Hypoxic preconditioning induced neuroprotection against cerebral ischemic injuries and its cPKCγ-mediated molecular mechanism

Neurochemistry International

Volumn 58, Issue 6, 2011, Pages 684-692

  Zhang, Nan ^a   Yin, Yanling ^a   Han, Song ^a   Jiang, Jun ^a   Yang, Weiwei ^a   Bu, Xiangning ^a   Li, Junfa ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

cPKC ; Hypoxic preconditioning; MCAO; Proteomics; Synapsin

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 5 METHOXY 1H INDOL 3 YL] 3 (1H INDOL 3 YL)MALEIMIDE; PROTEIN KINASE C GAMMA; SYNAPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN HYPOXIA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; CYTOSOL; DOWN REGULATION; HYPOXIC PRECONDITIONING; ISCHEMIC PRECONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN INTERACTION; PROTEOMICS; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANOXIA; BLOTTING, WESTERN; BRAIN ISCHEMIA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME ACTIVATION; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; ISCHEMIC PRECONDITIONING; MALE; MICE; MICE, INBRED BALB C; PROTEIN KINASE C;

MUS;

EID: 79953728169     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.02.007     Document Type: Article

References (48)

1. J. Aronowski, J.C. Grotta, R. Strong, and M.N. Waxham Interplay between the gamma isoform of PKC and calcineurin in regulation of vulnerability to focal cerebral ischemia J. Cereb. Blood Flow Metab. 20 2000 343 349 (Pubitemid 30108453)
2. S. Ashwal, B. Tone, H.R. Tian, D.J. Cole, and W.J. Pearce Core and penumbral nitric oxide synthase activity during cerebral ischemia and reperfusion Stroke 29 1998 1037 1046
3. H. Bolay, Y. Gursoy-Ozdemir, Y. Sara, R. Onur, A. Can, and T. Dalkara Persistent defect in transmitter release and synapsin phosphorylation in cerebral cortex after transient moderate ischemic injury Stroke 33 2002 1369 1375 (Pubitemid 34517062)
4. R. Bright, and D. Mochly-Rosen The role of protein kinase C in cerebral ischemic and reperfusion injury Stroke 36 2005 2781 2790
5. X. Bu, P. Huang, Z. Qi, N. Zhang, S. Han, L. Fang, and J. Li Cell type-specific activation of p38 MAPK in the brain regions of hypoxic preconditioned mice Neurochem. Int. 51 2007 459 466 (Pubitemid 47513761)
6. P. Calabresi, D. Centonze, A. Pisani, L. Cupini, and G. Bernardi Synaptic plasticity in the ischaemic brain Lancet Neurol. 2 2003 622 629 (Pubitemid 37162571)
7. H.C. Chang, Y.R. Yang, S.G. Wang, and R.Y. Wang Effects of treadmill training on motor performance and extracellular glutamate level in striatum in rats with or without transient middle cerebral artery occlusion Behav. Brain Res. 205 2009 450 455
8. C. Chen, and S. Tonegawa Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain Annu. Rev. Neurosci. 20 1997 157 184 (Pubitemid 27106379)
9. D. Chin, K.E. Winkler, and A.R. Means Characterization of substrate phosphorylation and use of calmodulin mutants to address implications from the enzyme crystal structure of calmodulin-dependent protein kinase I J. Biol. Chem. 272 1997 31235 31240 (Pubitemid 28013253)
10. C. Cid, L. Garcia-Bonilla, E. Camafeita, J. Burda, M. Salinas, and A. Alcazar Proteomic characterization of protein phosphatase 1 complexes in ischemia-reperfusion and ischemic tolerance Proteomics 7 2007 3207 3218 (Pubitemid 47477962)
11. E. Fdez, and S. Hilfiker Vesicle pools and synapsins: new insights into old enigmas Brain Cell Biol. 35 2006 107 115 (Pubitemid 47630632)
12. C.N. Giachello, F. Fiumara, C. Giacomini, A. Corradi, C. Milanese, M. Ghirardi, F. Benfenati, and P.G. Montarolo MAPK/Erk-dependent phosphorylation of synapsin mediates formation of functional synapses and short-term homosynaptic plasticity J. Cell Sci. 123 2010 881 893
13. M. Gschwendt, S. Dieterich, J. Rennecke, W. Kittstein, H.J. Mueller, and F.J. Johannes Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes FEBS Lett. 392 1996 77 80 (Pubitemid 26276722)
