Kallikrein-related peptidase 6 orchestrates astrocyte form and function through proteinase activated receptor-dependent mechanisms

References

Allen, M., Ghosh, S., Ahern, G.P., Villapol, S., Maguire-Zeiss, K.A., and Conant, K. (2016). Protease induced plasticity: matrix metalloproteinase-1 promotes neurostructural changes through activation of protease activated receptor 1. Sci. Rep. 6, 35497.10.1038/srep35497Search in Google Scholar PubMed PubMed Central

Anderson, M.A., Ao, Y., and Sofroniew, M.V. (2014). Heterogeneity of reactive astrocytes. Neurosci. Lett. 565, 23–29.10.1016/j.neulet.2013.12.030Search in Google Scholar PubMed PubMed Central

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, 3116–3126.10.1074/jbc.M510096200Search in Google Scholar PubMed

Anisowicz, A., Sotiropoulou, G., Stenman, G., Mok, S.C., and Sager, R. (1996). A novel protease homolog differentially expressed in breast and ovarian cancer. Mol. Med. 2, 624–636.10.1007/BF03401646Search in Google Scholar

Ashby, E.L., Kehoe, P.G., and Love, S. (2010). Kallikrein-related peptidase 6 in Alzheimer’s disease and vascular dementia. Brain Res. 1363, 1–10.10.1016/j.brainres.2010.09.017Search in Google Scholar PubMed

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, 24562–24570.10.1074/jbc.M202392200Search in Google Scholar PubMed

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 myelencephalon-specific protease. Biochemistry 41, 1165–1173.10.1021/bi015781aSearch in Google Scholar PubMed

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, 920–922.10.1096/fj.03-1212fjeSearch in Google Scholar PubMed

Borgono, C.A., Miacovos, M.P., and Diamandis, E.P. (2004). Human tissue kallikreins: physiologic roles and applications in cancer. Mol. Cancer Res. 2, 257–280.10.1158/1541-7786.257.2.5Search in Google Scholar

Boven, L.A., Vergnolle, N., Henry, S.D., Silva, C., Imai, Y., Holden, J., Warren, K., Hollenberg, M.D., and Power, C. (2003). Up-regulation of proteinase-activated receptor 1 expression in astrocytes during HIV encephalitis. J. Immunol. 170, 2638–2646.10.4049/jimmunol.170.5.2638Search in Google Scholar PubMed

Burda, J.E., Radulovic, M., Yoon, H., and Scarisbrick, I. A. (2013). Critical role for PAR1 in kallikrein 6-mediated oligodendrogliopathy. Glia 61, 1456–1470.10.1002/glia.22534Search in Google Scholar

Citron, B.A., Smirnova, I.V., Arnold, P.M., and Festoff, B.W. (2000). Upregulation of neurotoxic serine proteases, prothrombin, and protease-activated receptor 1 early after spinal cord injury. J. Neurotrauma. 17, 1191–1203.10.1089/neu.2000.17.1191Search in Google Scholar

Diamandis, E.P., Yousef, G.M., Petraki, C., and Soosaipillai, A. R. (2000). Human kallikrein 6 as a biomarker of alzheimer’s disease. Clin. Biochem. 33, 663–667.10.1016/S0009-9120(00)00185-5Search in Google Scholar

Dong, Y., Tan, O.L., Loessner, D., Stephens, C., Walpole, C., Boyle, G.M., Parsons, P.G., and Clements, J.A. (2010). Kallikrein-related peptidase 7 promotes multicellular aggregation via the α(5)β(1) integrin pathway and paclitaxel chemoresistance in serous epithelial ovarian carcinoma. Cancer Res. 70, 2624–2633.10.1158/0008-5472.CAN-09-3415Search in Google Scholar PubMed

