Suppression of mitochondrial fission in experimental cerebral ischemia: The potential neuroprotective target of p38 MAPK inhibition

Neurochemistry International

Volumn 90, Issue , 2015, Pages 1-8

  Zhang, Xue Mei ^a   Zhang, Li ^b   Wang, Guili ^b,c   Niu, Wenxiu ^b   He, Zhijie ^b   Ding, Li ^b   Jia, Jie ^b  

^a The Department of Neurosurgery Henanxinxiang Center Hospital   (China)

^b FUDAN UNIVERSITY   (China)

^c FUJIAN UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Mitochondrial fission; Mitophagy; Neuroprotection; p38

Indexed keywords

4 [4 (4 FLUOROPHENYL) 5 (2 METHOXY 4 PYRIMIDINYL) 1 IMIDAZOLYL]CYCLOHEXANOL; DLP1 PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; LOSMAPIMOD; MFF PROTEIN; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P62; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; EXPERIMENTAL STROKE; FRAGMENTATION REACTION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL FISSION; MITOPHAGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; TRANSIENT ISCHEMIC ATTACK; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MITOCHONDRION; PHYSIOLOGY; SPRAGUE DAWLEY RAT; STROKE;

ANIMALS; AUTOPHAGY; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; MALE; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; NEUROPROTECTIVE AGENTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE INHIBITORS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; STROKE;

EID: 84947033848     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2015.06.010     Document Type: Article

References (47)

