated with neurodegeneration. J. Neurochem. 69:1890-1896.
9. Olejar, T., R. Matej, M. Zadinova, and P. Pouckova. 2002. Proteinase-activated receptor-2 expression on cerebral neurones after radiation damage: immunohistochemical observation in Wistar rats. Int. J. Tissue React. 24:81-88.
10. Rohatgi, T., P. Henrich-Noack, F. Sedehizade, M. Goertler, C.W. Wallesch, K.G. Reymann, and G. Reiser. 2004. Transient focal ischemia in rat brain differentially regulates mRNA expression of protease-activated receptors 1 to 4. J. Neurosci. Res. 75:273-279.
11. Hemmer, B., J.J. Archelos, and H.P. Hartung. 2002. New concepts in the immunopathogenesis of multiple sclerosis. Nat. Rev. Neurosci. 3:291-301.
12. Steinman, L., R. Martin, C. Bernard, P. Conlon, and J.R. Oksenberg. 2002. Multiple sclerosis: deeper understanding of its pathogenesis reveals new targets for therapy. Annu. Rev. Neurosci. 25:491-505.
13. Prat, A., and J. Antel. 2005. Pathogenesis of multiple sclerosis. Curr. Opin. Neurol. 18:225-230.
14. Hafler, D.A., J.M. Slavik, D.E. Anderson, K.C. O'Connor, P. De Jager, and C. Baecher-Allan. 2005. Multiple sclerosis. Immunol. Rev. 204:208-231.
15. Ristori, G., C. Montesperelli, A. Perna, S. Cannoni, L. Battistini, G. Borsellino, P. Riccio, G. Pesole, A. Chersi, C. Pozzilli, et al. 2000. Global immune disregulation in multiple sclerosis: from the adaptive response to the innate immunity. J. Neuroimmunol. 107:216-219.
16. Sospedra, M., and R. Martin. 2005. Immunology of multiple sclerosis. Annu. Rev. Immunol. 23:683-747.
17. Owens, T., and S. Sriram. 1995. The immunology of multiple sclerosis and its animal model, experimental allergic encephalomyelitis. Neurol. Clin. 13:51-73.
18. Behi, M.E., S. Dubucquoi, D. Lefranc, H. Zephir, J. De Seze, P. Vermersch, and L. Prin. 2005. New insights into cell responses involved in experimental autoimmune encephalomyelitis and multiple sclerosis. Immunol. Lett. 96:11-26.
19. Ubl, J.J., C. Vohringer, and G. Reiser. 1998. Co-existence of two types of [Ca2+]i-inducing protease-activated receptors (PAR-1 and PAR-2) in rat astrocytes and C6 glioma cells. Neuroscience. 86:597-609.
20. D'Andrea, M.R., C.K. Derian, D. Leturcq, S.M. Baker, A. Brunmark, P. Ling, A.L. Darrow, R.J. Santulli, L.F. Brass, and P. Andrade-Gordon. 1998. Characterization of protease-activated receptor-2 immunoreactivity in normal human tissues. J. Histochem. Cytochem. 46:157-164.
21. Johansson, U., C. Lawson, M. Dabare, D. Syndercombe-Court, A.C. Newland, G.L. Howells, and M.G. Macey. 2005. Human peripheral blood monocytes express protease receptor-2 and respond to receptor activation by production of IL-6, IL-8, and IL-1{beta}. J. Leukoc. Biol. 78:967-975.
22. Colognato, R., J.R. Slupsky, M. Jendrach, L. Burysek, T. Syrovets, and T. Simmet. 2003. Differential expression and regulation of protease-activated receptors in human peripheral monocytes and monocyte-derived antigen-presenting cells. Blood. 102:2645-2652.
23. Steinhoff, M., N. Vergnolle, S.H. Young, M. Tognetto, S. Amadesi, H.S. Ennes, M. Trevisani, M.D. Hollenberg, J.L. Wallace, G.H. Caughey, et al. 2000. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat. Med. 6:151-158.
24. Noorbakhsh, F., N. Vergnolle, J.C. McArthur, C. Silva, M. Vodjgani, P. Andrade-Gordon, M.D. Hollenberg, and C. Power. 2005. Proteinase-activated receptor-2 induction by neuroinflammation prevents neuronal death during HIV infection. J. Immunol. 174:7320-7329.
