Protease-activated receptors in neuronal development, neurodegeneration, and neuroprotection: Thrombin as signaling molecule in the brain

Neuroscientist

Volumn 10, Issue 6, 2004, Pages 501-512

  Rohatgi, Tanuja ^a   Sedehizade, Fariba ^a   Reymann, Klaus G ^b   Reiser, Georg ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Alzheimer's disease; CNS; Cytoprotection; G protein coupled receptor; Neurodegenerative disorders; Protease activated receptor; Serine protease; Stroke; Thrombin

Indexed keywords

BRAIN RECEPTOR; G PROTEIN COUPLED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; SERINE PROTEINASE; THROMBIN;

AMINO TERMINAL SEQUENCE; CELL DEATH; CELL FUNCTION; CELL SURVIVAL; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONCENTRATION RESPONSE; CYTOTOXICITY; DEGENERATIVE DISEASE; DRUG BLOOD LEVEL; LIGAND BINDING; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; NEUROPROTECTION; PATHOPHYSIOLOGY; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STROKE;

ANIMALS; BRAIN; CELL DIFFERENTIATION; HUMANS; NEURODEGENERATIVE DISEASES; NEURONS; NEUROPROTECTIVE AGENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PROTEINASE-ACTIVATED; SIGNAL TRANSDUCTION; THROMBIN;

EID: 9144238400     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858404269955     Document Type: Review

References (75)

