Serine proteases in the functional activity of the nervous system
https://doi.org/10.34680/2076-8052.2023.2(131).196-207
Abstract
Serine proteases, including trypsin, thrombin, plasminogen activators, plasmin and several others, are synthesized in nervous tissue, mainly in the brain, including the cortex, limbic system and cerebellum. This review examines the involvement of serine proteases in neuroplasticity and behavioral regulation. Endogenous serine proteases play an important role in the formation, development and maintenance of the nervous system. Through limited proteolysis, these proteases activate PARs (protease-activated receptors), modify other receptors or their ligands, process neurotrophic factors, degrade intercellular matrix and cell adhesion proteins and initiate complex signal transduction cascades necessary for structural modification of synapses. The involvement of serine proteases in morphological and functional synaptic plasticity may underlie cognitive processes, including learning and memory in animals and humans.
About the Authors
T. S. ZamolodchikovaRussian Federation
Zamolodchikova T. S.,
Moscow.
S. M. Tolpygo
Russian Federation
Tolpygo S. M.,
Moscow.
A. V. Kotov
Russian Federation
Kotov A. V.,
Veliky Novgorod.
References
1. Antonov V. K. Himiya proteoliza [Chemistry of proteolysis]. 2nd ed., rev. and add. Moscow, Nauka Publ., 1991. 503 p.
2. López-Otín C., Overall C. M. Protease degradomics: a new challenge for proteomics // Nature Reviews Molecular Cell BiologyNat. 2002. 3(7). 509-519. DOI: 10.1038/nrm858
3. Zamolodchikova T. S. Serinovye proteazy slizistoj tonkogo kishechnika — lokalizaciya, funkcional'nye svojstva, fiziologicheskaya rol' [Serine proteases of the small intestine mucosa – localization, functional properties, physiological role] // Biochemistry. 2012. 77(8). 989-1001. DOI: 10.1134/S0006297912080032
4. Almonte A. G., Sweatt J. D. Serine proteases, serine protease inhibitors, and protease-activated receptors: roles in synaptic function and behavior // Brain Reserch. 2011. 1407. 107-122. DOI: 10.1016/j.brainres.2011.06.042
5. Wang Y., Luo W., Reiser G. Trypsin and trypsin-like proteases in the brain: proteolysis and cellular functions // Cellblar and Molecular Life Sciences. 2008. 65(2). 237-252. DOI: 10.1007/s00018-007-7288-3
6. Semchenko V. V., Stepanov S. S., Bogolepov N. N. Sinapticheskaya plastichnost' golovnogo mozga: (fundamental'nye i prikladnye aspekty): monografiya [Synaptic plasticity of golovnaya mosga: (fundamental and adjacentarableve aspect): monograph]. Moscow, Direct-Media Publ., 2014. 498 p
7. Shiosaka S. Serine proteases regulating synaptic plasticity // Anatomical Science International. 2004. 79(3). 137-144. DOI: 10.1111/j.1447-073x.2004.00080.x
8. Dihanich M., Kaser M., Reinhard E., Cunningham D., Monard D. Prothrombin mRNA is expressed by cells of the nervous system // Neuron. 1991. 6(4). 575-581. DOI: 10.1016/0896-6273(91)90060-d
9. Teesalu T., Kulla A., Simisker A., Sirén V., Lawrence D. A., Asser T., Vaheri A. Tissue plasminogen activator and neuroserpin are widely expressed in the human central nervous system // Thrombosis and Haemostasis. 2004. 92(2). 358-368. DOI: 10.1160/TH02-12-0310
