Differential expression of multiple kallikreins in a viral model of multiple sclerosis points to unique roles in the innate and adaptive immune response

Biological Chemistry

Volumn 395, Issue 9, 2014, Pages 1063-1073

  Panos, Michael ^a   Christophi, George P ^a   Rodriguez, Moses ^a   Scarisbrick, Isobel A ^a  

^a MAYO CLINIC   (United States)

Author keywords

Axon injury; Demyelination; Inflammation; Multiple sclerosis; Serine protease; Theiler's murine encephalomyelitis virus

Indexed keywords

KALLIKREIN; KALLIKREIN 10; KALLIKREIN 13; KALLIKREIN 6; NEUROPSIN; STRATUM CORNEUM CHYMOTRYPTIC ENZYME; UNCLASSIFIED DRUG; VIRUS ANTIGEN; CAPSID PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONFERENCE PAPER; CONTROLLED STUDY; DEMYELINATION; DISEASE COURSE; FEMALE; GENETIC TRANSCRIPTION; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; MONOCYTE; MOUSE; MULTIPLE SCLEROSIS; MURINE ENCEPHALOMYELITIS VIRUS; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; T LYMPHOCYTE; UPREGULATION; VIRUS CAPSID; VIRUS ENCEPHALITIS; ANIMAL; BRAIN; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETICS; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPLEEN; THEILOVIRUS; TIME FACTOR; VIROLOGY;

MURINAE; MUS; THEILER'S ENCEPHALOMYELITIS VIRUS;

ADAPTIVE IMMUNITY; ANIMALS; BRAIN; CAPSID PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNITY, INNATE; KALLIKREINS; LYMPHOCYTE ACTIVATION; MICE; MONOCYTES; MULTIPLE SCLEROSIS; SPINAL CORD; SPLEEN; T-LYMPHOCYTES; THEILOVIRUS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84926343704     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0141     Document Type: Conference Paper

References (53)

