Serum levels of matrix metalloproteinases: Implications in clinical neurology

European Neurology

Volumn 67, Issue 2, 2012, Pages 121-128

  Romi, Fredrik ^a   Helgeland, Geir ^b   Gilhus, Nils Erik ^a,b  

^a HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

Matrix metalloproteinases; Multiple sclerosis; Myasthenia gravis; Neurodegenerative disease; Stroke

Indexed keywords

GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; NEUTROPHIL COLLAGENASE; STROMELYSIN; STROMELYSIN 2;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; AUTOIMMUNITY; DISEASE COURSE; ENZYME BLOOD LEVEL; EPILEPSY; EXTRACELLULAR MATRIX; HUMAN; MIGRAINE; MIGRAINE WITHOUT AURA; MULTIPLE SCLEROSIS; MYASTHENIA GRAVIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PRIORITY JOURNAL; RELAPSE; REVIEW; STROKE;

HUMANS; MATRIX METALLOPROTEINASES; NERVOUS SYSTEM DISEASES;

EID: 84855881970     PISSN: 00143022     EISSN: 14219913     Source Type: Journal    
DOI: 10.1159/000334862     Document Type: Review

References (77)

1. Yong VW, Agrawal SM, Stirling D: Targeting MMPs in acute and chronic neurological conditions. Neurotherapeutics 2007; 4: 580-589. (Pubitemid 47499287)
2. Morrison CJ, Butler GS, Rodríguez D, Overall CM: Matrix metalloproteinase proteomics: Substrates, targets, and therapy. Curr Opin Cell Biol 2009; 21: 645-653.
3. Murphy G, Nagase H: Progress in matrix metalloproteinase research. Mol Aspects Med 2008; 29: 290-308.
4. Bode W, Fernandez-Catalan C, Grams F, Gomis-Rüth FX, Nagase H, Tschesche H, Maskos K: Insights into MMP-TIMP interactions. Ann NY Acad Sci 1999; 878: 73-91. (Pubitemid 29353561)
5. Sternlicht MD, Werb Z: How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17: 463-516. (Pubitemid 33096184)
6. Michaluk P, Kaczmarek L: Matrix metalloproteinase-9 in glutamate-dependent adult brain function and dysfunction. Cell Death Differ 2007; 14: 1255-1258. (Pubitemid 46969864)
7. Greene J, Wang M, Liu YE, Raymond LA, Rosen C, Shi YE: Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J Biol Chem 1996; 271: 30375-30380. (Pubitemid 26404039)
8. Gomez DE, Alonso DF, Yoshiji H, Thorgeirsson UP: Tissue inhibitors of metalloproteinases: Structure, regulation and biological functions. Eur J Cell Biol 1997; 74: 111-122. (Pubitemid 27455388)
9. Hansson J, Vasan RS, Arnlöv J, Ingelsson E, Lind L, Larsson A, Michaëlsson K, Sundström J: Biomarkers of extracellular matrix metabolism (MMP-9 and TIMP-1) and risk of stroke, myocardial infarction, and causespecific mortality: Cohort study. PLoS One 2011; 6:e16185.
10. 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. (Pubitemid 47031205)
11. Witzemann V: Development of the neuromuscular junction. Cell Tissue Res 2006; 326: 263-271. (Pubitemid 44435807)
12. La Russa A, Cittadella R, De Marco EV, Valentino P, Andreoli V, Trecroci F, Latorre V, Gambardella A, Quattrone A: Single nucleotide polymorphism in the MMP-9 gene is associated with susceptibility to develop multiple sclerosis in an Italian case-control study. J Neuroimmunol 2010; 225: 175-179.
13. Arakaki PA, Marques MR, Santos MC: MMP-1 polymorphism and its relationship to pathological processes. J Biosci 2009; 34: 313-320.
14. Kotajima L, Aotsuka S, Fujimani M, Okawa-Takatsuji M, Kinoshita M, Sumiya M, Obata K: Increased levels of matrix metalloproteinase-3 in sera from patients with active lupus nephritis. Clin Exp Rheumatol 1998; 16: 409-415. (Pubitemid 28370851)