Dong, Y., Stephens, C., Walpole, C., Swedberg, J.E., Boyle, G.M., Parsons, P.G., McGuckin, M.A., Harris, J.M., and Clements, J.A. (2013). Paclitaxel resistance and multicellular spheroid formation are induced by kallikrein-related peptidase 4 in serous ovarian cancer cells in an ascites mimicking microenvironment. PLoS One 8, e57056.10.1371/journal.pone.0057056Search in Google Scholar PubMed PubMed Central

Drucker, K.L., Paulsen, A.R., Giannini, C., Decker, P.A., Blaber, S.I., 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. Oncol. 15, 305–318.10.1093/neuonc/nos313Search in Google Scholar PubMed PubMed Central

Drucker, K.L., Gianinni, C., Decker, P.A., Diamandis, E.P., and Scarisbrick, I.A. (2015). Prognostic significance of multiple kallikreins in high-grade astrocytoma. BMC Cancer 15, 565.10.1186/s12885-015-1566-5Search in Google Scholar PubMed PubMed Central

Farmer, W.T. and Murai, K. (2017). Resolving astrocyte heterogeneity in the CNS. Front Cell Neurosci. 11, 300.10.3389/fncel.2017.00300Search in Google Scholar PubMed PubMed Central

Halassa, M.M., Dal Maschio, M., Beltramo, R., Haydon, P.G., Benfenati, F., and Fellin, T. (2010). Integrated brain circuits: neuron-astrocyte interaction in sleep-related rhythmogenesis. ScientificWorldJ. 10, 1634–1645.10.1100/tsw.2010.130Search in Google Scholar PubMed PubMed Central

Hamby, M.E., Coppola, G., Ao, Y., Geschwind, D.H., Khakh, B.S., and Sofroniew, M.V. (2012). Inflammatory mediators alter the astrocyte transcriptome and calcium signaling elicited by multiple G-protein-coupled receptors. J. Neurosci. 32, 14489–14510.10.1523/JNEUROSCI.1256-12.2012Search in Google Scholar PubMed PubMed Central

Iadecola, C. and Nedergaard, M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369–1376.10.1038/nn2003Search in Google Scholar

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, 2625–2635.10.1093/hmg/ddg283Search in Google Scholar

Junge, C.E., Sugawara, T., Mannaioni, G., Alagarsamy, S., Conn, P.J., Brat, D.J., Chan, P.H., and Traynelis, S.F. (2003). The contribution of protease-activated receptor 1 to neuronal damage caused by transient focal cerebral ischemia. Proc. Natl. Acad. Sci. USA 100, 13019–13024.10.1073/pnas.2235594100Search in Google Scholar

Junge, C.E., Lee, C.J., Hubbard, K.B., Zhang, Z., Olson, J.J., Hepler, J.R., Brat, D.J., and Traynelis, S.F. (2004). Protease-activated receptor-1 in human brain: localization and functional expression in astrocytes. Exp. Neurol. 188, 94–103.10.1016/j.expneurol.2004.02.018Search in Google Scholar

Kalluri, R. and Weinberg, R.A. (2009). The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420–1428.10.1172/JCI39104Search in Google Scholar

Kasai, T., Tokuda, T., Yamaguchi, N., Watanabe, Y., Kametani, F., Nakagawa, M., and Mizuno, T. (2008). Cleavage of normal and pathological forms of alpha-synuclein by neurosin in vitro. Neurosci. Lett. 436, 52–56.10.1016/j.neulet.2008.02.057Search in Google Scholar

Laxmikanthan, G., Blaber, S.I., Bernett, M.J., Scarisbrick, I.A., Juliano, M.A., and Blaber, M. (2005). 1.70 Å X-ray structure of human apo kallikrein 1: structural changes upon peptide inhibitor/substrate binding. Proteins 58, 802–814.10.1002/prot.20368Search in Google Scholar