10. Shikamoto Y., Morita T. Expression of factor X in both the rat brain and cells of the central nervous system // FEBS Letters. 1999. 463(3). 387-389. DOI: 10.1016/s0014-5793(99)01657-9
11. Yahagi N., Ichinose M., Matsushima M., Matsubara Y., Miki K., Kurokawa K., Fukamachi H., Tashiro K., Shiokawa K., Kageyama T., Takahashi T., Inoue H., Takahashi R. Complementary DNA cloning and sequencing of rat enteropeptidase and tissue distribution of its Mrna // Biochemical and Biophysical Research Communications. 1996. 219(3). 806-812. DOI: 10.1006/bbrc.1996.0315
12. Sokolova E., Reiser G. Prothrombin/thrombin and the thrombin receptors PAR-1 and PAR-4 in the brain: localization, expression and participation in neurodegenerative diseases // Thrombosis and Haemostasis. 2008. 100(4). 576-581. DOI: 10.1160/th08-03-0131
13. Grabham P., Cunningham D. D. Thrombin receptor activation stimulates astrocyte proliferation and reversal of stellation by distinct pathways: involvement of tyrosine phosphorylation // Journal of Neurochemistry. 1995. 64(2). 583-591. DOI: 10.1046/j.1471-4159.1995.64020583.x
14. Gingrich M. B., Junge C. E., Lyuboslavsky P., Traynelis S. F. Potentiation of NMDA receptor function by the serine protease thrombin // Journal of Neuroscience. 2000. 20(12). 4582-4595. DOI: 10.1523/JNEUROSCI.20-12-04582.2000
15. Pang P. T., Teng H. K., Zaitsev E., Woo N. T., Sakata K., Zhen S., Teng K. K., Yung W.-H., Hempstead B. L., Lu B. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity // Science. 2004. 306(5695). 487-491. DOI: 10.1126/science.1100135
16. Tsilibary E., Tzinia A., Radenovic L., Stamenkovic V., Lebitko T., Mucha M., Pawlak R., Frischknecht R., Kaczmarek L. Neural ECM proteases in learning and synaptic plasticity // Progress in Brain Resarch. 2014. 214. 135-157. DOI: 10.1016/B978-0-444-63486-3.00006-2
17. Yuan H., Vance K. M., Junge C. E., Geballe M. T., Snyder J. P., Hepler J. R., Yepes M., Low C. M., Traynelis S. F. The serine protease plasmin cleaves the amino-terminal domain of the NR2A subunit to relieve zinc inhibition of the N-methyl-D-aspartate receptors // Journal of Biological Chemistry. 2009. 284(19). 2862-12873. DOI: 10.1074/jbc.M805123200
18. Nagai K., Fujii M., Kitazume S. Protein Tyrosine Phosphatase Receptor Type Z in Central Nervous System Disease // International Journal of Molecular Sciences. 2022. 23(4). 4414. DOI: 10.3390/ijms23084414
19. Medveczky P., Antal J., Patthy A., Kekesi K., Juhasz G., Szilagyi L., Graf L. Myelin basic protein, an autoantigen in multiple sclerosis, is selectively processed by human trypsin 4 // FEBS Letttrs. 2006. 580(2). 545-552. DOI: 10.1016/j.febslet.2005.12.067
20. Tamura H., Kawata M., Hamaguchi S., Ishikawa Y., Shiosaka S. Processing of neuregulin-1 by neuropsin regulates GABAergic neuron to control neural plasticity of the mouse hippocampus // Journal Neuroscience. 2012. 32(37). 12657-12672. DOI: 10.1523/JNEUROSCI.2542-12.2012
21. Attwood B. K., Bourgognon J. M., Patel S., Mucha M., Schiavon E., Skrzypiec A. E., Young K. W., Shiosaka S., Korostynski M., Piechota M., Przwelocki R., Pawlak R. Neuropsin cleaves EphB2 in the amygdala to control anxiety // Nature. 2011. 473. 372-375. DOI: 10.1038/nature09938