15. Chen WS, Lin KC, Chen CH, Liao HT, Wang HP, Li WY, Lee HT, Tsai CY, Chou CT: Autoantibody and biopsy grading are associated with expression of ICAM-1, MMP-3, and TRAIL in salivary gland mononuclear cells of Chinese patients with Sjogren's syndrome. J Rheumatol 2009; 36: 989-996.
16. Matache C, Stefanescu M, Dragomir C, Tanaseanu S, Onu A, Ofiteru A, Szegli G: Matrix metalloproteinase-9 and its natural inhibitor TIMP-1 expressed or secreted by peripheral blood mononuclear cells from patients with systemic lupus erythematosus. J Autoimmun 2003; 20: 323-331. (Pubitemid 36677524)
17. Kim WU, Min SY, Cho ML, Hong KH, Shin YJ, Park SH, Cho CS: Elevated matrix metalloproteinase-9 in patients with systemic sclerosis. Arthritis Res Ther 2005; 7:R71-R79.
18. Gruber BL, Sorbi D, French DL, Marchese MJ, Nuovo GJ, Kew RR, Arbeit LA: Markedly elevated serum MMP-9 (gelatinase B) levels in rheumatoid arthritis: A potentially useful laboratory marker. Clin Immunol Immunopathol 1996; 78: 161-171. (Pubitemid 26084595)
19. Konttinen YT, Halinen S, Hanemaaijer R, Sorsa T, Hietanen J, Ceponis A, Xu JW, Manthorpe R, Whittington J, Larsson A, Salo T, Kjeldsen L, Stenman UH, Eisen AZ: Matrix metalloproteinase (MMP)-9 type IV collagenase/gelatinase implicated in the pathogenesis of Sjogren's syndrome. Matrix Biol 1998; 17: 335-347. (Pubitemid 28486296)
20. Zucker S, Lysik RM, Zarrabi MH, Greenwald RA, Gruber B, Tickle SP, Baker TS, Docherty AJ: Elevated plasma stromelysin levels in arthritis. J Rheumatol 1994; 21: 2329-2333.
21. Levin VA, Phuphanich S, Yung WK, Forsyth PA, Maestro RD, Perry JR, Fuller GN, Baillet M: Randomized, double-blind, placebo-controlled trial of marimastat in glioblastoma multiforme patients following surgery and irradiation. J Neurooncol 2006; 78: 295-302. (Pubitemid 44018824)
22. Compston A, Coles A: Multiple sclerosis. Lancet 2008; 359: 1221-1231.
23. Stinissen P, Raus J, Zhang J: Autoimmune pathogenesis of multiple sclerosis: Role of autoreactive T lymphocytes and new immunotherapeutic strategies. Crit Rev Immunol 1997; 7: 33-75. (Pubitemid 27068807)
24. Goodin DS: The causal cascade to multiple sclerosis: A model for MS pathogenesis. PLoS One 2009; 4:e4565.
25. Ebers GC: Environmental factors and multiple sclerosis. Lancet Neurol 2008; 7: 268-277. (Pubitemid 351222732)
26. Burrell AM, Handel AE, Ramagopalan SV, Ebers GC, Morahan JM: Epigenetic mechanisms in multiple sclerosis and the major histocompatibility complex (MHC). Discov Med 2011; 11: 187-196.
27. Alexander JS, Harris MK, Wells SR, Mills G, Chalamidas K, Ganta VC, McGee J, Jennings MH, Gonzalez-Toledo E, Minagar A: Alterations in serum MMP-8, MMP-9, IL-12p40 and IL-23 in multiple sclerosis patients treated with interferon-beta1b. Mult Scler 2010; 1: 801-809.
28. Weaver A, Goncalves DaSilva 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. (Pubitemid 41429524)
29. Thorne M, Moore CS, Robertson GS: Lack of TIMP-1 increases severity of experimental autoimmune encephalomyelitis: Effects of darbepoetin alfa on TIMP-1 null and wildtype mice. J Neuroimmunol 2009; 211: 92-100.
30. Garcia-Montojo M, Dominguez-Mozo MI, de las Heras V, Bartolome M, Garcia-Martinez A, Arroyo R, Alvarez-Lafuente R: Neutralizing antibodies, MxA expression and MMP-9/TIMP-1 ratio as markers of bioavailability of interferon-beta treatment in multiple sclerosis patients: A two-year followup study. Eur J Neurol 2010; 17: 470-478.