Little, S.P., Dixon, E.P., Norris, F., Buckley, W., Becker, G.W., Johnson, M., Dobbins, J.R., Wyrick, T., Miller, J.R., MacKellar, W., et al. (1997). Zyme, a novel and potentially amyloidogenic enzyme cDNA isolated from Alzheimer’s disease brain. J. Biol. Chem. 272, 25135–25142.10.1074/jbc.272.40.25135Search in Google Scholar

Magklara, A., Mellati, A.A., Wasney, G.A., Little, S.P., Sotiropoulou, G., Becker, G.W., and Diamandis, E.P. (2003). Characterization of the enzymatic activity of human kallikrein 6: autoactivation, substrate specificity, and regulation by inhibitors. Biochem. Biophys. Res. Commun. 307, 948–955.10.1016/S0006-291X(03)01271-3Search in Google Scholar

Morel, L., Chiang, M.S.R., Higashimori, H., Shoneye, T., Iyer, L.K., Yelick, J., Tai, A. and Yang, Y. (2017). Molecular and functional properties of regional astrocytes in the adult brain. J. Neurosci. 37, 8706–8717.10.1523/JNEUROSCI.3956-16.2017Search in Google Scholar PubMed PubMed Central

Nakanishi-Matsui, M., Zheng, Y.W., Sulciner, D.J., Weiss, E.J., Ludeman, M.J., and Coughlin, S.R. (2000). PAR3 is a cofactor for PAR4 activation by thrombin. Nature 404, 609–613.10.1038/35007085Search in Google Scholar PubMed

Nicole, O., Goldshmidt, A., Hamill, C.E., Sorensen, S.D., Sastre, A., Lyuboslavsky, P., Hepler, J.R., McKeon, R.J., and Traynelis, S. F. (2005). Activation of protease-activated receptor-1 triggers astrogliosis after brain injury. J. Neurosci. 25, 4319–4329.10.1523/JNEUROSCI.5200-04.2005Search in Google Scholar PubMed PubMed Central

Noorbakhsh, F., Vergnolle, N., Hollenberg, M.D., and Power, C. (2003). Proteinase-activated receptors in the nervous system. Nat. Rev. Neurosci. 4, 981–990.10.1038/nrn1255Search in Google Scholar PubMed

Noorbakhsh, F., Vergnolle, N., McArthur, J.C., Silva, C., Vodjgani, M., Andrade-Gordon, P., Hollenberg, M.D., and Power, C. (2005). Proteinase-activated receptor-2 induction by neuroinflammation prevents neuronal death during HIV infection. J. Immunol. 174, 7320–7329.10.4049/jimmunol.174.11.7320Search in Google Scholar PubMed

Noorbakhsh, F., Tsutsui, S., Vergnolle, N., Boven, L.A., Shariat, N., Vodjgani, M., Warren, K.G., Andrade-Gordon, P., Hollenberg, M.D., and Power, C. (2006). Proteinase-activated receptor 2 modulates neuroinflammation in experimental autoimmune encephalomyelitis and multiple sclerosis. J. Exp. Med. 203, 425–435.10.1084/jem.20052148Search in Google Scholar PubMed PubMed Central

Ogawa, K., Yamada, T., Tsujioka, Y., Taguchi, J., Takahashi, M., Tsuboi, Y., Fujino, Y., Nakajima, M., Yamamoto, T., Akatsu, H., 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, 419–426.10.1046/j.1440-1819.2000.00731.xSearch in Google Scholar PubMed

Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Tea, I., Blaber, M., Blaber, S.I., Scarisbrick, I., Andrade-Gordon, P., Cottrell, G.S., Bunnett, N.W., et al. (2006a). Proteinase-activated receptors, targets for kallikrein signaling. J. Biol. Chem. 281, 32095–32112.10.1074/jbc.M513138200Search in Google Scholar PubMed

Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Vergnolle, N., Tea, I., Blaber, M., Blaber, S.I., Scarisbrick, I., Diamandis, E.P., and Hollenberg, M.D. (2006b). Kallikrein-mediated cell signalling: targeting proteinase-activated receptors (PARs). Biol. Chem. 387, 817–824.10.1515/BC.2006.104Search in Google Scholar PubMed

