Cleavage of osteopontin by matrix metalloproteinase-12 modulates experimental autoimmune encephalomyelitis disease in C57BL/6 mice

American Journal of Pathology

Volumn 177, Issue 3, 2010, Pages 1448-1458

  DaSilva, Angelika Goncalves ^a   Liaw, Lucy ^b   Yong, V Wee ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b Maine Medical Center Research Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MACROPHAGE ELASTASE; MESSENGER RNA; OSTEOPONTIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; FEMALE; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PROCESSING; WESTERN BLOTTING;

EID: 77956543890     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.091081     Document Type: Article

References (54)

1. Steinman L: Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell 1996, 85:299-302
2. Frohman EM, Racke MK, Raine CS: Multiple sclerosis: the plaque and its pathogenesis. N Engl J Med 2006, 354:942-955
3. Frohman EM: Multiple sclerosis. Med Clin North Am 2003, 87:867-897, viii-ix
4. Hafler DA, Slavik JM, Anderson DE, O'Connor KC, De Jager P, Baecher-Allan C: Multiple sclerosis. Immunol Rev 2005, 204:208-231
5. Chabas D, Baranzini SE, Mitchell D, Bernard CC, Rittling SR, Denhardt DT, Sobel RA, Lock C, Karpuj M, Pedotti R, Heller R, Oksenberg JR, Steinman L: The influence of the proinflammatory cyrokine, osteopontin, on autoimmune demyelinating disease. Science 2001, 294:1731-1735
6. Denhardt DT, Noda M, O'Regan AW, Pavlin D, Berman JS: Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 2001, 107:1055-1061
7. Keegan BM, Noseworthy JH: Multiple sclerosis. Annu Rev Med 2002, 53:285-302
8. Liu YN, Kang BB, Chen JH: Transcriptional regulation of human osteopontin promoter by C/EBPalpha and AML-1 in metastatic cancer cells. Oncogene 2004, 23:278-288
9. Jansson M, Panoutsakipoulou V, Baker J, Klein L, Cantor H: Attenuated experimental autoimmune encephalomyelitis in Eta-1/osteopontin- deficient mice. J Immunol 2002, 168:2096-2099
10. Blom T, Franzen A, Heinegard D, Holmdahl R: Comment on "The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease." Science 2003, 299:1845a
11. Vogt MH, Lopatinskaya L, Smits M, Polman CH, Nagelkerken L: Elevated osteopontin levels in active relapsing-remitting multiple sclerosis. Annals of Neurology 2003, 53:819-822
12. Fakaura H, Ogata A, Kon S, Fukazawa T, Kikuchi S, Tashiro K, Uede T: Increased osteopontin in cerebrospinal fluid and brains of patients with multiple sclerosis. Presented at the American Neurological Association 128 Annual meeting, San Francisco, 2003, 54 Suppl. 7:s1-94
13. Vogt MH, Floris S, Killestein J, Knol DL, Smits M, Barkhof F, Polman CH, Nagelkerken L: Osteopontin levels and increased disease activity in relapsing-remitting multiple sclerosis patients. J Neuroimmunol 2004, 155:155-160
14. Comabella M, Pericot I, Goertsches R, Espejo C, Castillo M, Blas- Navarro C, Montalban X: Plasma osteopontin levels in different clinical subtypes of multiple sclerosis. J Neuroimmunol 2005, 158:231-239
15. Chowdhury SA, Lin J, Sadiq SA: Specificity and correlation with disease activity of cerebrospinal fluid osteopontin levels in patients with multiple sclerosis. Arch Neurol 2008, 65:232-235
16. Braitch M, Nunan R, Niepel G, Edwards LJ, Constantinescu CS: Increased osteopontin levels in the cerebrospinal fluid of patients with multiple sclerosis. Arch Neurol 2008, 65:633-635
17. Mochida S, Hashimoto M, Matsui A, Naito M, Inao M, Nagoshi S, Nagano M, Egashira T, Mishiro S, Fujiwara K: Genetic polymorphims in promoter region of osteopontin gene may be a marker reflecting hepatitis activity in chronic hepatitis C patients. Biochem Biophys Res Commun 2004, 313:1079-1085
