Activated protein C analog promotes neurogenesis and improves neurological outcome after focal ischemic stroke in mice via protease activated receptor 1

Brain Research

Volumn 1507, Issue , 2013, Pages 97-104

  Wang, Yaoming ^a,b   Zhao, Zhen ^a   Chow, Nienwen ^c   Ali, Tracy ^c   Griffin, John H ^d   Zlokovic, Berislav V ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c ZZ Biotech LLC   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

3K3A APC; Neurogenesis; Neuroprotection; Protease activated receptor 1; Stroke

Indexed keywords

3K3A APC; ACTIVATED PROTEIN C; NEUROPROTECTIVE AGENT; PROTEINASE ACTIVATED RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; CORPUS CALLOSUM; CORRELATION ANALYSIS; DRUG EFFECT; DRUG EFFICACY; FUNCTIONAL STATUS; LOCOMOTION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SUBVENTRICULAR ZONE;

ANIMALS; BRAIN ISCHEMIA; INFARCTION, MIDDLE CEREBRAL ARTERY; LOCOMOTION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGENESIS; NEUROPROTECTIVE AGENTS; PROTEIN C; RECEPTOR, PAR-1; RECOMBINANT PROTEINS; RECOVERY OF FUNCTION; STROKE;

MURINAE; MUS;

EID: 84875873977     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.02.023     Document Type: Article

References (44)