Ostrowska, E. and Reiser, G. (2008). The protease-activated receptor-3 (PAR-3) can signal autonomously to induce interleukin-8 release. Cell Mol. Life Sci. 65, 970–981.10.1007/s00018-008-7555-ySearch in Google Scholar PubMed

Pampalakis, G., Sykioti, V.S., Ximerakis, M., Stefanakou-Kalakou, I., Melki, R., Vekrellis, K., and Sotiropoulou, G. (2017). KLK6 proteolysis is implicated in the turnover and uptake of extracellular alpha-synuclein species. Oncotarget 8, 14502–14515.10.18632/oncotarget.13264Search in Google Scholar PubMed PubMed Central

Panos, M., Christophi, G.P., Rodriguez, M., and Scarisbrick, I.A. (2014). Differential expression of multiple kallikreins in a viral model of multiple sclerosis points to unique roles in the innate and adaptive immune response. Biol. Chem. 395, 1063–1073.10.1515/hsz-2014-0141Search in Google Scholar PubMed PubMed Central

Paul, I., Bhattacharya, S., Chatterjee, A., and Ghosh, M.K. (2013). Current understanding on EGFR and Wnt/beta-catenin signaling in glioma and their possible crosstalk. Genes Cancer 4, 427–446.10.1177/1947601913503341Search in Google Scholar PubMed PubMed Central

Pekny, M., Pekna, M., Messing, A., Steinhauser, C., Lee, J.M., Parpura, V., Hol, E.M., Sofroniew, M.V., and Verkhratsky, A. (2016). Astrocytes: a central element in neurological diseases. Acta Neuropathol. 131, 323–345.10.1007/s00401-015-1513-1Search in Google Scholar PubMed

Prassas, I., Eissa, A., Poda, G., and Diamandis, E.P. (2015). Unleashing the therapeutic potential of human kallikrein-related serine proteases. Nat. Rev. Drug Discov. 14, 183–202.10.1038/nrd4534Search in Google Scholar PubMed

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, 1072–1089.10.1097/NEN.0000000000000007Search in Google Scholar PubMed PubMed Central

Radulovic, M., Yoon, H., Wu, J., Mustafa, K., Fehlings, M.G., and Scarisbrick, I.A. (2015). Genetic targeting of protease activated receptor 2 reduces inflammatory astrogliosis and improves recovery of function after spinal cord injury. Neurobiol. Dis. 83, 75–89.10.1016/j.nbd.2015.08.021Search in Google Scholar PubMed PubMed Central

Radulovic, M., Yoon, H., Wu, J., Mustafa, K., and Scarisbrick, I.A. (2016). Targeting the thrombin receptor modulates inflammation and astrogliosis to improve recovery after spinal cord injury. Neurobiol. Dis. 93, 226–242.10.1016/j.nbd.2016.04.010Search in Google Scholar PubMed PubMed Central

Rajput, P.S., Lyden, P.D., Chen, B., Lamb, J.A., Pereira, B., Lamb, A., Zhao, L., Lei, I.F., and Bai, J. (2014). Protease activated receptor-1 mediates cytotoxicity during ischemia using in vivo and in vitro models. Neuroscience 281C, 229–240.10.1016/j.neuroscience.2014.09.038Search in Google Scholar PubMed PubMed Central

Ramachandran, R., Eissa, A., Mihara, K., Oikonomopoulou, K., Saifeddine, M., Renaux, B., Diamandis, E., and Hollenberg, M.D. (2012). Proteinase-activated receptors (PARs): differential signalling by kallikrein-related peptidases KLK8 and KLK14. Biol. Chem. 393, 421–427.10.1515/hsz-2011-0251Search in Google Scholar PubMed