1. Angelo, P.F., Lima, A.R., Alves, F.M., Blaber, S.I., Scarisbrick, I.A., Blaber, M., Juliano, L., and Juliano, M.A. (2006). Substrate specificity of human kallikrein 6: salt and glycosaminoglycan activation effects. J. Biol. Chem. 281, 3116-3126.
2. Attwood, B.K., Bourgognon, J.M., Patel, S., Mucha, M., Schiavon, E., Skrzypiec, A.E., Young, K.W., Shiosaka, S., Korostynski, M., Piechota, M., et al. (2011). Neuropsin cleaves EphB2 in the amygdala to control anxiety. Nature 473, 372-375.
3. Bernett, M.J., Blaber, S.I., Scarisbrick, I.A., Dhanarajan, P., Thompson, S.M., and 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.
4. Bhoola, K., Ramsaroop, R., Plendl, J., Cassim, B., Dlamini, Z., and Naicker, S. (2001). Kallikrein and kinin receptor expression in inflammation and cancer. Biol. Chem. 382, 77-89.
5. Blaber, S.I., Scarisbrick, I.A., Bernett, M.J., Dhanarajan, P., Seavy, M.A., Jin, Y., Schwartz, M.A., Rodriguez, M., and Blaber, M. (2002). Enzymatic properties of rat myelencephalonspecific protease. Biochemistry 41, 1165-1173.
6. Blaber, S.I., Ciric, B., Christophi, G.P., Bernett, M.J., Blaber, M., Rodriguez, M., and Scarisbrick, I.A. (2004). Targeting kallikrein 6-proteolysis attenuates CNS inflammatory disease. FASEB J. 19, 920-922.
7. Briot, A., Deraison, C., Lacroix, M., Bonnart, C., Robin, A., Besson, C., Dubus, P., and Hovnanian, A. (2009). Kallikrein 5 induces atopic dermatitis-like lesions through PAR2-mediated thymic stromal lymphopoietin expression in Netherton syndrome. J. Exp. Med. 206, 1135-1147.
8. Burda, J.E., Radulovic, M., Yoon, H., and Scarisbrick, I.A. (2013). Critical role for PAR1 in kallikrein 6-mediated oligodendrogliopathy. Glia 61, 1456-1470.
9. Chen, Z.L., Yoshida, S., Kato, K., Momota, Y., Suzuki, J., Tanaka, T., Ito, J., Nishino, H., Aimoto, S., Kiyama, H., et al. (1995). Expression and activity-dependent changes of a novel limbic-serine protease gene in the hippocampus. J. Neurosci. 15, 5088-5097.
10. Christophi, G.P., Isackson, P.J., Blaber, S.I., Blaber, M., Rodriguez, M., and Scarisbrick, I.A. (2004). Distinct promoters regulate tissue-specific and differential expression of kallikrein 6 in CNS demyelinating disease. J. Neurochem. 91, 1439-1449.
11. Davies, B., Kearns, I.R., Ure, J., Davies, C.H., and Lathe, R. (2001). Loss of hippocampal serine protease BSP1/neuropsin predisposes to global seizure activity. J. Neurosci. 21, 6993-7000.
12. Denic, A., Zoecklein, L., Kerkvliet, J., Papke, L., Edukulla, R., Warrington, A., Bieber, A., Pease, L.R., David, C.S., and Rodriguez, M. (2011). Transgenic expression of viral capsid proteins predisposes to axonal injury in a murine model of multiple sclerosis. Brain Pathol. 21, 501-515.
13. Diamandis, E.P., Scorilas, A., Kishi, T., Blennow, K., Luo, L.Y., Soosaipillai, A., Rademaker, A.W., and Sjogren, M. (2004). Altered kallikrein 7 and 10 concentrations in cerebrospinal fluid of patients with Alzheimer's disease and frontotemporal dementia. Clin. Biochem. 37, 230-237.
14. Drucker, K.D., Paulsen, A.P., Giannini, C., Decker, P.A., Blaber, I.S., Blaber, M., Uhm, J.H., O'Neill, B.P., Jenkins, R.B., and Scarisbrick, I.A. (2013). Clinical significance and novel mechanism of action of kallikrein 6 in glioblastoma. Neuro-Oncology 15, 305-18.
15. Gonzalez, H., Ottervald, J., Nilsson, K.C., Sjogren, N., Miliotis, T., Von Bahr, H., Khademi, M., Eriksson, B., Kjellstrom, S., Vegvari, A., 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.
16. Hebb, A.L., Bhan, V., Wishart, A.D., Moore, C.S., and Robertson, G.S.(2011). Human kallikrein 6 cerebrospinal levels are elevated in multiple sclerosis. Curr. Drug Discov. Technol. 7, 137-140.
17. Hovnanian, A. (2013). Netherton syndrome: skin inflammation and allergy by loss of protease inhibition. Cell Tissue Res. 351, 289-300.