1. Böhm SK, Khitin LM, Grady EF, Aponte G, Payan DG, Bunnett NW. 1996. Mechanisms of desensitization and resensitization of proteinase-activated receptor-2. J Biol Chem 271:22003-16.
2. Böhm SK, Kong W, Bromme D, Smeekens SP, Anderson DC, Connolly A, and others. 1996. Molecular cloning, expression and potential functions of the human proteinase-activated receptor-2. Biochem J 314:1009-16.
3. Boven LA, Vergnolle N, Henry SD, Silva C, Imai Y, Holden J, and others. 2003. Up-regulation of proteinase-activated receptor I expression in astrocytes during HIV encephalitis. J Immunol 170:2638-46.
4. Carreno-Muller E, Herrera AJ, de Pablos RM, Tomas-Camardiel M, Venero JL, Cano J, and others. 2003. Thrombin induces in vivo degeneration of nigral dopaminergic neurones along with the activation of microglia. J Neurochem 84:1201-14.
5. Cavanaugh KP, Gurwitz D, Cunningham DD, Bradshaw RA. 1990. Reciprocal modulation of astrocyte stellation by thrombin and protease nexin-1. J Neurochem 54:1735-43.
6. Chambers RC, Dabbagh K, McAnulty RJ, Gray AJ, Blanc-Brude OP, Laurent GJ. 1998. Thrombin stimulates fibroblast procollagen production via proteolytic activation of protease-activated receptor 1. Biochem J 333:121-7.
7. Choi SH, Joe EH, Kim SU, Jin BK. 2003. Thrombin-induced microglial activation produces degeneration of nigral dopaminergic neurons in vivo. J Neurosci 23:5877-86.
8. Choi SH, Lee da Y, Ryu JK, Kim J, Joe EH, Jin BK. 2003. Thrombin induces nigral dopaminergic neurodegeneration in vivo by altering expression of death-related proteins. Neurobiol Dis 14:181-93.
9. Coughlin S. 2000. Thrombin signalling and protease-activated receptors. Nature 407:258-64.
10. Cunningham DD, Donovan FM. 1997. Regulation of neurons and astrocytes by thrombin and protease nexin-1. Relationship to brain injury. Adv Exp Med Biol 425:67-75.
11. Damiano BP, D'Andrea MR, de Garavilla L, Cheung WM, Andrade-Gordon P. 1999. Increased expression of protease activated receptor-2 (PAR-2) in balloon-injured rat carotid artery. Thromb Haemost 81:808-14.
12. D'Andrea MR, Derian CK, Leturcq D, Baker SM, Brunmark A, Ling P, and others. 1998. Characterization of protease-activated receptor-2 immunoreactivity in normal human tissues. J Histochem Cytochem 46:157-64.
13. D'Andrea MR, Saban MR, Nguyen NB, Andrade-Gordon P, Saban R. 2003. Expression of protease-activated receptor-1, -2, -3, and -4 in control and experimentally inflamed mouse bladder. Am J Pathol 162:907-23.
14. Dery O, Thoma MS, Wong H, Grady EF, Bunnett NW. 1999. Trafficking of proteinase-activated receptor-2 and beta-arrestin-I tagged with green fluorescent protein. beta-Arrestin-dependent endocytosis of a proteinase receptor. J Biol Chem 274:18524-35.
15. Donovan FM, Cunningham DD. 1998. Signaling pathways involved in thrombin-induced cell protection. J Biol Chem 273:12746-52.
16. Donovan FM, Pike CJ, Cotman CW, Cunningham DD. 1997. Thrombin induces apoptosis in cultured neurons and astrocytes via a pathway requiring tyrosine kinase and RhoA activities. J Neurosci 17:5316-26.
17. Ehrenreich H, Costa T, Clouse KA, Pluta RM, Ogino Y, Coligan JE, and others. 1993. Thrombin is a regulator of astrocytic endothelin-1. Brain Res 600:201-7.
18. Fang M, Kovacs KJ, Fisher LL, Larson AA. 2003. Thrombin inhibits NMDA-mediated nociceptive activity in the mouse: possible mediation by endothelin. J Physiol 549:903-17.
19. Festoff BW, Smirnova IV, Ma J, Citron BA. 1996. Thrombin, its receptor and protease nexin I, its potent serpin, in the nervous system. Semin Thromb Hemost 22:267-71.
20. Friedmann I, Faber-Elman A, Yoles E, Schwartz M. 1999. Injury-induced gelatinase and thrombin-like activities in regenerating and nonregenerating nervous systems. FASEB J 13:533-43.
21. Friedmann I, Yoles E, Schwartz M. 2001. Thrombin attenuation is neuroprotective in the injured rat optic nerve. J Neurochem 76:641-9.
22. Griffin JH, Fernandez JA, Liu D, Cheng T, Guo H, Zlokovic BV. 2004. Activated protein C and ischemic stroke. Crit Care Med 32:S247-53.
23. Hollenberg MD, Laniyonu AA, Saifeddine M, Moore GJ. 1993. Role of the amino- and carboxyl-terminal domains of thrombin receptor-derived polypeptides in biological activity in vascular endothelium and gastric smooth muscle: evidence for receptor subtypes. Mol Pharmacol 43:921-30.
24. Hollenberg MD, Saifeddine M, al-Ani B, Kawabata A. 1997. Proteinase-activated receptors: structural requirements for activity, receptor cross-reactivity, and receptor selectivity of receptor-activating peptides. Can J Physiol Pharmacol 75:832-41.