18. Niino M, Kikuchi S, Fukazawa T, Yabe I, Tashiro K: Genetic polymorphisms of osteopontin in association with multiple sclerosis in Japanese patients. J Neuroimmunol 2003, 136:125-129 (Pubitemid 36298851)
19. Caillier S, Barcellos LF, Baranzini SE, Swerdin A, Lincoln RR, Steinman L, Martin E, Haines JL, Pericak-Vance M, Hauser SL, Oksenberg JR: Osteopontin polymorphisms and disease course in multiple sclerosis. Genes Immun 2003, 4:312-315 (Pubitemid 39562131)
20. Hensiek AE, Roxburgh R, Meranian M, Seaman S, Yeo T, Compston DAS, Sawcer SJ: Osteopontin genes and clinical severity of multiple sclerosis. J Neurol 2003, 250:943-947
21. Diaz-Sanchez M, Williams K, DeLuca GC, Esiri MM: Protein co-expression with axonal injury in multiple sclerosis plaques. Acta Neuropathol 2006, 111:289-299
22. Sinclair C, Mirakhur M, Kirk J, Farrell M, McQuaid S: Up-regulation of osteopontin and alphaBeta-crystallin in the normal-appearing white matter of multiple sclerosis: an immunohistochemical study utilizing tissue microarrays. Neuropathol Appl Neurobiol 2005, 31:292-303 (Pubitemid 40769528)
23. Koning N, Bo L, Hoek RM, Huitinga I: Downregulation of macrophage inhibitory molecules in multiple sclerosis lesions. Ann Neurol 2007, 62:504-514 (Pubitemid 350308775)
24. Hur EM, Youssef S, Haws ME, Zhang SY, Sobel RA, Steinman L: Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat Immunol 2007, 8:74-83 (Pubitemid 46242361)
25. Sodek J, Ganss B, McKee MD: Osteopontin. Crit Rev Oral Biol Med 2000, 11:279-303
26. Scatena M, Liaw L, Giachelli CM: Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol 2007, 27:2302-2309 (Pubitemid 350203943)
27. Hamada Y, Nokihara K, Okazaki M, Fujitani W, Matsumoto T, Matsuo M, Umakoshi Y, Takahashi J, Matsuura N: Angiogenic activity of osteopontin-derived peptide SVVYGLR. Biochem Biophys Res Commun 2003, 310:153-157 (Pubitemid 37168007)
28. Yamamoto N, Sakai F, Kon S, Morimoto J, Kimura C, Yamazaki H, Okazaki I, Seki N, Fujii T, Uede T: Essential role of the cryptic epitope SLAYGLR within osteopontin in a murine model of rheumatoid arthritis. J Clin Invest 2003, 112:181-188 (Pubitemid 38056354)
29. Agnihotri R, Crawford HC, Haro H, Matrisian LM, Havrda MC, Liaw L: Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin). J Biol Chem 2001, 276:28261-28267 (Pubitemid 37391532)
30. Hou P, Troen T, Ovejero MC, Kirkegaard T, Andersen TL, Byrjalsen I, Ferreras M, Sato T, Shapiro SD, Foged NT, Delaisse JM: Matrix metalloproteinase-12 (MMP-12) in osteoclasts: new lesson on the involvement of MMPs in bone resorption. Bone 2004, 34:37-47
31. Weaver A, Goncalves da Silva A, Nuttall RK, Edwards DR, Shapiro SD, Rivest S, Yong VW: An elevated matrix metalloproteinase (MMP) in an animal model of multiple sclerosis is protective by affecting Th1/Th2 polarization. FASEB J 2005, 19:1668-1670
32. Lindberg RL, De Groot CJ, Montagne L, Freitag P, van der Valk P, Kappos L, Leppert D: The expression profile of matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) in lesions and normal appearing white matter of multiple sclerosis. Brain 2001, 124:1743-1753
33. Pagenstecher A, Stalder AK, Kincaid CL, Shapiro SD, Campbell IL: Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states. Am J Pathol 1998, 152:729-741
34. Cossins JA, Clements JM, Ford J, Miller KM, Pigott R, Vos W, Van der Walk P, De Groot CJA: Enhanced expression of MMP-7 and MMP-9 in demyelinating multiple sclerosis lesions. Acta Neuropathologica 1997, 94:590-598