Rohatgi, T., Henrich-Noack, P., Sedehizade, F., Goertler, M., Wallesch, C.W., Reymann, K.G., and Reiser, G. (2004). Transient focal ischemia in rat brain differentially regulates mRNA expression of protease-activated receptors 1 to 4. J. Neurosci. Res. 75, 273–279.10.1002/jnr.10847Search in Google Scholar PubMed

Sandberg, C.J., Altschuler, G., Jeong, J., Stromme, K.K., Stangeland, B., Murrell, W., Grasmo-Wendler, U.H., Myklebost, O., Helseth, E., Vik-Mo, E.O., et al. (2013). Comparison of glioma stem cells to neural stem cells from the adult human brain identifies dysregulated Wnt- signaling and a fingerprint associated with clinical outcome. Exp. Cell Res. 319, 2230–2243.10.1016/j.yexcr.2013.06.004Search in Google Scholar

Scarisbrick, I.A., Towner, M.D., and Isackson, P.J. (1996). Induction of serine proteases in the adult rat spinal cord following kainic acid administration. Soc. Neurosci. Abs. 22, 746.10.1016/0736-5748(96)80242-5Search in Google Scholar

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, 8156–8168.10.1523/JNEUROSCI.17-21-08156.1997Search in Google Scholar

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, 219–230.10.1002/(SICI)1098-1136(200005)30:3<219::AID-GLIA2>3.0.CO;2-2Search in Google Scholar

Scarisbrick, I.A. (2012). Kallikrein activity in the central nervous system. The Kallikreins. M. Schmitt, Sommerhoff, C., Fritz, H. and Magdolen, V. Berlin, De Gruyter Publishing: 349–372.Search in Google Scholar

Scarisbrick, I.A. and Blaber, M. (2012). Kallikrein-related peptidase 6. In: Handbook of proteolytic enzymes. A.J. Barrett and N.D. Rawlings, eds. (London, UK: Elsevier), pp. 2780–2786.10.1016/B978-0-12-382219-2.00612-8Search in Google Scholar

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, 1283–1296.10.1093/brain/awf142Search in Google Scholar

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. (2006). Dynamic role of kallikrein 6 in traumatic spinal cord injury. Eur. J. Neurosci 24, 1457–1469.10.1111/j.1460-9568.2006.05021.xSearch in Google Scholar

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, e18376.10.1371/journal.pone.0018376Search in Google Scholar

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, 355–367.10.1515/hsz-2011-0241Search in Google Scholar

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, 709–722.10.1111/j.1750-3639.2012.00577.xSearch in Google Scholar

Schrader, C.H., Kolb, M., Zaoui, K., Flechtenmacher, C., Grabe, N., Weber, K.J., Hielscher, T., Plinkert, P.K., and Hess, J. (2015). Kallikrein-related peptidase 6 regulates epithelial-to-mesenchymal transition and serves as prognostic biomarker for head and neck squamous cell carcinoma patients. Mol. Cancer 14, 107.10.1186/s12943-015-0381-6Search in Google Scholar PubMed PubMed Central

Shigetomi, E., Bowser, D.N., Sofroniew, M.V., and Khakh, B.S. (2008). Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J. Neurosci. 28, 6659–6663.10.1523/JNEUROSCI.1717-08.2008Search in Google Scholar PubMed PubMed Central

Silver, J. and Miller, J.H. (2004). Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146–156.10.1038/nrn1326Search in Google Scholar PubMed

Sotiropoulou, G. and Pampalakis, G. (2010). Kallikrein-related peptidases: bridges between immune functions and extracellular matrix degradation. Biol. Chem. 391, 321–331.10.1515/bc.2010.036Search in Google Scholar

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 alpha-synuclein and reduces the pathology in an alpha-synuclein model of LBD. Mol. Ther. 21, 31–41.10.1038/mt.2012.66Search in Google Scholar PubMed PubMed Central