18. Ishikawa, Y., Horii, Y., Tamura, H., and Shiosaka, S. (2008). Neuropsin (KLK8)-dependent and -independent synaptic tagging in the Schaffer-collateral pathway of mouse hippocampus. J. Neurosci. 28, 843-849.
19. Iwata, A., Maruyama, M., Akagi, T., Hashikawa, T., Kanazawa, I., Tsuji, S., and Nukina, N. (2003). Alpha-synuclein degradation by serine protease neurosin: implication for pathogenesis of synucleinopathies. Hum. Mol. Genet. 12, 2625-2635.
20. Komai, S., Matsuyama, T., Matsumoto, K., Kato, K., Kobayashi, M., Imamura, K., Yoshida, S., Ugawa, S., and Shiosaka, S. (2000). Neuropsin regulates an early phase of schaffer-collateral longterm potentiation in the murine hippocampus. Eur. J. Neurosci. 12, 1479-1486.
21. Lawrence, M.G., Stephens, C.R., Need, E.F., Lai, J., Buchanan, G., and Clements, J.A. (2012). Long terminal repeats act as androgen-responsive enhancers for the PSA-kallikrein locus. Endocrinology 153, 3199-3210.
22. Lin, X., Njenga, M.K., Johnson, A.J., Pavelko, K.D., David, C.S., Pease, L.R., and 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.
23. Lundwall, A. (2013). Old genes and new genes: the evolution of the kallikrein locus. Thromb. Haemost. 109, 469-475.
24. Matsumoto-Miyai, K., Ninomiya, A., Yamasaki, H., Tamura, H., Nakamura, Y., and Shiosaka, S. (2003). NMDA-dependent proteolysis of presynaptic adhesion molecule L1 in the hippocampus by neuropsin. J. Neurosci. 23, 7727-7736.
25. McGavern, D.B., Murray, P.D., and Rodriguez, M. (1999). Quantitation of spinal cord demyelination, remyelination, atrophy, and axonal loss in a model of progressive neurologic injury. J. Neurosci. Res. 58, 492-504.
26. McGavern, D.B., Murray, P.D., Rivera-Quinones, C., Schmelzer, J.D., Low, P.A., and Rodriguez, M. (2000). Axonal loss results in spinal cord atrophy, electrophysiological abnormalities and neurological deficits following demyelination in a chronic inflammatory model of multiple sclerosis. Brain 123, 519-531.
27. Oikonomopoulou, K., DeAngelis, R.A., Chen, H., Diamandis, E.P., Hollenberg, M.D., Ricklin, D., and Lambris, J.D. (2013). Induction of complement C3a receptor responses by kallikreinrelated peptidase 14. J. Immunol. 191, 3858-3866.
28. Oka, T., Akisada, M., Okabe, A., Sakurai, K., Shiosaka, S., and Kato, K. (2002). Extracellular serine protease neuropsin (KLK8) modulates neurite outgrowth and fasciculation of mouse hippocampal neurons in culture. Neurosci. Lett. 321, 141-144.
29. Pavelko, K.D., Pease, L.R., David, C.S., and Rodriguez, M. (2007). Genetic deletion of a single immunodominant T-cell response confers susceptibility to virus-induced demyelination. Brain Pathol. 17, 184-196.
30. Radulovic, M., Yoon, H., Larson, N., Wu, J., Linbo, R., Burda, J.E., Diamandis, E.P., Blaber, S.I., Blaber, M., Fehlings, M.G., et al. (2013). Kallikrein cascades in traumatic spinal cord injury: in vitro evidence for roles in axonopathy and neuron degeneration. J. Neuropathol. Exp. Neurol. 72, 1072-1089.
31. Rodriguez, M., Zoecklein, L., Kerkvliet, J.G., Pavelko, K.D., Papke, L., Howe, C.L., Pease, L.R., and David, C. (2008). Human HLA-DR transgenes protect mice from fatal virus-induced encephalomyelitis and chronic demyelination. J. Virol. 82, 3369-3380.
32. Scarisbrick, I.A. (2008). The multiple sclerosis degradome: enzymatic cascades in development and progression of central nervous system inflammatory disease. Curr. Topics Microbiol. Immunol. 318, 133-175.
33. Scarisbrick, I.A. (2012). Kallikrein activity in the central nervous system. In: The Kallikreins, M. Schmitt, C. Sommerhoff, H. Fritz, and V. Magdolen, eds. (Berlin: De Gruyter), pp. 349-372.
34. Scarisbrick, I.A., Towner, M.D., and Isackson, P.J. (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.
35. Scarisbrick, I.A., Asakura, K., Blaber, S., Blaber, M., Isackson, P.J., Beito, T., Rodriguez, M., and Windebank, A.J. (2000). Preferential expression of myelencephalon specific protease by oligodendrocytes of the adult rat spinal cord white matter. Glia 30, 219-230.