35. Kouwenhoven M, Ozenci V, Gomes A, Yarilin D, Giedraitis V, Press R, Link H: Multiple sclerosis: elevated expression of matrix metalloproteinases in blood monocytes. J Autoimmun 2001, 16:463-470
36. Anthony DCC, Ferguson B, Matyzak MK, Millert KM, Esiri MM, Perry VH: Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke. Neuropathol Appl Neurobiol 1997, 23:406-415
37. Agrawal S, Anderson P, Durbeej M, van Rooijen N, Ivars F, Opdenakker G, Sorokin LM: Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 2006, 203:1007-1019
38. Folgueras AR, Fueyo A, Garcia-Suarez O, Cox J, Astudillo A, Tortorella P, Campestre C, Gutierrez-Fernandez A, Fanjul-Fernandez M, Pennington CJ, Edwards DR, Overall CM, Lopez-Otin C: Collagenase-2 deficiency or inhibition impair experimental autoimmune encephalomyelitis in mice. J Biol Chem 2008, 283:9465-9474
39. Yong VW, Power C, Forsyth P, Edwards DR: Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2001, 2:502-511
40. Yong VW, Zabad RK, Agrawal S, Goncalves Dasilva A, Metz LM: Elevation of matrix metalloproteinases (MMPs) in multiple sclerosis and impact of immunomodulators. J Neurol Sci 2007, 259:79-84
41. Agrawal SM, Lau L, Yong VW: MMPs in the central nervous system: where the good guys go bad. Semin Cell Dev Biol 2008, 19:42-51
42. Goncalves DaSilva A, Yong VW: Matrix metalloproteinase-12 deficiency worsens relapsing-remitting experimental autoimmune encephalomyelitis in association with cytokine and chemokine dysregulation. Am J Pathol 2009, 174:898-909
43. Liaw L, Birk DE, Ballas CB, Whitsitt JS, Davidson JM, Hogan BL: Altered wound healing in mice lacking a functional osteopontin gene (spp1). J Clin Invest 1998, 101:1468-1478
44. Shipley JM, Wesselschmidt RL, Kobayashi DK, Ley TJ, Shapiro SD: Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci USA 1996, 93:3942-3946
45. Wells JE, Biernaskie J, Szymanska A, Larsen PH, Yong VW, Corbett D: Matrix metalloproteinase (MMP)-12 expression has a negative impact on sensorimotor function following intracerebral haemorrhage in mice. Eur J Neurosci 2005, 21:187-196
46. Giuliani F, Metz LM, Wilson T, Fan Y, Bar-Or A, Yong VW: Additive effect of the combination of glatiramer acetate and minocycline in a model of MS. J Neuroimmunol 2005, 158:213-221
47. Larsen PH: Matrix metalloproteinases: clearing the way for myelin formation in the CNS. Neuroscience. Calgary, University of Calgary, 2004, pp 1-167
48. DaSilva AG, Yong VW: Expression and regulation of matrix metalloproteinase- 12 in experimental autoimmune encephalomyelitis and by bone marrow derived macrophages in vitro. J Neuroimmunol 2008, 199:24-34
49. Rittling SR, Matsumoto HN, McKee MD, Nanci A, An XR, Novick KE, Kowalski AJ, Noda M, Denhardt DT: Mice lacking osteopontin show normal development and bone structure but display altered osteoclast formation in vitro. J Bone Miner Res 1998, 13:1101-1111
50. Masuda H, Takahashi Y, Asai S, Takayama T: Distinct gene expression of osteopontin in patients with ulcerative colitis. J Surgical research 2003, 111:85-90
51. Rosenberg GA: Matrix metalloproteinases and neuroinflammation in multiple sclerosis. Neuroscientist 2002, 8:586-595
52. Selvaraju R, Bernasconi L, Losberger C, Graber P, Kadi L, Avellana- Adalid V, Picard-Riera N, Van Evercooren AB, Cirillo R, Kosco-Vilbois M, Feger G, Papoian R, Boschert U: Osteopontin is upregulated during in vivo demyelination and remyelination and enhances myelin formation in vitro. Mol Cell Neurosci 2004, 25:707-721
53. Larsen PH, DaSilva AG, Conant K, Yong VW: Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J Neurosci 2006, 26:2207-2214
54. Stromnes IM, Goverman JM: Osteopontin-induced survival of T cells. Nat Immunol 2007, 8:19-20