31. Leppert D, Waubant E, Burk MR, Oksenberg JR, Hauser SL: Interferon beta-1b inhibits gelatinase secretion and in vivo migration of human T cells: A possible mechanism for treatment efficacy in multiple sclerosis. Ann Neurol 1996; 40: 846-852. (Pubitemid 27044602)
32. Kanesaka T, Mori M, Hattori T, Oki T, Kuwabara S: Serum matrix metalloproteinase-3 levels correlate with disease activity in relapsing-remitting multiple sclerosis. J Neurol Neurosurg Psychiatry 2006; 77: 185-188. (Pubitemid 43220839)
33. Luckman S, Gilhus NE, Romi F: Matrix metalloproteinases-3 in myasthenia gravis compared to other neurological disorders and healthy controls. Autoimmune Dis 2011; 2011: 151258.
34. Fainardi E, Castellazzi M, Tamborino C, Trentini A, Manfrinato MC, Baldi E, Tola MR, Dallocchio F, Granieri E, Bellini T: Potential relevance of cerebrospinal fluid and serum levels and intrathecal synthesis of active matrix metalloproteinase-2 (MMP-2) as markers of disease remission in patients with multiple sclerosis. Mult Scler 2009; 15: 547-554.
35. Agrawal SM, Silva C, Tourtellotte WW, Yong VW: EMMPRIN: A novel regulator of leukocyte transmigration into the CNS in multiple sclerosis and experimental autoimmune encephalomyelitis. J Neurosci 2011; 31: 669-677.
36. Niimi N, Kohyama K, Kamei S, Matsumoto Y: Intravenous immunoglobulin therapy prevents development of autoimmune encephalomyelitis and suppresses activation of matrix metalloproteinases. Neuropathology 2011; 31: 392-400.
37. Zabad RK, Metz LM, Todoruk TR, Zhang Y, Mitchell JR, Yeung M, Patry DG, Bell RB, Yong VW: The clinical response to minocycline in MS is accompanied by immune changes. Mult Scler 2007; 13: 517-526.
38. Hu W, Metselaar J, Ben LH, Cravens PD, Singh MP, Frohman EM, Eagar TN, Racke MK, Kieseier BC, Stüve O: PEG minocycline-liposomes ameliorate CNS autoimmune disease. PLoS One 2009; 4:e4151.
39. Mazzini F, Nuti E, Petri A, Rossello A: Immobilization of matrix metalloproteinase 8 (MMP-8) for online drug screening. J Chromatogr B Analyt Technol Biomed Life Sci 2011; 879: 756-762.
40. Yong VW: Differential mechanisms of action of interferon- and glatiramer acetate in MS. Neurology 2002; 59: 802-808.
41. Lindstrøm JM, Seybold ME, Lennon VA, Whittingham S, Duane DD: Antibody to acetylcholine receptor in myasthenia gravis: Prevalence, clinical correlates, and diagnostic value. 1975. Neurology 1998; 51: 933-939.
42. Evoli A, Batocchi AP, Minisci C, Di Schino C, Tonali P: Therapeutic options in ocular myasthenia gravis. Neuromuscul Disord 2001; 11: 208-216. (Pubitemid 32201147)
43. Luchanok U, Kaminski HJ: Ocular myasthenia: Diagnostic and treatment recommendations and the evidence base. Curr Opin Neurol 2008; 21: 8-15.
44. Wilcox N: Myasthenia gravis. Curr Opin Immunol 1993; 5: 910-917.
45. Li Z, Forester N, Vincent A: Modulation of acetylcholine receptor function in TE671 (rhabdomyocyosarcoma) cells by non-AchR ligands: Possible relevance to seronegative myasthenia gravis. J Neuroimmunol 1996; 64: 179-183. (Pubitemid 26094634)
46. Hoch W, McConville J, Helms S, Newsom-Davis J, Melms A, Vincent A: Auto-antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat Med 2001; 7: 365-368. (Pubitemid 32224355)