Spencer, B., Valera, E., Rockenstein, E., Trejo-Morales, M., Adame, A., and Masliah, E. (2015). A brain-targeted, modified neurosin (kallikrein-6) reduces alpha-synuclein accumulation in a mouse model of multiple system atrophy. Mol. Neurodegener 10, 48.10.1186/s13024-015-0043-6Search in Google Scholar PubMed PubMed Central

Tatebe, H., Watanabe, Y., Kasai, T., Mizuno, T., Nakagawa, M., Tanaka, M., and Tokuda, T. (2010). Extracellular neurosin degrades α-synuclein in cultured cells. Neurosci. Res. 67, 341–346.10.1016/j.neures.2010.04.008Search in Google Scholar PubMed

Terayama, R., Bando, Y., Takahashi, T., and Yoshida, S. (2004). Differential expression of neuropsin and protease M/neurosin in oligodendrocytes after injury to the spinal cord. Glia 48, 91–101.10.1002/glia.20058Search in Google Scholar PubMed

Tong, X., Shigetomi, E., Looger, L.L., and Khakh, B.S. (2013). Genetically encoded calcium indicators and astrocyte calcium microdomains. Neuroscientist 19, 274–291.10.1177/1073858412468794Search in Google Scholar PubMed

Uchida, A., Oka, Y., Aoyama, M., Suzuki, S., Yokoi, T., Katano, H., Mase, M., Tada, T., Asai, K., and Yamada, K. (2004). Expression of myelencephalon-specific protease in transient middle cerebral artery occlusion model of rat brain. Brain Res. Mol. Brain Res. 126, 129–136.10.1016/j.molbrainres.2004.04.009Search in Google Scholar PubMed

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, 855–870.10.1111/j.1471-4159.2008.05658.xSearch in Google Scholar

Verkhratsky, A., Orkand, R.K., and Kettenmann, H. (1998). Glial calcium: homeostasis and signaling function. Physiol. Rev. 78, 99–141.10.1152/physrev.1998.78.1.99Search in Google Scholar

Wang, H., Ubl, J.J., and Reiser, G. (2002). Four subtypes of protease-activated receptors, co-expressed in rat astrocytes, evoke different physiological signaling. Glia 37, 53–63.10.1002/glia.10012Search in Google Scholar

Wang, H., Wen, S., Bunnett, N.W., Leduc, R., Hollenberg, M.D., and MacNaughton, W.K. (2008). Proteinase-activated receptor-2 induces cyclooxygenase-2 expression through β-catenin and cyclic AMP-response element-binding protein. J. Biol. Chem. 283, 809–815.10.1074/jbc.M703021200Search in Google Scholar

Yamashiro, K., Tsuruoka, N., Kodama, S., Tsujimoto, M., Yamamura, Y., Tanaka, T., Nakazato, H., and Yamaguchi, N. (1997). Molecular cloning of a novel trypsin-like serine protease (neurosin) preferentially expressed in brain. Biochim. Biophys. Acta 1350, 11–14.10.1016/S0167-4781(96)00187-XSearch in Google Scholar

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, 283–298.10.1111/jnc.12293Search in Google Scholar

Yoon, H., Walters, G., Paulsen, A.R., and Scarisbrick, I.A. (2017). Astrocyte heterogeneity across the brain and spinal cord occurs developmentally, in adulthood and in response to demyelination. PLoS One 12, e0180697.10.1371/journal.pone.0180697Search in Google Scholar

Yuan, Y.M. and He, C. (2013). The glial scar in spinal cord injury and repair. Neurosci Bull 29, 421–435.10.1007/s12264-013-1358-3Search in Google Scholar

Zarghooni, M., Soosaipillai, A., Grass, L., Scorilas, A., Mirazimi, N., and Diamandis, E. P. (2002). Decreased concentration of human kallikrein 6 in brain extracts of Alzheimer’s disease patients. Clin. Biochem. 35, 225–231.10.1016/S0009-9120(02)00292-8Search in Google Scholar