25. Ishihara H, Connolly AJ, Zeng D, Kahn ML, Zheng YW, Timmons C, and others. 1997. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature 386:502-6.
26. Jalink K, Moolenaar WH. 1992. Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. J Cell Biol 118:411-9.
27. Jenkins AL, Chinni C, De Niese MR, Blackhart B, Mackie EJ. 2000. Expression of protease-activated receptor-2 during embryonic development. Dev Dyn 218:465-71.
28. Junge CE, Sugawara T, Mannaioni G, Alagarsamy S, Conn PJ, Brat DJ, and others. 2003. The contribution of protease-activated receptor I to neuronal damage caused by transient focal cerebral ischemia. Proc Natl Acad Sci U S A 100:13019-24.
29. Kahn ML, Hammes SR, Botka C, Coughlin SR. 1998. Gene and locus structure and chromosomal localization of the protease-activated receptor gene family. J Biol Chem 273:23290-6.
30. Kawabata A, Saifeddine M, Al-Ani B, Leblond L, Hollenberg MD. 1999. Evaluation of proteinase-activated receptor-1 (PAR1 ) agonists and antagonists using a cultured cell receptor desensitization assay: activation of PAR2 by PAR1-targeted ligands. J Pharmacol Exp Ther 288:358-70.
31. Knight DA, Lim S, Scaffidi AK, Roche N, Chung KF, Stewart GA, and others. 2001. Protease-activated receptors in human airways: upregulation of PAR-2 in respiratory epithelium from patients with asthma. J Allergy Clin Immunol 108:797-803.
32. 2+-induced regulation of ion channel and MAP kinase functions. Nature 376:737-45.
33. Mahajan VB, Pai KS, Lau A, Cunningham DD. 2000. Creatine kinase, an ATP-generating enzyme, is required for thrombin receptor signaling to the cytoskeleton. Proc Natl Acad Sci U S A 97:12062-7.
34. Miller S, Sehati N, Romano C, Cotman CW. 1996. Exposure of astrocytes to thrombin reduces levels of the metabotropic glutamate receptor mGluR5. J Neurochem 67:1435-47.
35. Molino M, Barnathan ES, Numerof R, Clark J, Dreyer M, Cumashi A, and others. 1997. Interactions of mast cell tryptase with thrombin receptors and PAR-2. J Biol Chem 272:4043-9.
36. Niclou SP, Suidan HS, Pavlik A, Vejsada R, Monard D. 1998. Changes in the expression of protease-activated receptor 1 and protease nexin-1 mRNA during rat nervous system development and after nerve lesion. Eur J Neurosci 10:1590-607.
37. Nystedt S, Emilsson K, Wahlestedt C, Sundelin J. 1994. Molecular cloning of a potential proteinase activated receptor. Proc Natl Acad Sci U S A 91:9208-12.
38. Pai KS, Cunningham DD. 2002. Geldanamycin specifically modulates thrombin-mediated morphological changes in mouse neuroblasts. J Neurochem 80:715-8.
39. Pai KS, Mahajan VB, Lau A, Cunningham DD. 2001. Thrombin receptor signaling to cytoskeleton requires Hsp90. J Biol Chem 276:32642-7.
40. Paing MM, Stutts AB, Kohout TA, Lefkowitz RJ, Trejo J. 2002. beta-Arrestins regulate protease-activated receptor-1 desensitization but not internalization or Down-regulation. J Biol Chem 277:1292-300. Epub 2001 Nov 2.
41. Pike CJ, Vaughan PJ, Cunningham DD, Cotman CW. 1996. Thrombin attenuates neuronal cell death and modulates astrocyte reactivity induced by beta-amyloid in vitro. J Neurochem 66:1374-82.
42. Rohatgi T, Henrich-Noack P, Sedehizade F, Goertler M, Wallesch CW, Reymann KG, and others. 2004. Transient focal ischemia in rat brain differentially regulates mRNA expression of protease-activated receptors 1 to 4. J Neurosci Res 75:273-9.
43. Rohatgi T, Sedehizade F, Sabel BA, Reiser G. 2003. Protease-activated receptor subtype expression in developing eye and adult retina of the rat after optic nerve crush. J Neurosci Res 73:246-54.
44. Schultheiss M, Neumcke B, Richter HP. 1997. Endogenous trypsin receptors in Xenopus oocytes: linkage to internal calcium stores. Cell Mol Life Sci 53:842-9.
45. Seatter MJ, Drummond R, Kanke T, Macfarlane SR, Hollenberg MD, Plevin R. 2004. The role of the C-terminal tail in protease-activated receptor-2-mediated Ca2+ signalling, proline-rich tyrosine kinase-2 activation, and mitogen-activated protein kinase activity. Cell Signal 16:21-9.
46. 2+ response in rat astrocytes by endogenous arachidonic acid liberation. J Neurochem 82:1252-61.
47. Sinnreich M, Meins M, Niclou SP, Suidan HS, Monard D. 2004. Prothrombin overexpressed in post-natal neurones requires blood factors for activation in the mouse brain. J Neurochem 88:1380-8.
48. Smith-Swintosky VL, Cheo-Isaacs CT, D'Andrea MR, Santulli RJ, Darrow AL, Andrade-Gordon P. 1997. Protease-activated receptor-2 (PAR-2) is present in the rat hippocampus and is associated with neurodegeneration. J Neurochem 69:1890-6.
49. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS, and others. 2000. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nature Med 6:151-8.