25. Bruck, W., and C. Stadelmann. 2005. The spectrum of multiple sclerosis: new lessons from pathology. Curr. Opin. Neurol. 18:221-224.
26. Bar-Or, A., E.M. Oliveira, D.E. Anderson, and D.A. Hafler. 1999. Molecular pathogenesis of multiple sclerosis. J. Neuroimmunol. 100:252-259.
27. Markovic-Plese, S., and H.F. McFarland. 2001. Immunopathogenesis of the multiple sclerosis lesion. Curr. Neurol. Neurosci. Rep. 1:257-262.
28. Barnett, M.H., and J.W. Prineas. 2004. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 55:458-468.
29. Matute, C., and F. Perez-Cerda. 2005. Multiple sclerosis: novel perspectives on newly forming lesions. Trends Neurosci. 28:173-175.
30. Hendriks, J.J., C.E. Teunissen, H.E. de Vries, and C.D. Dijkstra. 2005. Macrophages and neurodegeneration. Brain Res. Brain Res. Rev. 48:185-195.
31. Olson, J.K., J. Ludovic Croxford, and S.D. Miller. 2004. Innate and adaptive immune requirements for induction of autoimmune demyelinating disease by molecular mimicry. Mol. Immunol. 40:1103-1108.
32. Jack, C., F. Ruffini, A. Bar-Or, and J.P. Antel. 2005. Microglia and multiple sclerosis. J. Neurosci. Res. 81:363-373.
33. Tsutsui, S., F. Noorbakhsh, A. Sullivan, A.J. Henderson, K. Warren, K. Toney-Earley, S.E. Waltz, and C. Power. 2005. RON-regulated innate immunity is protective in an animal model of multiple sclerosis. Ann. Neurol. 57:883-895.
34. Buntinx, M., P. Stinissen, P. Steels, M. Ameloot, and J. Raus. 2002. Immune-mediated oligodendrocyte injury in multiple sclerosis: molecular mechanisms and therapeutic interventions. Crit. Rev. Immunol. 22:391-424.
35. Jin, G., T. Hayashi, J. Kawagoe, T. Takizawa, T. Nagata, I. Nagano, M. Syoji, and K. Abe. 2005. Deficiency of PAR-2 gene increases acute focal ischemic brain injury. J. Cereb. Blood Flow Metab. 25:302-313.
36. Fields, R.C., J.G. Schoenecker, J.P. Hart, M.R. Hoffman, S.V. Pizzo, and J.H. Lawson. 2003. Protease-activated receptor-2 signaling triggers dendritic cell development. Am. J. Pathol. 162:1817-1822.
37. Ferrell, W.R., J.C. Lockhart, E.B. Kelso, L. Dunning, R. Plevin, S.E. Meek, A.J. Smith, G.D. Hunter, J.S. McLean, F. McGarry, et al. 2003. Essential role for proteinase-activated receptor-2 in arthritis. J. Clin. Invest. 111:35-41.
38. Cenac, N., A.M. Coelho, C. Nguyen, S. Compton, P. Andrade-Gordon, W.K. MacNaughton, J.L. Wallace, M.D. Hollenberg, N.W. Bunnett, R. Garcia-Villar, et al. 2002. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor- 2. Am. J. Pathol. 161:1903-1915.
39. Ebeling, C., P. Forsythe, J. Ng, J.R. Gordon, M. Hollenberg, and H. Vliagoftis. 2005. Proteinase-activated receptor 2 activation in the airways enhances antigen-mediated airway inflammation and airway hyperresponsiveness through different pathways. J. Allergy Clin. Immunol. 115:623-630.
40. Seeliger, S., C.K. Derian, N. Vergnolle, N.W. Bunnett, R. Nawroth, M. Schmelz, P.Y. Von Der Weid, J. Buddenkotte, C. Sunderkotter, D. Metze, et al. 2003. Proinflammatory role of proteinase-activated receptor-2 in humans and mice during cutaneous inflammation in vivo. FASEB J. 17:1871-1885.