22. Reif R., Sales S., Hettwer S., Dreier B., Gisler C., Wölfel J., Lüscher D., Zurlinden A., Stephan A., Ahmed S., Baici A., Ledermann B., Kunz B., Sonderegger P. Specific cleavage of agrin by neurotrypsin, a synaptic protease linked to mental retardation // FASEB Journal. 2007. 21(13). 3468-3478. DOI: 10.1096/fj.07-8800com
23. Turgeon V. L., Houenou L. J. The role of thrombin-like (serine) proteases in the development, plasticity and pathology of the nervous system // Brain Research Reviews. 1997. 25(1). 85-95. DOI: 10.1016/s0165-0173(97)00015-5
24. Almonte A. G., Hamill C. E., Chhatwal J. P., Wingo T. S., Barber J. A., Lyuboslavsky P. N., Sweatt D. J., Ressler K. J., White D. A., Traynelis S. F. Learning and memory deficits in mice lacking protease activated receptor-1 // Neurobiology of Learning and Memory. 2007. 88(3). 295-304. DOI: 10.1016/j.nlm.2007.04.004
25. ohman R. J., Jones N. C., O'Brien T. J., Cocks T. M. A regulatory role for protease-activated receptor-2 in motivational learning in rats. Neurobiology of Learning and emory // 2009. 92(3). 301-309. DOI: 10.1016/j.nlm.2009.03.010
26. Maggio N., Shavit E., Chapman J., Segal M. Thrombin induces long-term potentiation of reactivity to afferent stimulation and facilitates epileptic seizures in rat hippocampal slices: toward understanding the functional consequences of cerebrovascular insults // Journal of Neuroscience. 2008. 28(3). 32-36. DOI: 10.1523/JNEUROSCI.3665-07.2008
27. Mhatre M., Nguyen A., Kashani S., Pham T., Adesina A., Grammas P. Thrombin, a mediator of neurotoxicity and memory impairment // Neurobiology of Aging. 2004. 25(6). 783-793. DOI: 10.1016/j.neurobiolaging.2003.07.007
28. Calabresi P., Napolitano M., Centonze D., Marfia G. A., Gubellini P., Teule M. A., Berretta N., Bernardi G., Frati L., Tolu M., Gulino A. Tissue plasminogen activator controls multiple forms of plasticity and memory // European Journal of Neuroscience. 2000. 12(3). 1002-1012. DOI: 10.1046/j.1460-9568.2000.00991.x
29. Pawlak R., Magarinos A.M., Melchor J., McEwen B., Strickland S. Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior // Nature Neuroscience. 2003. 6(3). 168-174. DOI: 10.1038/nn998
30. Nakagami Y., Abe K., Nishiyama N., Matsuke N. Laminin degradation by plasmin regulates long-term potentiation // Journal of Neuroscience. 2000. 20(5). 2003-2010. DOI: 10.1523/JNEUROSCI.20-05-02003.2000
31. Nagai T., Kamei H., Ito M., Hashimoto K., Takuma K., Nabeshima T., Yamada K. Modification by the tissue plasminogen activator-plasmin system of morphine-induced dopamine release and hyperlocomotion, but not anti-nociceptive effect in mice // Journal of Neurochemistry. 2005. 93(5). 1272-1279. DOI: 10.1111/j.1471-4159.2005.03117.x
32. Kawashita E., Kanno Y., Ikeda K., Kuretake H., Matsuo O., Matsuno H. Altered behavior in mice with deletion of the alpha2-antiplasmin gene // PLoS One. 2014. 9(5). e97947. DOI: 10.1371/journal.pone.0097947
33. Tamura H., Ishikawa Y., Shiosaka S. Does extracellular proteolysis control mammalian cognition? // Nature Reviews Neuroscience. 2013. 24(4). 365-374. DOI: 10.1515/revneuro-2013-0007
Review
For citations:
Zamolodchikova T.S., Tolpygo S.M., Kotov A.V. Serine proteases in the functional activity of the nervous system. Title in english. 2023;(2(131)):196-207. (In Russ.) https://doi.org/10.34680/2076-8052.2023.2(131).196-207