36. Scarisbrick, I.A., Isackson, P.J., Ciric, B., Windebank, A.J., and Rodriguez, M. (2001). MSP, a trypsin-like serine protease, is abundantly expressed in the human nervous system. J. Comp. Neurol. 431, 347-361.
37. Scarisbrick, I.A., Blaber, S.I., Lucchinetti, C.F., Genain, C.P., Blaber, M., and Rodriguez, M. (2002). Activity of a newly identified serine protease in CNS demyelination. Brain 125, 1283-1296.
38. Scarisbrick, I.A., Blaber, S.I., Tingling, J.T., Rodriguez, M., Blaber, M., and Christophi, G.P. (2006a). Potential scope of action of tissue kallikreins in CNS immune-mediated disease. J. Neuroimmunol. 178, 167-176.
39. Scarisbrick, I.A., Sabharwal, P., Cruz, H., Larsen, N., Vandell, A., Blaber, S.I., Ameenuddin, S., Papke, L.M., Fehlings, M.G., Reeves, R.K., et al. (2006b). Dynamic role of kallikrein 6 in traumatic spinal cord injury. Eur. J. Neurosci. 24, 1457-1469.
40. Scarisbrick, I.A., Linbo, R., Vandell, A.G., Keegan, M., Blaber, S.I., Blaber, M., Sneve, D., Lucchinetti, C.F., Rodriguez, M., and Diamandis, E.P. (2008). Kallikreins are associated with secondary progressive multiple sclerosis and promote neurodegeneration. Biol. Chem. 389, 739-745.
41. Scarisbrick, I.A., Epstein, B., Cloud, B.A., Yoon, H., Wu, J., Renner, D.N., Blaber, S.I., Blaber, M., Vandell, A.G., and Bryson, A.L. (2011). Functional role of kallikrein 6 in regulating immune cell survival. PLoS One 6, e18376.
42. Scarisbrick, I.A., Radulovic, M., Burda, J.E., Larson, N., Blaber, S.I., Giannini, C., Blaber, M., and Vandell, A.G. (2012a). Kallikrein 6 is a novel molecular trigger of reactive astrogliosis. Biol. Chem. 393, 355-367.
43. Scarisbrick, I.A., Yoon, H., Panos, M., Larson, N., Blaber, S.I., Blaber, M., and Rodriguez, M. (2012b). Kallikrein 6 regulates early CNS demyelination in a viral model of multiple sclerosis. Brain Pathol. 22, 709-722.
44. Shimizu-Okabe, C., Yousef, G.M., Diamandis, E.P., Yoshida, S., Shiosaka, S., and Fahnestock, M. (2001). Expression of the kallikrein gene family in normal and Alzheimer's disease brain. NeuroReport 12, 2747-2751.
45. Sotiropoulou, G. and Pampalakis, G. (2012). Targeting the kallikreinrelated peptidases for drug development. Trends Pharmacol. Sci. 33, 623-634.
46. Sotiropoulou, G., Pampalakis, G., and Diamandis, E.P. (2009). Functional roles of human kallikrein-related peptidases. J. Biol. Chem. 284, 32989-32994.
47. Spencer, B., Michael, S., Shen, J., Kosberg, K., Rockenstein, E., Patrick, C., Adame, A., and Masliah, E. (2013). Lentivirus mediated delivery of neurosin promotes clearance of wild-type alphasynuclein and reduces the pathology in an alpha-synuclein model of LBD. Mol. Ther. 21, 31-41.
48. Tamura, H., Ishikawa, Y., Hino, N., Maeda, M., Yoshida, S., Kaku, S., and Shiosaka, S. (2006). Neuropsin is essential for early processes of memory acquisition and Schaffer collateral long-term potentiation in adult mouse hippocampus in vivo. J. Physiol. 570, 541-551.
49. Terayama, R., Bando, Y., Yamada, M., and Yoshida, S. (2005). Involvement of neuropsin in the pathogenesis of experimental autoimmune encephalomyelitis. Glia 52, 108-118.
50. Tsunoda, I. and Fujinami, R.S. (2010). Neuropathogenesis of Theiler's murine encephalomyelitis virus infection, an animal model for multiple sclerosis. J. Neuroimmune Pharmacol. 5, 355-369.
51. Vandell, A.G., Larson, N., Laxmikanthan, G., Panos, M., Blaber, S.I., Blaber, M., and Scarisbrick, I.A. (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.
52. Yauch, R.L., Palma, J.P., Yahikozawa, H., Koh, C.S., and Kim, B.S. (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.
53. Yoon, H., Radulovic, M., Wu, J., Blaber, S.I., Blaber, M., Fehlings, M.G., and Scarisbrick, I.A. (2013). Kallikrein 6 signals through PAR1 and PAR2 to promote neuron injury and exacerbate glutamate neurotoxicity. J. Neurochem. 127, 283-298.