1. F.C. Barone, E.A. Irving, A.M. Ray, J.C. Lee, S. Kassis, S. Kumar, A.M. Badger, J.J. Legos, J.A. Erhardt, E.H. Ohlstein, A.J. Hunter, D.C. Harrison, K. Philpott, B.R. Smith, J.L. Adams, and A.A. Parsons Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia Med. Res. Rev. 21 2001 129 145
2. F.C. Barone, E.A. Irving, A.M. Ray, J.C. Lee, S. Kassis, S. Kumar, A.M. Badger, R.F. White, M.J. McVey, J.J. Legos, J.A. Erhardt, A.H. Nelson, E.H. Ohlstein, A.J. Hunter, K. Ward, B.R. Smith, J.L. Adams, and A.A. Parsons SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia J. Pharmacol. Exp. Ther. 296 2001 312 321
3. C. Bertoni-Freddari, P. Fattoretti, T. Casoli, G. Di Stefano, M. Solazzi, E. Perna, and C. De Angelis Reactive structural dynamics of synaptic mitochondria in ischemic delayed neuronal death Ann. N. Y. Acad. Sci. 1090 2006 26 34
4. J.P. Bolanos, M.A. Moro, I. Lizasoain, and A. Almeida Mitochondria and reactive oxygen and nitrogen species in neurological disorders and stroke: therapeutic implications Adv. Drug Deliv. Rev. 61 2009 1299 1315
5. H.M. Bramlett, and W.D. Dietrich Pathophysiology of cerebral ischemia and brain trauma: similarities and differences J. Cereb. Blood Flow. Metab. 24 2004 133 150
6. J. Cao, J.I. Viholainen, C. Dart, H.K. Warwick, M.L. Leyland, and M.J. Courtney The PSD95-nNOS interface: a target for inhibition of excitotoxic p38 stress-activated protein kinase activation and cell death J. Cell. Biol. 168 2005 117 126
7. D.C. Chan Fusion and fission: interlinked processes critical for mitochondrial health Annu Rev. Genet. 46 2012 265 287
8. D.H. Cho, T. Nakamura, and S.A. Lipton Mitochondrial dynamics in cell death and neurodegeneration Cell. Mol. Life Sci. 67 2010 3435 3447
9. X. Deschenes-Simard, F. Kottakis, S. Meloche, and G. Ferbeyre ERKs in cancer: friends or foes? Cancer Res. 74 2014 412 419
10. S.A. Detmer, and D.C. Chan Functions and dysfunctions of mitochondrial dynamics Nat. Rev. Mol. Cell. Biol. 8 2007 870 879
11. X. Gan, S. Huang, L. Wu, Y. Wang, G. Hu, G. Li, H. Zhang, H. Yu, R.H. Swerdlow, J.X. Chen, and S.S. Yan Inhibition of ERK-DLP1 signaling and mitochondrial division alleviates mitochondrial dysfunction in Alzheimer's disease cybrid cell Biochim. Biophys. Acta 1842 2014 220 231
12. M.J. Goldenthal, and J. Marin-Garcia Mitochondrial signaling pathways: a receiver/integrator organelle Mol. Cell. Biochem. 262 2004 1 16
13. J. Grohm, S.W. Kim, U. Mamrak, S. Tobaben, A. Cassidy-Stone, J. Nunnari, N. Plesnila, and C. Culmsee Inhibition of Drp1 provides neuroprotection in vitro and in vivo Cell. Death Differ. 19 2012 1446 1458
14. Q.H. Guan, D.S. Pei, T.L. Xu, and G.Y. Zhang Brain ischemia/reperfusion-induced expression of DP5 and its interaction with Bcl-2, thus freeing Bax from Bcl-2/Bax dimmers are mediated by c-Jun N-terminal kinase (JNK) pathway Neurosci. Lett. 393 2006 226 230
15. J. Harada, and M. Sugimoto An inhibitor of p38 and JNK MAP kinases prevents activation of caspase and apoptosis of cultured cerebellar granule neurons Jpn. J. Pharmacol. 79 1999 369 378
16. T. Hayashi, and K. Abe Ischemic neuronal cell death and organellae damage Neurol. Res. 26 2004 827 834
17. Y. Hirota, S. Yamashita, Y. Kurihara, X. Jin, M. Aihara, T. Saigusa, D. Kang, and T. Kanki Mitophagy is primarily due to alternative autophagy and requires the MAPK1 and MAPK14 signaling pathways Autophagy 11 2015 332 343
18. H.C. Huang, and P.S. Klein Multiple roles for glycogen synthase kinase-3 as a drug target in Alzheimer's disease Curr. Drug Targets 7 2006 1389 1397
19. E.A. Irving, and M. Bamford Role of mitogen- and stress-activated kinases in ischemic injury J. Cereb. Blood Flow. Metab. 22 2002 631 647
20. M. Komatsu, S. Waguri, M. Koike, Y.S. Sou, T. Ueno, T. Hara, N. Mizushima, J. Iwata, J. Ezaki, S. Murata, J. Hamazaki, Y. Nishito, S. Iemura, T. Natsume, T. Yanagawa, J. Uwayama, E. Warabi, H. Yoshida, T. Ishii, A. Kobayashi, M. Yamamoto, Z. Yue, Y. Uchiyama, E. Kominami, and K. Tanaka Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice Cell 131 2007 1149 1163
21. L.L. Lackner Shaping the dynamic mitochondrial network BMC Biol. 12 2014 35
22. J.C. Lee, S. Kumar, D.E. Griswold, D.C. Underwood, B.J. Votta, and J.L. Adams Inhibition of p38 MAP kinase as a therapeutic strategy Immunopharmacology 47 2000 185 201
23. J.J. Legos, J.A. Erhardt, R.F. White, S.C. Lenhard, S. Chandra, A.A. Parsons, R.F. Tuma, and F.C. Barone SB 239063, a novel p38 inhibitor, attenuates early neuronal injury following ischemia Brain Res. 892 2001 70 77