1. E. Candelario-Jalil, D. Alvarez, A. González-Falcón, M. García-Cabrera, G. Martínez-Sánchez, N. Merino, A. Giuliani, and O.S. León Neuroprotective efficacy of nimesulide against hippocampal neuronal damage following transient forebrain ischemia Eur. J. Pharmacol. 453 2002 189 195
2. J. Chen, Z.G. Zhang, Y. Li, Y. Wang, L. Wang, H. Jiang, C. Zhang, M. Lu, M. Katakowski, C.S. Feldkamp, and M. Chopp Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke Ann. Neurol. 53 2003 743 751
3. T. Cheng, D. Liu, J.H. Griffin, J.A. Fernández, F. Castellino, E.D. Rosen, K. Fukudome, and B.V. Zlokovic Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective Nat. Med. 9 2003 338 342
4. T. Cheng, A.L. Petraglia, Z. Li, M. Thiyagarajan, Z. Zhong, Z. Wu, D. Liu, S.B. Maggirwar, R. Deane, J.A. Fernández, B. LaRue, J.H. Griffin, M. Chopp, and B.V. Zlokovic Activated protein C inhibits tissue plasminogen activator-induced brain hemorrhage Nat. Med. 12 2006 1278 1285
5. A.J. Connolly, H. Ishihara, M.L. Kahn, R.V. Farese Jr., and S.R. Coughlin Role of the thrombin receptor in development and evidence for a second receptor Nature 381 1996 516 519
6. J.A. Fernández, X. Xu, D. Liu, B.V. Zlokovic, and J.H. Griffin Recombinant murine-activated protein C is neuroprotective in a murine ischemic stroke model Blood Cells, Mol., Dis. 30 2003 271 276
7. A.J. Gale, A. Tsavaler, and J.H. Griffin Molecular characterization of an extended binding site for coagulation factor Va in the positive exosite of activated protein C J. Biol. Chem. 277 2002 28836 28840
8. Y. Gong, Y. Hua, R.F. Keep, J.T. Hoff, and G. Xi Intracerebral hemorrhage: effects of aging on brain edema and neurological deficits Stroke 35 2004 2571 2575
9. L. Gorbacheva, O. Davidova, E. Sokolova, S. Ishiwata, V. Pinelis, S. Strukova, and G. Reiser Endothelial protein C receptor is expressed in rat cortical and hippocampal neurons and is necessary for protective effect of activated protein C at glutamate excitotoxicity J. Neurochem. 111 2009 967 975
10. J.H. Griffin, B.V. Zlokovic, and L.O. Mosnier Protein C anticoagulant and cytoprotective pathways Int. J. Hematol. 95 2012 333 345
11. H. Guo, D. Liu, H. Gelbard, T. Cheng, R. Insalaco, J.A. Fernández, J.H. Griffin, and B.V. Zlokovic Activated protein C prevents neuronal apoptosis via protease activated receptors 1 and 3 Neuron 41 2004 563 572
12. H. Guo, I. Singh, Y. Wang, R. Deane, T. Barrett, J.A. Fernández, N. Chow, J.H. Griffin, and B.V. Zlokovic Neuroprotective activities of activated protein C mutant with reduced anticoagulant activity Eur. J. Neurosci. 29 2009 1119 1130
13. H. Guo, Y. Wang, I. Singh, D. Liu, J.A. Fernández, J.H. Griffin, N. Chow, and B.V. Zlokovic Species-dependent neuroprotection by activated protein C mutants with reduced anticoagulant activity J. Neurochem. 109 2009 116 124
14. D.L. Heath, and R. Vink Improved motor outcome in response to magnesium therapy received up to 24 h after traumatic diffuse axonal brain injury in rats J. Neurosurg. 90 1999 504 509
15. C.E. Junge, T. Sugawara, G. Mannaioni, S. Alagarsamy, P.J. Conn, D.J. Brat, P.H. Chan, and S.F. Traynelis The contribution of protease-activated receptor 1 to neuronal damage caused by transient focal cerebral ischemia Proc. Natl. Acad. Sci. U.S.A. 100 2003 13019 13024
16. E. Kerschen, I. Hernandez, M. Zogg, S. Jia, M.J. Hessner, J.A. Fernandez, J.H. Griffin, C.S. Huettner, F.J. Castellino, and H. Weiler Activated protein C targets CD8+ dendritic cells to reduce the mortality of endotoxemia in mice J.Clin. Invest. 120 2010 3167 3178
17. E.J. Kerschen, J.A. Fernandez, B.C. Cooley, X.V. Yang, R. Sood, L.O. Mosnier, F.J. Castellino, N. Mackman, J.H. Griffin, and H. Weiler Endotoxemia and sepsis mortality reduction by non-anticoagulant activated protein C J. Exp. Med. 204 2007 2439 2448
18. D. Liu, T. Cheng, H. Guo, J.A. Fernández, J.H. Griffin, X. Song, and B.V. Zlokovic Tissue plasminogen activator neurovascular toxicity is controlled by activated protein C Nat. Med. 10 2004 1379 1383
19. Y. Luo, C.-C. Kuo, H. Shen, J. Chou, N.H. Greig, B.J. Hoffer, and Y. Wang Delayed treatment with a p53 inhibitor enhances recovery in stroke brain Ann. Neurol. 65 2009 520 530
20. L.O. Mosnier, A.J. Gale, S. Yegneswaran, and J.H. Griffin Activated protein C variants with normal cytoprotective but reduced anticoagulant activity Blood 104 2004 1740 1744
21. L.O. Mosnier, B.V. Zlokovic, and J.H. Griffin The cytoprotective protein C pathway Blood 109 2007 3161 3172