47. McConville J, Farrugia ME, Beeson D, Kishore U, Metcalfe R, Newsom-Davis J, Vincent A: Detection and characterization of MuSK antibodies in seronegative myasthenia gravis. Ann Neurol 2004; 55: 580-584. (Pubitemid 38391977)
48. Fuhrer C, Sugiyama JE, Taylor RG, Hall ZW: Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle. EMBO 1997; 16: 4951-4960. (Pubitemid 27348404)
49. Borges LS, Ferns M: Agrin-induced phosphorylation of the acetylcholine receptor regulates cytoskeletal anchoring and clustering. J Cell Biol 2001; 153: 1-11. (Pubitemid 34280189)
50. Romi F, Skeie GO, Gilhus NE, Aarli JA: Striational antibodies in myasthenia gravis: Reactivity and possible clinical significance. Arch Neurol 2005; 62: 442-446. (Pubitemid 40349480)
51. Faber-Elmann A, Grabovsky V, Dayan M, Sela M, Alon R, Mozes E: An altered peptide ligand inhibits the activities of matrix metalloproteinase-9 and phospholipase C, and inhibits T cell interactions with VCAM-1 induced in vivo by a myasthenogenic T cell epitope. FASEB J 2001; 15: 187-194. (Pubitemid 32061669)
52. Romi F, Gilhus NE, Luckman S: Serum matrix metalloproteinase-3 (MMP-3) levels are elevated in myasthenia gravis. J Neuroimmunol 2008; 195: 96-99.
53. Helgeland G, Petzold A, Luckman SP, Gilhus NE, Plant GT, Romi F: Matrix metalloproteinases in myasthenia gravis. Eur Neurol 2011; 65: 53-58.
54. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T: Regulation of matrix metalloproteinases: An overview. Mol Cell Biochem 2003; 253: 269-285.
55. Ogata Y, Enghild JJ, Nagase H: Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9. J Biol Chem 1992; 267: 3581-3584.
56. Vempati P, Karagiannis ED, Popel AS: A biochemical model of matrix metalloproteinase 9 activation and inhibition. J Biol Chem 2007; 282: 37585-37596.
57. Sternlicht MD, Werb Z: ECM proteinases; in Kreis T, Vale R (eds): Guidebook to the Extracellular Matrix and Adhesion Proteins. New York, Oxford University Press, 1999, pp 503-562.
58. VanSaun M, Humburg BC, Arnett MG, Pence M, Werle MJ: Activation of Matrix Metalloproteinase-3 is altered at the frog neuromuscular junction following changes in synaptic activity. Dev Neurobiol 2007; 67: 1488-1497. (Pubitemid 350067593)
59. VanSaun M, Werle MJ: Matrix metalloproteinase-3 removes agrin from synaptic basal lamina. J Neurobiol 2000; 43: 140-149. (Pubitemid 30241212)
60. VanSaun M, Herrera AA, Werle MJ: Structural alterations at the neuromuscular junctions of matrix metalloproteinase 3 null mutant mice. J Neurocytol 2002; 32: 1129-1142. (Pubitemid 39004722)
61. Rymner MM, Akhtar N, Martin C, Summers D: Management of acute ischemic stroke: Time is brain. Mo Med 2010; 107: 333-337.
62. Ramos-Fernandez M, Bellolio MF, Stead LG: Matrix metalloproteinase-9 as a marker for acute ischemic stroke: A systematic review. J Stroke Cerebrovasc Dis 2011; 20: 47-54.
63. Rosell A, Alvarez-Sabin J, Arenillas JF, Rovira A, Delgado P, Fernàndez-Cadenas I, Penalba A, Molina CA, Montaner J: A matrix metalloproteinase protein array reveals a strong relation between MMP-9 and MMP-13 with diffusion-weighted image lesion increase in human stroke. Stroke 2005; 36: 1415-1420. (Pubitemid 40967504)
64. Lien LM, Hsieh YC, Bai CH, Chen WH, Chiu HC, Hsieh FI, Shyu KG, Chiou HY, Hsu CY: Association of blood active matrix metalloproteinase-3 with carotid plaque score from a community population in Taiwan. Atherosclerosis 2010; 212: 595-600.