50. Striggow F, Riek M, Breder J, Henrich-Noack P, Reymann KG, Reiser G. 2000. The protease thrombin is an endogenous mediator of hippocampal neuroprotection against ischemia at low concentrations but causes degeneration at high concentrations. Proc Natl Acad Sci U S A 97:2264-9.
51. Striggow F, Riek-Burchardt M, Kiesel A, Schmidt W, Henrich-Noack P, Breder J, and others. 2001. Four different types of protease-activated receptors are widely expressed in the brain and are upregulated in hippocampus by severe ischemia. Eur J Neurosci 14:595-608.
52. 2+. Br J Pharmacol 139:1014-22.
53. Suidan HS, Bouvier J, Schaerer E, Stone SR, Monard D, Tschopp J. 1994. Granzyme A released upon stimulation of cytotoxic T lymphocytes activates the thrombin receptor on neuronal cells and astrocytes. Proc Natl Acad Sci U S A 91:8112-6.
54. Suo Z, Wu M, Ameenuddin S, Anderson HE, Zoloty JE, Citron BA, and others. 2002. Participation of protease-activated receptor-I in thrombin-induced microglial activation. J Neurochem 80:655-66.
55. Suo Z, Wu M, Citron BA, Gao C, Festoff BW. 2003. Persistent protease-activated receptor 4 signaling mediates thrombin-induced microglial activation. J Biol Chem 278:31177-83.
56. Suo Z, Wu M, Citron BA, Palazzo RE, Festoff BW. 2003. Rapid tau aggregation and delayed hippocampal neuronal death induced by persistent thrombin signaling. J Biol Chem 278:37681-9.
57. Trejo J, Chambard JC, Karin M, Brown JH. 1992. Biphasic increase in c-jun mRNA is required for induction of AP-1-mediated gene transcription: differential effects of muscarinic and thrombin receptor activation. Mol Cell Biol 12:4742-50.
58. Trejo J, Coughlin SR. 1999. The cytoplasmic tails of protease-activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J Biol Chem 274:2216-24.
59. Turgeon VL, Lloyd ED, Wang S, Festoff BW, Houenou LJ. 1998. Thrombin perturbs neurite outgrowth and induces apoptotic cell death in enriched chick spinal motoneuron cultures through caspase activation. J Neurosci 18:6882-91.
60. 2+ signalling evoked by the tethered ligand. J Physiol 525:319-30.
61. i-inducing protease-activated receptors (PAR-1 and PAR-2) in rat astrocytes and C6 glioma cells. Neuroscience 86:597-609.
62. Vaughan PJ, Pike CJ, Cotman CW, Cunningham DD. 1995. Thrombin receptor activation protects neurons and astrocytes from cell death produced by environmental insults. J Neurosci 15:5389-401.
63. Vergnolle N, Derian CK, D'Andrea MR, Steinhoff M, Andrade-Gordon P. 2002. Characterization of thrombin-induced leukocyte rolling and adherence: a potential proinflammatory role for proteinase-activated receptor-4. J Immunol 169:1467-73.
64. Vergnolle N, Wallace JL, Bunnett NW, Hollenberg MD. 2001. Protease-activated receptors in inflammation, neuronal signaling and pain. Trends Pharmacol Sci 22:146-52.
65. Vu TK, Hung DT, Wheaton VI, Coughlin SR. 1991. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64:1057-68.
66. 2+-sensitive tyrosine kinase Pyk2 and Src in thrombin signalling in rat astrocytes. J Neurochem 84:1349-57.
67. Wang H, Ubl JJ, Reiser G. 2002. Four subtypes of protease-activated receptors, co-expressed in rat astrocytes, evoke different physiological signaling. Glia 37:53-63.
68. Wang H, Ubl JJ, Stricker R, Reiser G. 2002. Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways. Am J Physiol Cell Physiol 283:C1351-64.
69. Wang Y, Richter-Landsberg C, Reiser G. 2004. Expression of protease-activated receptors (PARs) in OLN-93 oligodendroglial cells and mechanism of PAR-1-induced calcium signaling. Neuroscience 126:69-82.
70. Weinstein JR, Gold SJ, Cunningham DD, Gall CM. 1995. Cellular localization of thrombin receptor mRNA in rat brain: expression by mesencephalic dopaminergic neurons and codistribution with prothrombin mRNA. J Neurosci 15:2906-19.
71. Weinstein JR, Lau AL, Brass LF, Cunningham DD. 1998. Injury-related factors and conditions down-regulate the thrombin receptor (PAR-1) in a human neuronal cell line. J Neurochem 71:1034-50.
72. Xi G, Keep RF, Hua Y, Xiang J, Hoff JT. 1999. Attenuation of thrombin-induced brain edema by cerebral thrombin preconditioning. Stroke 30:1247-55.
73. Xi G, Reiser G, Keep RF. 2003. The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury: deleterious or protective? J Neurochem 84:3-9.
74. Xu WF, Andersen H, Whitmore TE, Presnell SR, Yee DP, Ching A, and others. 1998. Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci U S A 95:6642-6.
75. Yu Z, Ahmad S, Schwartz JL, Banville D, Shen SH. 1997. Protein-tyrosine phosphatase SHP2 is positively linked to proteinase-activated receptor 2-mediated mitogenic pathway. J Biol Chem 272:7519-24.