22. A.L. Petraglia, A.H. Marky, C. Walker, M. Thiyagarajan, and B.V. Zlokovic Activated protein C is neuroprotective and mediates new blood vessel formation and neurogenesis after controlled cortical impact Neurosurgery 66 2010 165 171 discussion 171-172
23. T. Schallert, and I.Q. Whishaw Bilateral cutaneous stimulation of the somatosensory system in hemidecorticate rats Behav. Neurosci. 98 1984 518 540
24. T.J. Shors, G. Miesegaes, A. Beylin, M. Zhao, T. Rydel, and E. Gould Neurogenesis in the adult is involved in the formation of trace memories Nature 410 2001 372 376
25. S. Soleman, P.K. Yip, D.A. Duricki, and L.D.F. Moon Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats Brain 135 2012 1210 1223
26. Y. Sun, K. Jin, L. Xie, J. Childs, X.O. Mao, A. Logvinova, and D.A. Greenberg VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia J. Clin. Invest. 111 2003 1843 1851
27. A. Taguchi, T. Soma, H. Tanaka, T. Kanda, H. Nishimura, H. Yoshikawa, Y. Tsukamoto, H. Iso, Y. Fujimori, D.M. Stern, H. Naritomi, and T. Matsuyama Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model J. Clin. Invest. 114 2004 330 338
28. M. Thiyagarajan, J.A. Fernández, S.M. Lane, J.H. Griffin, and B.V. Zlokovic Activated protein C promotes neovascularization and neurogenesis in postischemic brain via protease-activated receptor 1 J. Neurosci. 28 2008 12788 12797
29. H. Van Praag, B.R. Christie, T.J. Sejnowski, and F.H. Gage Running enhances neurogenesis, learning, and long-term potentiation in mice Proc. Natl. Acad. Sci. U.S.A. 96 1999 13427 13431
30. H. Van Praag, G. Kempermann, and F.H. Gage Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus Nat. Neurosci. 2 1999 266 270
31. C.T. Walker, A.H. Marky, A.L. Petraglia, T. Ali, N. Chow, and B.V. Zlokovic Activated protein C analog with reduced anticoagulant activity improves functional recovery and reduces bleeding risk following controlled cortical impact Brain Res. 1347 2010 125 131
32. L. Wang, Z. Zhang, Y. Wang, R. Zhang, and M. Chopp Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats Stroke 35 2004 1732 1737
33. Y. Wang, E. Kilic, U. Kilic, B. Weber, C.L. Bassetti, H.H. Marti, and D.M. Hermann VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena Brain 128 2005 52 63
34. Y. Wang, M. Thiyagarajan, N. Chow, I. Singh, H. Guo, T.P. Davis, and B.V. Zlokovic Differential neuroprotection and risk for bleeding from activated protein C with varying degrees of anticoagulant activity Stroke 40 2009 1864 1869
35. Y. Wang, Z. Zhang, N. Chow, T.P. Davis, J.H. Griffin, M. Chopp, and B.V. Zlokovic An activated protein C analog with reduced anticoagulant activity extends the therapeutic window of tissue plasminogen activator for ischemic stroke in rodents Stroke 43 2012 2444 2449
36. Z. Wen, and P. Wang Recombinant human erythropoietin increases cerebral cortical width index and neurogenesis following ischemic stroke Neural Regeneration Res. 2012 7
37. P.D. Williams, B.V. Zlokovic, J.H. Griffin, K.E. Pryor, and T.P. Davis Preclinical safety and pharmacokinetic profile of 3K3A-APC, a novel, modified activated protein C for ischemic stroke Curr. Pharm. Des. 18 2012 4215 4222
38. L. Zhang, Z. Zhang, R.L. Zhang, Y. Cui, M.C. LaPointe, B. Silver, and M. Chopp Tadalafil, a long-acting type 5 phosphodiesterase isoenzyme inhibitor, improves neurological functional recovery in a rat model of embolic stroke Brain Res. 1118 2006 192 198
39. R. Zhang, Y. Wang, L. Zhang, Z. Zhang, W. Tsang, M. Lu, L. Zhang, and M. Chopp Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats Stroke 33 2002 2675 2680
40. B.-Q. Zhao, S. Wang, H.-Y. Kim, H. Storrie, B.R. Rosen, D.J. Mooney, X. Wang, and E.H. Lo Role of matrix metalloproteinases in delayed cortical responses after stroke Nat. Med. 12 2006 441 445
41. Z. Zhong, H. Ilieva, L. Hallagan, R. Bell, I. Singh, N. Paquette, M. Thiyagarajan, R. Deane, J.A. Fernandez, S. Lane, A.B. Zlokovic, T. Liu, J.H. Griffin, N. Chow, F.J. Castellino, K. Stojanovic, D.W. Cleveland, and B.V. Zlokovic Activated protein C therapy slows ALS-like disease in mice by transcriptionally inhibiting SOD1 in motor neurons and microglia cells J. Clin. Invest. 119 2009 3437 3449
42. B.V. Zlokovic Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders Nat. Rev. Neurosci. 12 2011 723 738
43. B.V. Zlokovic, and J.H. Griffin Cytoprotective protein C pathways and implications for stroke and neurological disorders Trends Neurosci. 34 2011 198 209
44. B.V. Zlokovic, C. Zhang, D. Liu, J. Fernandez, J.H. Griffin, and M. Chopp Functional recovery after embolic stroke in rodents by activated protein C Ann. Neurol. 58 2005 474 477