Protease activated receptor-1 mediates cytotoxicity during ischemia using in vivo and in vitro models

Neuroscience

Volumn 281, Issue , 2014, Pages 229-240

  Rajput, P S ^a   Lyden, P D ^a   Chen, B ^a,b   Lamb, J A ^a   Pereira, B ^a   Lamb, A ^a   Zhao, L ^a   Lei, I F ^a   Bai, J ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b MCKINSEY AND COMPANY   (United States)

Author keywords

Cerebral ischemia; Lentivirus knock down; Oxygen glucose deprivation; Protease activated receptor 1; Thrombin

Indexed keywords

PROTEIN C FOS; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; SHORT HAIRPIN RNA; THROMBIN;

AGE; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN INFARCTION; BRAIN ISCHEMIA; CAUDATE NUCLEUS; CELL HYPOXIA; CONTROLLED STUDY; CYTOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; JUVENILE ANIMAL; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; ANIMAL; CELL CULTURE; CEREBRAL ARTERY DISEASE; COMPLICATION; DISEASE MODEL; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; SPRAGUE DAWLEY RAT; TRANSGENIC RAT;

ANIMALS; ASTROCYTES; BRAIN ISCHEMIA; CAUDATE NUCLEUS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; MICE, KNOCKOUT; NEURONS; NEUROPROTECTION; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RECEPTOR, PAR-1; THROMBIN;

EID: 84908193645     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.09.038     Document Type: Article

References (42)