65. Alvarez-Sabín J, Delgado P, Abilleira S, Molina CA, Arenillas J, Ribó M, Santamarina E, Quintana M, Monasterio J, Montaner J: Temporal profile of matrix metalloproteinases and their inhibitors after spontaneous intracerebral hemorrhage: Relationship to clinical and radiological outcome. Stroke 2004; 35: 1316-1322. (Pubitemid 38697450)
66. Pico F, Jacob MP, Labreuche J, Soufir N, Touboul PJ, Benessiano J, Cambien F, Grandchamp B, Michel JB, Amarenco P: Matrix metalloproteinase-3 and intracranial arterial dolichoectasia. Ann Neurol 2010; 67: 508-515.
67. Solé S, Petegnief V, Gorina R, Chamorro A, Planas AM: Activation of matrix metalloproteinase-3 and agrin cleavage in cerebral ischemia/reperfusion. J Neuropathol Exp Neurol 2004; 63: 338-349. (Pubitemid 38429031)
68. Zhao BQ, Tejima E, Lo EH: Neurovascular proteases in brain injury, hemorrhage and remodeling after stroke. Stroke 2007; 38 (suppl 2):748-752. (Pubitemid 46188254)
69. Sokolowska B, Jozwik A, Niebroj-Dobosz I, Janik P, Kwiecinski H: Evaluation of matrix metalloproteinases in serum of patients with amyotrophic lateral sclerosis with pattern recognition methods. J Physiol Pharmacol 2009; 60: 117-120.
70. Niebroj-Dobosz I, Janik P, Sokolowska B, Kwiecinski H: Matrix metalloproteinases and their tissue inhibitors in serum and cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Eur J Neurol 2010; 17: 226-231.
71. Kiaei M, Kipiani K, Calingasan NY, Wille E, Chen J, Heissig B, Rafii S, Lorenzl S, Beal MF: Matrix metalloproteinase-9 regulates TNFalpha and FasL expression in neuronal, glial cells and its absence extends life in a transgenic mouse model of amyotrophic lateral sclerosis. Exp Neurol 2007; 205: 74-81. (Pubitemid 46617492)
72. Lorenzl S, Narr S, Angele B, Krell HW, Gregorio J, Kiaei M, Pfister HW, Beal MF: The matrix metalloproteinases inhibitor Ro 28-2653 [correction of Ro 26-2853] extends survival in transgenic ALS mice. Exp Neurol 2006; 200: 166-171. (Pubitemid 44080757)
73. Horstmann S, Budig L, Gardner H, Koziol J, Deuschle M, Schilling C, Wagner S: Matrix metalloproteinases in peripheral blood and cerebrospinal fluid in patients with Alzheimer's disease. Int Psychogeriatr 2010; 22: 966-972.
74. Martins-Oliveira A, Speciali JG, Dach F, Marcaccini AM, Gonçalves FM, Gerlach RF, Tanus-Santos JE: Different circulating metalloproteinases profiles in women with migraine with and without aura. Clin Chim Acta 2009; 408: 60-64.
75. Wilczynski GM, Konopacki FA, Wilczek E, Lasiecka Z, Gorlewicz A, Michaluk P, Wawrzyniak M, Malinowska M, Okulski P, Kolodziej LR, Konopka W, Duniec K, Mioduszewska B, Nikolaev E, Walczak A, Owczarek D, Gorecki DC, Zuschratter W, Ottersen OP, Kaczmarek L: Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol 2008; 180: 1021-1035. (Pubitemid 351398426)
76. Takács E, Nyilas R, Szepesi Z, Baracskay P, Karlsen B, Røsvold T, Bjørkum AA, Czurkó A, Kovács Z, Kékesi AK, Juhász G: Matrix metalloproteinase-9 activity increased by two different types of epileptic seizures that do not induce neuronal death: A possible role in homeostatic synaptic plasticity. Neurochem Int 2010; 56: 799-809.
77. Yin P, Yang L, Zhou HY, Sun RP: Matrix metalloproteinase-9 may be a potential therapeutic target in epilepsy. Med Hypotheses 2011; 76: 184-186.