Kallikrein 6 regulates early CNS demyelination in a viral model of multiple sclerosis

Brain Pathology

Volumn 22, Issue 5, 2012, Pages 709-722

  Scarisbrick, Isobel A ^a   Yoon, Hyesook ^a   Panos, Michael ^a   Larson, Nadya ^a   Blaber, Sachiko I ^b   Blaber, Michael ^b   Rodriguez, Moses ^a  

^a MAYO CLINIC   (United States)

^b FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

poliovirus; serine protease; spinal cord; TMEV

Indexed keywords

CAPSID PROTEIN; KALLIKREIN 6; MYELIN BASIC PROTEIN; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; DEMYELINATING DISEASE; DISEASE COURSE; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; LEUKEMIA CELL; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; MYELITIS; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; SPINAL CORD; SPLEEN CELL; VIRUS CAPSID;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, VIRAL; HYPERSENSITIVITY; KALLIKREINS; MICE; MONOCYTES; MULTIPLE SCLEROSIS; RNA, MESSENGER; RNA, VIRAL; SPINAL CORD; STATISTICS, NONPARAMETRIC; T-LYMPHOCYTES; THEILOVIRUS; TIME FACTORS; UP-REGULATION;

EID: 84865482393     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2012.00577.x     Document Type: Article

References (70)