1. Adams H.P., Effron M.B., Torner J., Davalos A., Frayne J., Teal P., Leclerc J., Oemar B., Padgett L., Barnathan E.S., Hacke W. Emergency administration of abciximab for treatment of patients with acute ischemic stroke: results of an international phase III trial: Abciximab in Emergency Treatment of Stroke Trial (AbESTT-II). Stroke 2008, 39:87-99.
2. Ames A., Wright R.L., Kowada M., Thurston J.M., Majno G. Cerebral ischemia. II. The no-reflow phenomenon. Am J Pathol 1968, 52:437.
3. Bederson J.B., Pitts L.H., Tsuji M., Nishimura M.C., Davis R.L., Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 1986, 17:472-476.
4. Biller J., Massey E.W., Marler J.R., Adams H.P. A dose escalation study of ORG 10172 (low molecular weight heparinoid) in stroke. Neurology 1989, 39:262.
5. Cavanaugh K.P., Gurwitz D., Cunningham D.D., Bradshaw R.A. Reciprocal modulation of astrocyte stellation by thrombin and protease nexin-1. J Neurochem 1990, 54:1735-1743.
6. Chen B., Cheng Q., Yang K., Lyden P.D. Thrombin mediates severe neurovascular injury during ischemia. Stroke 2010, 41:2348-2352.
7. Chen B., Friedman B., Cheng Q., Tsai P., Schim E., Kleinfeld D., Lyden P.D. Severe blood-brain barrier disruption and surrounding tissue injury. Stroke 2009, 40:e666-e674.
8. Chen B., Friedman B., Whitney M.A., Winkle J.A., Lei I.F., Olson E.S., Cheng Q., Pereira B., Zhao L., Tsien R.Y., Lyden P.D. Thrombin activity associated with neuronal damage during acute focal ischemia. J Neurosci 2012, 32:7622-7631.
9. Coughlin S.R. Thrombin signalling and protease-activated receptors. Nature 2000, 407:258-264.
10. Davalos D., Baeten K.M., Whitney M.A., Mullins E.S., Friedman B., Olson E.S., Ryu J.K., Smirnoff D.S., Petersen M.A., Bedard C., Degen J.L., Tsien R.Y., Akassoglou K. Early detection of thrombin activity in neuroinflammatory disease. Ann Neurol 2014, 75:303-308.
11. Donovan F.M., Pike C.J., Cotman C.W., Cunningham D.D. Thrombin induces apoptosis in cultured neurons and astrocytes via a pathway requiring tyrosine kinase and RhoA activities. J Neurosci 1997, 17:5316-5326.
12. Fisher M., Feuerstein G., Howells D.W., Hurn P.D., Kent T.A., Savitz S.I., Lo E.H. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009, 40:2244-2250.
13. Gingrich M.B., Junge C.E., Lyuboslavsky P., Traynelis S.F. Potentiation of NMDA receptor function by the serine protease thrombin. J Neurosci 2000, 20:4582-4595.
14. Gingrich M.B., Traynelis S.F. Serine proteases and brain damage - is there a link?. Trends Neurosci 2000, 23:399-407.
15. Gordon D.L., Linhardt R., Adams H.P. Low-molecular-weight heparins and heparinoids and their use in acute or progressing ischemic stroke. Clin Neuropharmacol 1990, 13:522.
16. Grabham P., Cunningham D.D. Thrombin receptor activation stimulates astrocyte proliferation and reversal of stellation by distinct pathways: involvement of tyrosine phosphorylation. J Neurochem 1995, 64:583-591.
17. Gurwitz D., Cunningham D.D. Thrombin modulates and reverses neuroblastoma neurite outgrowth. Proc Natl Acad Sci USA 1988, 85:3440-3444.
18. Hollenberg M.D., Compton S.J. International union of pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev 2002, 54:203-217.
19. Hu E., Mueller E., Oliviero S., Papaioannou V.E., Johnson R., Spiegelman B.M. Targeted disruption of the c-fos gene demonstrates c-fos-dependent and -independent pathways for gene expression stimulated by growth factors or oncogenes. EMBO J 1994, 13:3094-3103.
20. Junge C.E., Sugawara T., Mannaioni G., Alagarsamy S., Conn P.J., Brat D.J., Chan P.H., Traynelis S.F. The contribution of protease-activated receptor 1 to neuronal damage caused by transient focal cerebral ischemia. Proc Natl Acad Sci USA 2003, 100:13019-13024.
21. Lapchak P.A., Zhang J.H., Noble-Haeusslein L.J. RIGOR guidelines: escalating STAIR and STEPS for effective translational research. Trans Stroke Res 2013, 4:279-285.
22. Lee K.R., Colon G.P., Betz A.L., Keep R.F., Kim S., Hoff J.T. Edema from intracerebral hemorrhage: the role of thrombin. J Neurosurg 1996, 84:91-96.
23. Lee K.R., Drury I., Vitarbo E., Hoff J.T. Seizures induced by intracerebral injection of thrombin: a model of intracerebral hemorrhage. J Neurosurg 1997, 87:73-78.
24. Liu J., Schuff-Werner P., Steiner M. Double transfection improves small interfering RNA-induced thrombin receptor (PAR-1) gene silencing in DU 145 prostate cancer cells. FEBS Lett 2004, 577:175-180.
25. Liu J., Schuff-Werner P., Steiner M. Thrombin/thrombin receptor (PAR-1)-mediated induction of IL-8 and VEGF expression in prostate cancer cells. Biochem Biophys Res Commun 2006, 343:183-189.
26. Lyden P., Levy H., Weymer S., Pryor K., Kramer W., Griffin J.H., Davis T.P., Zlokovic B. Phase 1 safety, tolerability and pharmacokinetics of 3K3A-APC in healthy adult volunteers. Curr Pharm Des 2013, 19:7479-7485.
27. Lyden P., Pereira B., Chen B., Zhao L., Lamb J., Lei I.F., Rajput P. Direct thrombin inhibitor argatroban reduces stroke damage in 2 different models. Stroke 2014, 45:896-899.
28. Macfarlane S.R., Seatter M.J., Kanke T., Hunter G.D., Plevin R. Proteinase-activated receptors. Pharmacol Rev 2001, 53:245-282.
29. Mao Y., Zhang M., Tuma R.F., Kunapuli S.P. Deficiency of PAR4 attenuates cerebral ischemia/reperfusion injury in mice. J Cereb Blood Flow Metab 2010, 30:1044-1052.
30. Rohatgi T., Sedehizade F., Reymann K.G., Reiser G. Protease-activated receptors in neuronal development, neurodegeneration, and neuroprotection: thrombin as signaling molecule in the brain. Neuroscientist 2004, 10:501-512.
31. Sarker K.P., Abeyama K., Nishi J., Nakata M., Tokioka T., Nakajima T., Kitajima I., Maruyama I. Inhibition of thrombin-induced neuronal cell death by recombinant thrombomodulin and E5510, a synthetic thrombin receptor signaling inhibitor. Thromb Haemost 1999, 82:1071-1077.
32. Sharp F.R., Sagar S.M. Alterations in gene expression as an index of neuronal injury: heat shock and the immediate early gene response. Neurotoxicology 1994, 15:51-59.
33. Shibata M., Kumar S.R., Amar A., Fernandez J.A., Hofman F., Griffin J.H., Zlokovic B.V. Anti-inflammatory, antithrombotic, and neuroprotective effects of activated protein C in a murine model of focal ischemic stroke. Circulation 2001, 103:1799-1805.
34. Striggow F., Riek M., Breder J., Henrich-Noack P., Reymann K.G., Reiser G. 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 USA 2000, 97:2264-2269.
35. Van Winkle J.A., Chen B., Lei I.F., Pereira B., Rajput P.S., Lyden P.D. Concurrent middle cerebral artery occlusion and intra-arterial drug infusion via ipsilateral common carotid artery catheter in the rat. J Neurosci Meth 2012, 213:63-69.
36. Villares G.J., Zigler M., Wang H., Melnikova V.O., Wu H., Friedman R., Leslie M.C., Vivas-Mejia P.E., Lopez-Berestein G., Sood A.K., Bar-Eli M. Targeting melanoma growth and metastasis with systemic delivery of liposome-incorporated protease-activated receptor-1 small interfering RNA. Cancer Res 2008, 68:9078-9086.
37. Vu T.K., Hung D.T., Wheaton V.I., Coughlin S.R. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 1991, 64:1057-1068.
38. Wang Y., Zhang Z., Chow N., Davis T.P., Griffin J.H., Chopp M., Zlokovic B.V. An activated protein C analog with reduced anticoagulant activity extends the therapeutic window of tissue plasminogen activator for ischemic stroke in rodents. Stroke 2012, 43:2444-2449.
39. Wang Y., Zhao Z., Chow N., Rajput P.S., Griffin J.H., Lyden P.D., Zlokovic B.V. Activated protein C analog protects from ischemic stroke and extends the therapeutic window of tissue-type plasminogen activator in aged female mice and hypertensive rats. Stroke 2013, 44:3529-3536.
40. Weinstein J.R., Lau A.L., Brass L.F., Cunningham D.D. Injury-related factors and conditions down-regulate the thrombin receptor (PAR-1) in a human neuronal cell line. J Neurochem 1998, 71:1034-1050.
41. Xi G., Reiser G., Keep R.F. The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury: deleterious or protective?. J Neurochem 2003, 84:3-9.
42. Zhang J., Wang Y., Zhu P., Wang X., Lv M., Feng H. SiRNA-mediated silence of protease-activated receptor-1 minimizes ischemic injury of cerebral cortex through HSP70 and MAP2. J Neurological Sci 2012, 320:6-11.