41. Coughlin, S.R., and E. Camerer. 2003. PARticipation in inflammation. J. Clin. Invest. 111:25-27.
42. Su, X., E. Camerer, J.R. Hamilton, S.R. Coughlin, and M.A. Matthay. 2005. Protease-activated receptor-2 activation induces acute lung inflammation by neuropeptide-dependent mechanisms. J. Immunol. 175:2598-2605.
43. Cocks, T.M., B. Fong, J.M. Chow, G.P. Anderson, A.G. Frauman, R.G. Goldie, P.J. Henry, M.J. Carr, J.R. Hamilton, and J.D. Moffatt. 1999. A protective role for protease-activated receptors in the airways. Nature. 398:156-160.
44. Fiorucci, S., A. Mencarelli, B. Palazzetti, E. Distrutti, N. Vergnolle, M.D. Hollenberg, J.L. Wallace, A. Morelli, and G. Cirino. 2001. Proteinase-activated receptor 2 is an anti-inflammatory signal for colonic lamina propria lymphocytes in a mouse model of colitis. Proc. Natl. Acad. Sci. USA. 98:13936-13941.
45. Johnston, J.B., C. Silva, J. Holden, K.G. Warren, A.W. Clark, and C. Power. 2001. Monocyte activation and differentiation augment human endogenous retrovirus expression: implications for inflammatory brain diseases. Ann. Neurol. 50:434-442.
46. Antony, J.M., G. van Marle, W. Opii, D.A. Butterfield, F. Mallet, V.W. Yong, J.L. Wallace, R.M. Deacon, K. Warren, and C. Power. 2004. Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat. Neurosci. 7:1088-1095.
47. Tsutsui, S., J. Schnermann, F. Noorbakhsh, S. Henry, V.W. Yong, B.W. Winston, K. Warren, and C. Power. 2004. A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J. Neurosci. 24:1521-1529.
48. Power, C., S. Henry, M.R. Del Bigio, P.H. Larsen, D. Corbett, Y. Imai, V.W. Yong, and J. Peeling. 2003. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann. Neurol. 53:731-742.
49. Corley, S.M., U. Ladiwala, A. Besson, and V.W. Yong. 2001. Astrocytes attenuate oligodendrocyte death in vitro through an alpha(6) integrin-laminin-dependent mechanism. Glia. 36:281-294.
50. Damiano, B.P., W.M. Cheung, R.J. Santulli, W.P. Fung-Leung, K. Ngo, R.D. Ye, A.L. Darrow, C.K. Derian, L. de Garavilla, and P. Andrade-Gordon. 1999. Cardiovascular responses mediated by protease-activated receptor-2 (PAR-2) and thrombin receptor (PAR-1) are distinguished in mice deficient in PAR-2 or PAR- 1. J. Pharmacol. Exp. Ther. 288:671-678.
51. Riches, D.W., and G.A. Underwood. 1991. Expression of interferon-beta during the triggering phase of macrophage cytocidal activation. Evidence for an autocrine/paracrine role in the regulation of this state. J. Biol. Chem. 266:24785-24792.
52. Oh, L.Y., P.H. Larsen, C.A. Krekoski, D.R. Edwards, F. Donovan, Z. Werb, and V.W. Yong. 1999. Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J. Neurosci. 19:8464-8475.
53. Al-Ani, B., M. Saifeddine, A. Kawabata, B. Renaux, S. Mokashi, and M.D. Hollenberg. 1999. Proteinase-activated receptor 2 (PAR(2)): development of a ligand-binding assay correlating with activation of PAR(2) by PAR(1)- and PAR(2)-derived peptide ligands. J. Pharmacol. Exp. Ther. 290:753-760.
54. Overbergh, L., D. Valckx, M. Waer, and C. Mathieu. 1999. Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine. 11:305-312.
55. Liu, J., M.W. Marino, G. Wong, D. Grail, A. Dunn, J. Bettadapura, A.J. Slavin, L. Old, and C.C. Bernard. 1998. TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 4:78-83.
56. Brundula, V., N.B. Rewcastle, L.M. Metz, C.C. Bernard, and V.W. Yong. 2002. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain. 125:1297-1308.
57. Youssef, S., O. Stuve, J.C. Patarroyo, P.J. Ruiz, J.L. Radosevich, E.M. Hur, M. Bravo, D.J. Mitchell, R.A. Sobel, L. Steinman, and S.S. Zamvil. 2002. The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature. 420:78-84.