1. Abraham M, Shapiro S, Karni A, Weiner HL, Miller A, (2005) Gelatinases (MMP-2 and MMP-9) are preferentially expressed by Th1 vs Th2 cells. J Neuroimmunol 163: 157-164. (Pubitemid 40692958)
2. Akassoglou K, Adams RA, Bauer J, Mercado P, Tseveleki V, Lassmann H, et al, (2004) Fibrin depletion decreases inflammation and delays the onset of demyelination in a tumor necrosis factor transgenic mouse model for multiple sclerosis. Proc Natl Acad Sci U S A 101: 6698-6703. (Pubitemid 38586037)
3. Alvord EC, Hruby S, Sires LR, (1979) Degradation of myelin basic protein by cerebrospinal fluid: preservation of antigenic determinants under physiological conditions. Ann Neurol 6: 474-482. (Pubitemid 10174405)
4. Angelo PF, Lima AR, Alves FM, Blaber SI, Scarisbrick IA, Blaber M, et al, (2006) Substrate specificity of human kallikrein 6: salt and glycosaminoglycan activation effects. J Biol Chem 281: 3116-3126. (Pubitemid 43845921)
5. Bar-Or A, Nuttall RK, Duddy M, Alter A, Kim HJ, Ifergan I, et al, (2003) Analyses of all matrix metalloproteinase members in leukocytes emphasize monocytes as major inflammatory mediators in multiple sclerosis. Brain 126: 2738-2749. (Pubitemid 37463092)
6. Bernett MJ, Blaber SI, Scarisbrick IA, Dhanarajan P, Thompson SM, Blaber M, (2002) Crystal structure and biochemical characterization of human kallikrein 6 reveals that a trypsin-like kallikrein is expressed in the central nervous system. J Biol Chem 277: 24562-24570. (Pubitemid 34951983)
7. Blaber SI, Scarisbrick IA, Bernett MJ, Dhanarajan P, Seavy MA, Jin Y, et al, (2002) Enzymatic properties of rat myelencephalon-specific protease. Biochemistry 41: 1165-1173. (Pubitemid 34083769)
8. Blaber SI, Ciric B, Christophi GP, Bernett MJ, Blaber M, Rodriguez M, Scarisbrick IA, (2004) Targeting kallikrein 6-proteolysis attenuates CNS inflammatory disease. FASEB J 19: 920-922.
9. Cammer W, Brosnan CF, Basile C, Bloom BR, Norton WT, (1986) Complement potentiates the degradation of myelin proteins by plasmin: implications for a mechanism of inflammatory demyelination. Brain Res 364: 91-101. (Pubitemid 16149019)
10. Christophi GP, Isackson PJ, Blaber SI, Blaber M, Rodriguez M, Scarisbrick IA, (2004) Distinct promoters regulate tissue-specific and differential expression of kallikrein 6 in CNS demyelinating disease. J Neurochem 91: 1439-1449. (Pubitemid 39658570)
11. Cuzner ML, Gveric D, Strand C, Loughlin AJ, Paemen L, Opdenakker G, Newcombe J, (1996) The expression of tissue-type plasminogen activator, matrix metalloproteases and endogenous inhibitors in the central nervous system in multiple sclerosis: comparison of stages in lesion evolution. J Neuropathol Exp Neurol 55: 1194-1204. (Pubitemid 26397138)
12. Denic A, Zoecklein L, Kerkvliet J, Papke L, Edukulla R, Warrington A, et al, (2011) Transgenic expression of viral capsid proteins predisposes to axonal injury in a murine model of multiple sclerosis. Brain Pathol 21: 501-515.
13. Fainardi E, Castellazzi M, Bellini T, Manfrinato MC, Baldi E, Casetta I, et al, (2006) Cerebrospinal fluid and serum levels and intrathecal production of active matrix metalloproteinase-9 (MMP-9) as markers of disease activity in patients with multiple sclerosis. Mult Scler 12: 294-301. (Pubitemid 43827184)
14. Gerety SJ, Rundell MK, Dal Canto MC, Miller SD, (1994) Class II-restricted T cell responses in Theiler's murine encephalomyelitis virus-induced demyelinating disease. VI. Potentiation of demyelination with and characterization of an immunopathologic CD4+ T cell line specific for an immunodominant VP2 epitope. J Immunol 152: 919-929.
15. Gijbels K, Masure S, Carton H, Opdenakker G, (1992) Gelatinase in cerebrospinal fluid of patients with multiple sclerosis and other inflammatory neurological disorders. J Neuroimmunol 41: 29-34.
16. Gonzalez H, Ottervald J, Nilsson KC, Sjogren N, Miliotis T, Von Bahr H, et al, (2009) Identification of novel candidate protein biomarkers for the post-polio syndrome-implications for diagnosis, neurodegeneration and neuroinflammation. J Proteomics 71: 670-681.