14. W. Hamabe, R. Fujita, and H. Ueda Insulin receptor-protein kinase C-gamma signaling mediates inhibition of hypoxia-induced necrosis of cortical neurons J. Pharmacol. Exp. Ther. 313 2005 1027 1034 (Pubitemid 40727006)
15. S. Hayashi, T. Ueyama, T. Kajimoto, K. Yagi, E. Kohmura, and N. Saito Involvement of gamma protein kinase C in estrogen-induced neuroprotection against focal brain ischemia through G protein-coupled estrogen receptor J. Neurochem. 93 2005 883 891 (Pubitemid 40695747)
16. J. Jia, X. Wang, H. Li, S. Han, P. Zu, and J. Li Activations of nPKCepsilon and ERK1/2 were involved in oxygen-glucose deprivation-induced neuroprotection via NMDA receptors in hippocampal slices of mice J. Neurosurg. Anesthesiol. 19 2007 18 24 (Pubitemid 46045770)
17. J. Jiang, W. Yang, P. Huang, X. Bu, N. Zhang, and J. Li Increased phosphorylation of Ets-like transcription factor-1 in neurons of hypoxic preconditioned mice Neurochem. Res. 34 2009 1443 1450
18. J.N. Jovanovic, F. Benfenati, Y.L. Siow, T.S. Sihra, J.S. Sanghera, S.L. Pelech, P. Greengard, and A.J. Czernik Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions Proc. Natl. Acad. Sci. U.S.A. 93 1996 3679 3683 (Pubitemid 26127596)
19. E. Kilic, D.M. Hermann, S. Kugler, U. Kilic, H. Holzmuller, C. Schmeer, and M. Bahr Adenovirus-mediated Bcl-X(L) expression using a neuron-specific synapsin-1 promoter protects against disseminated neuronal injury and brain infarction following focal cerebral ischemia in mice Neurobiol. Dis. 11 2002 275 284 (Pubitemid 36135691)
20. J. Krupinski, M.A. Slevin, P. Kumar, J. Gaffney, and J. Kaluza Protein kinase C expression and activity in the human brain after ischaemic stroke Acta Neurobiol. Exp. (Wars.) 58 1998 13 21 (Pubitemid 28129313)
21. J. Li, C. Niu, S. Han, P. Zu, H. Li, Q. Xu, and L. Fang Identification of protein kinase C isoforms involved in cerebral hypoxic preconditioning of mice Brain Res. 1060 2005 62 72 (Pubitemid 41483590)
22. J. Li, Y. Qu, P. Zu, S. Han, G. Gao, Q. Xu, and L. Fang Increased isoform-specific membrane translocation of conventional and novel protein kinase C in human neuroblastoma SH-SY5Y cells following prolonged hypoxia Brain Res. 1093 2006 25 32 (Pubitemid 43946405)
23. D. Lin, D.L. Boyle, and D.J. Takemoto IGF-I-induced phosphorylation of connexin 43 by PKCgamma: regulation of gap junctions in rabbit lens epithelial cells Invest Ophthalmol. Vis. Sci. 44 2003 1160 1168 (Pubitemid 36297836)
24. Y. Liu, J. Li, J. Yang, F. Ji, X. Bu, N. Zhang, and B. Zhang Inhibition of PKCgamma membrane translocation mediated morphine preconditioning-induced neuroprotection against oxygen-glucose deprivation in the hippocampus slices of mice Neurosci. Lett. 444 2008 87 91
25. D. Lloyd-Jones, R.J. Adams, T.M. Brown, M. Carnethon, S. Dai, S.G. De, T.B. Ferguson, E. Ford, K. Furie, C. Gillespie, A. Go, K. Greenlund, N. Haase, S. Hailpern, P.M. Ho, V. Howard, B. Kissela, S. Kittner, D. Lackland, L. Lisabeth, A. Marelli, M.M. McDermott, J. Meigs, D. Mozaffarian, M. Mussolino, G. Nichol, V.L. Roger, W. Rosamond, R. Sacco, P. Sorlie, V.L. Roger, T. Thom, S. Wasserthiel-Smoller, N.D. Wong, and J. Wylie-Rosett Heart disease and stroke statistics-2010 update: a report from the American heart association Circulation 121 2010 e46 e215
26. G.W. Lu, and H.Y. Liu Downregulation of nitric oxide in the brain of mice during their hypoxic preconditioning J. Appl. Physiol. 91 2001 1193 1198
27. C.W. Mahoney, K. Seki, and K.P. Huang Phosphorylation of MARCKS, neuromodulin, and neurogranin by protein kinase C exhibits differential responses to diacylglycerols Cell Signal. 7 1995 679 685
28. J.D. Marsh, and S.G. Keyrouz Stroke prevention and treatment J. Am. Coll. Cardiol. 56 2010 683 691
29. K. Mayanagi, P.V. Katakam, T. Gaspar, F. Domoki, and D.W. Busija Acute treatment with rosuvastatin protects insulin resistant (C57BL/6J ob/ob) mice against transient cerebral ischemia J. Cereb. Blood Flow Metab. 28 2008 1927 1935