24. K. Lei, A. Nimnual, W.X. Zong, N.J. Kennedy, R.A. Flavell, C.B. Thompson, D. Bar-Sagi, and R.J. Davis The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase Mol. Cell. Biol. 22 2002 4929 4942
25. W. Liu, F. Tian, T. Kurata, N. Morimoto, and K. Abe Dynamic changes of mitochondrial fusion and fission proteins after transient cerebral ischemia in mice J. Neurosci. Res. 90 2012 1183 1189
26. E.Z. Longa, P.R. Weinstein, S. Carlson, and R. Cummins Reversible middle cerebral artery occlusion without craniectomy in rats Stroke 20 1989 84 91
27. J. Marin-Garcia, and M.J. Goldenthal Mitochondria play a critical role in cardioprotection J. Card. Fail 10 2004 55 66
28. L.K. Newby, M.S. Marber, C. Melloni, L. Sarov-Blat, L.H. Aberle, P.E. Aylward, G. Cai, R.J. de Winter, C.W. Hamm, J.F. Heitner, R. Kim, A. Lerman, M.R. Patel, J.F. Tanguay, J.J. Lepore, H.R. Al-Khalidi, D.L. Sprecher, C.B. Granger, and S. Investigators Losmapimod, a novel p38 mitogen-activated protein kinase inhibitor, in non-ST-segment elevation myocardial infarction: a randomised phase 2 trial Lancet 384 2014 1187 1195
29. K. Nozaki, M. Nishimura, and N. Hashimoto Mitogen-activated protein kinases and cerebral ischemia Mol. Neurobiol. 23 2001 1 19
30. S. Okuno, A. Saito, T. Hayashi, and P.H. Chan The c-Jun N-terminal protein kinase signaling pathway mediates Bax activation and subsequent neuronal apoptosis through interaction with Bim after transient focal cerebral ischemia J. Neurosci. 24 2004 7879 7887
31. A.V. Ougolkov, and D.D. Billadeau Targeting GSK-3: a promising approach for cancer therapy? Future Oncol. 2 2006 91 100
32. S. Park, S.G. Choi, S.M. Yoo, J.H. Son, and Y.K. Jung Choline dehydrogenase interacts with SQSTM1/p62 to recruit LC3 and stimulate mitophagy Autophagy 10 2014 1906 1920
33. G. Pearson, F. Robinson, T. Beers Gibson, B.E. Xu, M. Karandikar, K. Berman, and M.H. Cobb Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions Endocr. Rev. 22 2001 153 183
34. C.S. Piao, J.B. Kim, P.L. Han, and J.K. Lee Administration of the p38 MAPK inhibitor SB203580 affords brain protection with a wide therapeutic window against focal ischemic insult J. Neurosci. Res. 73 2003 537 544
35. P.R. Purnell, and H.S. Fox Autophagy-mediated turnover of dynamin-related protein 1 BMC Neurosci. 14 2013 86
36. S. Sridharan, K. Jain, and A. Basu Regulation of autophagy by kinases Cancers (Basel) 3 2011 2630 2654
37. V. Stambolic, and J.R. Woodgett Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation Biochem. J. 303 Pt 3 1994 701 704
38. R.L. Stornetta, and J.J. Zhu Ras and rap signaling in synaptic plasticity and mental disorders Neuroscientist 17 2011 54 78
39. T. Sugino, K. Nozaki, Y. Takagi, I. Hattori, N. Hashimoto, T. Moriguchi, and E. Nishida Activation of mitogen-activated protein kinases after transient forebrain ischemia in gerbil hippocampus J. Neurosci. 20 2000 4506 4514
40. R. Sugioka, S. Shimizu, and Y. Tsujimoto Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis J. Biol. Chem. 279 2004 52726 52734
41. X. Sui, N. Kong, L. Ye, W. Han, J. Zhou, Q. Zhang, C. He, and H. Pan p38 and JNK MAPK pathways control the balance of apoptosis and autophagy in response to chemotherapeutic agents Cancer Lett. 344 2014 174 179
42. B.R. Webster, I. Scott, K. Han, J.H. Li, Z. Lu, M.V. Stevens, D. Malide, Y. Chen, L. Samsel, P.S. Connelly, M.P. Daniels, J.P. McCoy Jr., C.A. Combs, M. Gucek, and M.N. Sack Restricted mitochondrial protein acetylation initiates mitochondrial autophagy J. Cell. Sci. 126 2013 4843 4849
43. Z. Xia, M. Dickens, J. Raingeaud, R.J. Davis, and M.E. Greenberg Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis Science 270 1995 1326 1331
44. L. Zhang, Z. He, Q. Zhang, Y. Wu, X. Yang, W. Niu, Y. Hu, and J. Jia Exercise pretreatment promotes mitochondrial dynamic protein OPA1 expression after cerebral ischemia in rats Int. J. Mol. Sci. 15 2014 4453 4463
45. L. Zhang, W. Niu, Z. He, Q. Zhang, Y. Wu, C. Jiang, C. Tang, Y. Hu, and J. Jia Autophagy suppression by exercise pretreatment and p38 inhibition is neuroprotective in cerebral ischemia Brain Res. 1587 2014 127 132
46. J.J. Zhu, Y. Qin, M. Zhao, L. Van Aelst, and R. Malinow Ras and rap control AMPA receptor trafficking during synaptic plasticity Cell 110 2002 443 455
47. W. Zuo, S. Zhang, C.Y. Xia, X.F. Guo, W.B. He, and N.H. Chen Mitochondria autophagy is induced after hypoxic/ischemic stress in a Drp1 dependent manner: the role of inhibition of Drp1 in ischemic brain damage Neuropharmacology 86 2014 103 115