17. Gveric D, Hanemaaijer R, Newcombe J, van Lent NA, Sier CF, Cuzner ML, (2001) Plasminogen activators in multiple sclerosis lesions: implications for the inflammatory response and axonal damage. Brain 124: 1978-1988. (Pubitemid 32945899)
18. Haile Y, Simmen KC, Pasichnyk D, Touret N, Simmen T, Lu JQ, et al, (2011) Granule-derived granzyme B mediates the vulnerability of human neurons to T cell-induced neurotoxicity. J Immunol 187: 4861-4872.
19. Han MH, Hwang SI, Roy DB, Lundgren DH, Price JV, Ousman SS, et al, (2008) Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature 451: 1076-1081. (Pubitemid 351317445)
20. Hebb AL, Bhan V, Wishart AD, Moore CS, Robertson GS, (2011) Human kallikrein 6 cerebrospinal levels are elevated in multiple sclerosis. Curr Drug Discov Technol 7: 137-140.
21. Kumnok J, Ulrich R, Wewetzer K, Rohn K, Hansmann F, Baumgartner W, Alldinger S, (2008) Differential transcription of matrix-metalloproteinase genes in primary mouse astrocytes and microglia infected with Theiler's murine encephalomyelitis virus. J Neurovirol 14: 205-217. (Pubitemid 351895542)
22. Leppert D, Waubant E, Burk MR, Oksenberg JR, Hauser SL, (1996) Interferon beta-1b inhibits gelatinase secretion and in vitro migration of human T cells: a possible mechanism for treatment efficacy in MS. Ann Neurol 40: 846-852. (Pubitemid 27044602)
23. Leppert D, Ford J, Stabler G, Grygar C, Lienert C, Huber S, et al, (1998) Matrix metalloproteinase-9 (gelatinase B) is selectively elevated in CSF during relapses and stable phases of multiple sclerosis. Brain 121: 2327-2334. (Pubitemid 28552469)
24. Lin X, Njenga MK, Johnson AJ, Pavelko KD, David CS, Pease LR, Rodriguez M, (2002) Transgenic expression of Theiler's murine encephalomyelitis virus genes in H-2(b) mice inhibits resistance to virus-induced demyelination. J Virol 76: 7799-7811. (Pubitemid 34761002)
25. Lindberg RLP, De Groot CJA, Montagne L, Freitag P, van der Valk P, Kappos L, Leppert D, (2001) The expression profile of matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) in lesions and normal appearing white matter of multiple sclerosis. Brain 124: 1743-1753. (Pubitemid 32845436)
26. Lipton HL, (1975) Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect Immun 11: 1147-1155.
27. Maeda A, Sobel RA, (1996) Matrix metalloproteinases in the normal human central nervous system, microglia nodules, and multiple sclerosis lesions. J Neuropathol Exp Neurol 55: 300-309. (Pubitemid 26085579)
28. Mandler RN, Dencoff JD, Midani F, Ford CC, Ahmed W, Rosenberg GA, (2001) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in cerebrospinal fluid differ in multiple sclerosis and Devic's neuromyelitis optica. Brain 124: 493-498. (Pubitemid 32221316)
29. McFarlin DE, McFarland HF, (1982) Multiple sclerosis (first of two parts). N Engl J Med 307: 1183-1188. (Pubitemid 12037979)
30. McGavern DB, Zoecklein L, Drescher KM, Rodriguez M, (1999) Quantitative assessment of neurologic deficits in a chronic progressive murine model of CNS demyelination. Exp Neurol 158: 171-181. (Pubitemid 29344329)
31. McGavern DB, Zoecklein L, Sathornsumetee S, Rodriguez M, (2000) Assessment of hindlimb gait as a powerful indicator of axonal loss in a murine model of progressive CNS demyelination. Brain Res 877: 396-400.
32. Metz LM, Ahang Y, Yeung M, Party DG, Bell RB, Stoian CA, et al, (2004) Minocycline reduces gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Ann Neurol 55: 756-758.
33. Miller SD, Gerety SJ, (1990) Immunologic aspects of Theiler's murine encephalomyelitis virus (TMEV)-induced demyelinating disease. Semin Virol 1: 263-272.
34. Mitsui S, Okui A, Uemura H, Mizuno T, Yamada T, Yamamura Y, Yamaguchi N, (2002) Decreased cerebrospinal fluid levels of neurosin (KLK6), an aging-related protease, as a possible new risk factor for Alzheimer's disease. Ann N Y Acad Sci 977: 216-223. (Pubitemid 35418156)