30. 2+-dependent synaptic activity J. Neurosci. 26 2006 11670 11681 (Pubitemid 44772139)
31. C.P. Nelson, S.R. Nahorski, and R.A. Challiss Temporal profiling of changes in phosphatidylinositol 4,5-bisphosphate, inositol 1,4,5-trisphosphate and diacylglycerol allows comprehensive analysis of phospholipase C-initiated signalling in single neurons J. Neurochem. 107 2008 602 615
32. T.A. Nguyen, L.J. Takemoto, and D.J. Takemoto Inhibition of gap junction activity through the release of the C1B domain of protein kinase Cgamma (PKCgamma) from 14-3-3: identification of PKCgamma-binding sites J. Biol. Chem. 279 2004 52714 52725 (Pubitemid 39656647)
33. C. Niu, J. Li, X. Cui, S. Han, P. Zu, H. Li, and Q. Xu Changes in cPKC isoform-specific membrane translocation and protein expression in the brain of hypoxic preconditioned mice Neurosci. Lett. 384 2005 1 6 (Pubitemid 40826607)
34. M.A. Perez-Pinzon Mechanisms of neuroprotection during ischemic preconditioning: lessons from anoxic tolerance Comp. Biochem. Physiol A: Mol. Integr. Physiol. 147 2007 291 299 (Pubitemid 46617985)
35. M. Ploughman, Z. Attwood, N. White, J.J. Dore, and D. Corbett Endurance exercise facilitates relearning of forelimb motor skill after focal ischemia Eur. J. Neurosci. 25 2007 3453 3460 (Pubitemid 46872775)
36. M. Ploughman, S. Granter-Button, G. Chernenko, Z. Attwood, B.A. Tucker, K.M. Mearow, and D. Corbett Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia Brain Res. 1150 2007 207 216 (Pubitemid 46702117)
37. K.A. Powell, V.A. Valova, C.S. Malladi, O.N. Jensen, M.R. Larsen, and P.J. Robinson Phosphorylation of dynamin I on Ser-795 by protein kinase C blocks its association with phospholipids J. Biol. Chem. 275 2000 11610 11617 (Pubitemid 30237719)
38. G.M. Ramakers, D.D. Gerendasy, and P.N. de Graan Substrate phosphorylation in the protein kinase Cgamma knockout mouse J. Biol. Chem. 274 1999 1873 1874
39. E.B. Rex, M.L. Rankin, Y. Yang, Q. Lu, C.R. Gerfen, P.A. Jose, and D.R. Sibley Identification of RanBP 9/10 as interacting partners for protein kinase C (PKC) gamma/delta and the D1 dopamine receptor: regulation of PKC-mediated receptor phosphorylation Mol. Pharmacol. 78 2010 69 80
40. R. Rodriguez, J. Santiago-Mejia, C. Gomez, and E.R. San-Juan A simplified procedure for the quantitative measurement of neurological deficits after forebrain ischemia in mice J. Neurosci. Methods 147 2005 22 28 (Pubitemid 41058665)
41. M. Rodriguez-Munoz, l.T.-M. de, P. Sanchez-Blazquez, J.B. Wang, and J. Garzon NMDAR-nNOS generated zinc recruits PKCgamma to the HINT1-RGS17 complex bound to the C terminus of Mu-opioid receptors Cell Signal. 20 2008 1855 1864
42. J.L. Rosales, M.J. Nodwell, R.N. Johnston, and K.Y. Lee Cdk5/p25(nck5a) interaction with synaptic proteins in bovine brain J. Cell Biochem. 78 2000 151 159 (Pubitemid 30346391)
43. N. Saito, and Y. Shirai Protein kinase C gamma (PKC gamma): function of neuron specific isotype J. Biochem. 132 2002 683 687 (Pubitemid 35408489)
44. A. Stemer, and P. Lyden Evolution of the thrombolytic treatment window for acute ischemic stroke Curr. Neurol. Neurosci. Rep. 10 2010 29 33
45. E.J. Wexler, E.E. Peters, A. Gonzales, M.L. Gonzales, A.M. Slee, and J.S. Kerr An objective procedure for ischemic area evaluation of the stroke intraluminal thread model in the mouse and rat J. Neurosci. Methods 113 2002 51 58 (Pubitemid 33123329)
46. 2+/ calmodulin-dependent phosphorylation of synapsin I in insulin exocytosis J. Pharmacol. Sci. 93 2003 30 34 (Pubitemid 37254263)
47. 2+-dependent (classical) PKC mRNA isoforms after transient cerebral ischemia in gerbil hippocampus Brain Res. 779 1998 254 258 (Pubitemid 28039958)
48. N. Zhang, G. Gao, X. Bu, S. Han, L. Fang, and J. Li Neuron-specific phosphorylation of c-Jun N-terminal kinase increased in the brain of hypoxic preconditioned mice Neurosci. Lett. 423 2007 219 224 (Pubitemid 47285484)