35. Norga K, Paemen L, Masure S, Dillen C, Heremans H, Billiau A, et al, (1995) Prevention of acute autoimmune encephalomyelitis and abrogation of relapses in murine models of multiple sclerosis by the protease inhibitor d-penicillamine. Inflamm Res 44: 529-534. (Pubitemid 26008748)
36. Ogawa K, Yamada T, Tsujioka Y, Taguchi J, Takahashi M, Tsuboi Y, et al, (2000) Localization of a novel type trypsin-like serine protease, neurosin, in brain tissues of Alzheimer's disease and Parkinson's disease. Psychiatry Clin Neurosci 54: 419-426.
37. Paemen L, Olsson T, Soderstron M, Damme JV, Opdenakker G, (1994) Evaluation of gelatinases and IL-6 in the cerebrospinal fluid of patients with optic neuritis, multiple sclerosis and other inflammatory neurological diseases. Eur J Neurosci 1: 55-63. (Pubitemid 2141296)
38. Pavelko KD, Pease LR, David CS, Rodriguez M, (2007) Genetic deletion of a single immunodominant T-cell response confers susceptibility to virus-induced demyelination. Brain Pathol 17: 184-196. (Pubitemid 46466138)
39. Pierce ML, Rodriguez M, (1989) Erichrome stain for myelin on osmicated tissue embedded in glycol methacrylate plastic. J Histotechnol 12: 35-36.
40. Poser CM, (1986) Pathogenesis of multiple sclerosis. A critical reappraisal. Acta Neuropathol (Berl) 71: 1-10. (Pubitemid 16023576)
41. Proost P, Van Damme J, Opdenakker G, (1993) Leukocyte gelatinase B cleavage releases encephalitogens from human myelin basic protein. Biochem Biophys Res Commun 192: 1175-1781.
42. Puente SS, Sanchez LM, Overall CM, Lopez-Otin C, (2003) Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 4: 544-558. (Pubitemid 36781345)
43. Rivera-Quinones C, McGavern D, Schmelzer JD, Hunter SF, Low PA, Rodriguez M, (1998) Absence of neurological deficits following extensive demyelination in a class I-deficient murine model of multiple sclerosis. Nat Med 4: 187-193. (Pubitemid 28137373)
44. Rodriguez M, Oleszak E, Leibowitz J, (1987) Theiler's murine encephalomyelitis: a model of demyelination and persistence of virus. Crit Rev Immunol 7: 325-365.
45. Rodriguez M, Zoecklein L, Kerkvliet JG, Pavelko KD, Papke L, Howe CL, et al, (2008) Human HLA-DR transgenes protect mice from fatal virus-induced encephalomyelitis and chronic demyelination. J Virol 82: 3369-3380. (Pubitemid 351429914)
46. Rosenberg GA, Estrada EY, Dencoff JE, Stetler-Stevenson WG, (1995) TNF-alpha-induced gelatinase beta causes delayed opening of the blood-brain barrier: an expanded therapeutic window. Brain Res 703: 151-155. (Pubitemid 3013581)
47. Rosenberg GA, Dencoff JE, Correa NJ, Reiners M, Ford CC, (1996) Effect of steroids on CSF matrix metalloproteinases in multiple sclerosis: relation to blood-brain barrier injury. Neurology 46: 1626-1632. (Pubitemid 26185784)
48. Scarisbrick IA, (2008) The multiple sclerosis degradome: enzymatic cascades in development and progression of central nervous system inflammatory disease. Curr Top Microbiol Immunol 318: 133-175.
49. Scarisbrick IA, Towner MD, Isackson PJ, (1997) Nervous system specific expression of a novel serine protease: regulation in the adult rat spinal cord by excitotoxic injury. J Neurosci 17: 8156-8168. (Pubitemid 27461040)
50. Scarisbrick IA, Blaber SI, Lucchinetti CF, Genain CP, Blaber M, Rodriguez M, (2002) Activity of a newly identified serine protease in CNS demyelination. Brain 125: 1283-1296. (Pubitemid 34587138)
51. Scarisbrick IA, Blaber SI, Tingling JT, Rodriguez M, Blaber M, Christophi GP, (2006) Potential scope of action of tissue kallikreins in CNS immune-mediated disease. J Neuroimmunol 178: 167-176. (Pubitemid 44307340)
52. Scarisbrick IA, Sabharwal P, Cruz H, Larsen N, Vandell A, Blaber SI, et al, (2006) Dynamic role of kallikrein 6 in traumatic spinal cord injury. Eur J Neurosci 24: 1457-1469. (Pubitemid 44401668)
53. Scarisbrick IA, Linbo R, Vandell AG, Keegan M, Blaber SI, Blaber M, et al, (2008) Kallikreins are associated with secondary progressive multiple sclerosis and promote neurodegeneration. Biol Chem 389: 739-745. (Pubitemid 352009418)
54. Scarisbrick IA, Epstein B, Cloud BA, Yoon H, Wu J, Renner DN, et al, (2011) Functional role of kallikrein 6 in regulating immune cell survival. PLoS ONE 6: e18376. 1-11.
55. Scarisbrick IA, Radulovic M, Larson N, Burda J, Blaber I, Giannini C, et al, (2012) Kallikrein 6 is a novel molecular trigger of reactive astrogliosis. Biol Chem (in press).
56. Skuljec J, Gudi V, Ulrich R, Frichert K, Yildiz O, Pul R, et al, (2011) Matrix metalloproteinases and their tissue inhibitors in cuprizone-induced demyelination and remyelination of brain white and gray matter. J Neuropathol Exp Neurol 70: 758-769.
57. Stuve O, Dooley NP, Uhm JH, Antel JP, Francis GS, Williams G, Yong VW, (1996) Interferon beta-1b decreases the migration of T lymphocytes in vitro: effects on matrix metalloproteinase-9. Ann Neurol 40: 853-863. (Pubitemid 27044603)
58. Tsunoda I, Fujinami RS, (2010) Neuropathogenesis of Theiler's murine encephalomyelitis virus infection, an animal model for multiple sclerosis. J Neuroimmune Pharmacol 5: 355-369.
59. Uchida A, Oka Y, Aoyama M, Suzuki S, Yokoi T, Katano H, et al, (2004) Expression of myelencephalon-specific protease in transient middle cerebral artery occlusion model of rat brain. Brain Res 126: 129-136. (Pubitemid 38891834)
60. Ulrich R, Baumgartner W, Gerhauser I, Seeliger F, Haist V, Deschl U, Alldinger S, (2006) MMP-12, MMP-3, and TIMP-1 are markedly upregulated in chronic demyelinating theiler murine encephalomyelitis. J Neuropathol Exp Neurol 65: 783-793. (Pubitemid 44200319)
61. Ure DR, Rodriguez M, (2002) Preservation of neurologic function during inflammatory demyelination correlates with axon sparing in a mouse model of multiple sclerosis. Neuroscience 111: 399-411. (Pubitemid 34442622)
62. Vandell AG, Larson N, Laxmikanthan G, Panos M, Blaber SI, Blaber M, Scarisbrick IA, (2008) Protease activated receptor dependent and independent signaling by kallikreins 1 and 6 in CNS neuron and astroglial cell lines. J Neurochem 107: 855-870.
63. Warrington AE, Asakura K, Bieber AJ, Ciric B, Van Keulen V, Kaveri SV, et al, (2000) Human monoclonal antibodies reactive to oligodendrocytes promote remyelination in a model of multiple sclerosis. Proc Natl Acad Sci U S A 97: 6820-6825. (Pubitemid 30412798)
64. Waubant E, Goodkin DE, Gee L, Bacchetti P, Sloan R, Stewart T, et al, (1999) Serum MMP-9 and TIMP-1 levels are related to MRI activity in relapsing multiple sclerosis. Am Acad Neurol 53: 1397-1401. (Pubitemid 29491927)
65. Weaver A, Goncalves da Silva A, Nuttall RK, Edwards DR, Shapiro SD, Rivest S, Yong VW, (2005) An elevated matrix metalloproteinase (MMP) in an animal model of multiple sclerosis is protective by affecting Th1/Th2 polarization. FASEB J 19: 1668-1670. (Pubitemid 41429524)
66. Yang Y, Tian SJ, Wu L, Huang DH, Wu WP, (2011) Fibrinogen depleting agent batroxobin has a beneficial effect on experimental autoimmune encephalomyelitis. Cell Mol Neurobiol 31: 437-448.
67. Yauch RL, Palma JP, Yahikozawa H, Koh CS, Kim BS, (1998) Role of individual T-cell epitopes of Theiler's virus in the pathogenesis of demyelination correlates with the ability to induce a Th1 response. J Virol 72: 6169-6174. (Pubitemid 28283410)
68. Yoon H, Laxmikanthan G, Lee J, Blaber SI, Rodriguez A, Kogot JM, et al, (2007) Activation profiles and regulatory cascades of the human kallikrein-related peptidases. J Biol Chem 282: 31852-31864. (Pubitemid 350106429)
69. Yoon H, Blaber SI, Debela M, Goettig P, Scarisbrick IA, Blaber M, (2009) A completed KLK activome profile: investigation of activation profiles of KLK9, 10, and 15. Biol Chem 390: 373-377.
70. Zarghooni M, Soosaipillai A, Grass L, Scorilas A, Mirazimi N, Diamandis EP, (2002) Decreased concentration of human kallikrein 6 in brain extracts of Alzheimer's disease patients. Clin Biochem 35: 225-231. (Pubitemid 34634185)