Mitochondrial translocation of p53 mediates release of cytochrome c and hippocampal CA1 neuronal death after transient global cerebral ischemia in rats

Journal of Neuroscience

Volumn 26, Issue 30, 2006, Pages 7974-7983

  Endo, Hidenori ^a   Kamada, Hiroshi ^a   Nito, Chikako ^a   Nishi, Tatsuro ^a   Chan, Pak H ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Apoptosis; Global cerebral ischemia; Hippocampal CA1 neurons; Mitochondrial translocation; p53; Rat

Indexed keywords

CYTOCHROME C; DNA FRAGMENT; PIFITHRIN ALPHA; PROTEIN BCL XL; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN MITOCHONDRION; CELL DEATH; CONTROLLED STUDY; ENZYME RELEASE; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT; TRANSIENT ISCHEMIC ATTACK; WESTERN BLOTTING; ANIMAL; APOPTOSIS; CELL CULTURE; METABOLISM; MITOCHONDRION; PATHOLOGY; PROTEIN TRANSPORT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CYTOCHROMES C; HIPPOCAMPUS; MALE; MITOCHONDRIA; NEURONS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33747056618     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0897-06.2006     Document Type: Article

References (41)

1. Abe K, Aoki M, Kawagoe J, Yoshida T, Hattori A, Kogure K, Itoyama Y (1995) Ischemic delayed neuronal death. A mitochondrial hypothesis. Stroke 26:1478-1489.
2. Chan PH (1996) Role of oxidants in ischemic brain damage. Stroke 27:1124-1129.
3. Chan PH, Kawase M, Murakami K, Chen SF, Li Y, Calagui B, Reola L, Carlson E, Epstein CJ (1998) Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci 18:8292-8299.
4. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303:1010-1014.
5. Chipuk JE, Bouchier-Hayes L, Kuwana T, Newmeyer DD, Green DR (2005) PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 309:1732-1735.
6. Crumrine RC, Thomas AL, Morgan PF (1994) Attenuation of p53 expression protects against focal ischemic damage in transgenic mice. J Cereb Blood Flow Metab 14:887-891.
7. Culmsee C, Zhu X, Yu Q-S, Chan SL, Camandola S, Guo Z, Greig NH, Mattson MP (2001) A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid β-peptide. J Neurochem 77:220-228.
8. Culmsee C, Siewe J, Junker V, Retiounskaia M, Schwarz S, Camandola S, El-Metainy S, Behnke H, Mattson MP, Krieglstein J (2003) Reciprocal inhibition of p53 and nuclear factor-κB transcriptional activities determines cell survival or death in neurons. J Neurosci 23:8586-8595.
9. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM (2004) In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol 24:6728-6741.
10. Fujimura M, Morita-Fujimura Y, Kawase M, Copin J-C, Calagui B, Epstein CJ, Chan PH (1999) Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome c and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J Neurosci 19:3414-3422.
11. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Chan PH (2003a) Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stress and prevents delayed neuronal cell death. J Cereb Blood Flow Metab 23:949-961.
12. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Dodd RL, Nishi T, Maier CM, Kinouchi H, Chan PH (2003b) Oxidative damage to the endoplasmic reticulum is implicated in ischemic neuronal cell death. J Cereb Blood Flow Metab 23:1117-1128.
13. Jordán J, Galindo MF, Prehn JHM, Weichselbaum RR, Beckett M, Ghadge GD, Roos RP, Leiden JM, Miller RJ (1997) p53 expression induces apoptosis in hippocampal pyramidal neuron cultures. J Neurosci 17:1397-1405.
14. Kelly KJ, Plotkin Z, Vulgamott SL, Dagher PC (2003) p53 mediates the apoptotic response to GTP depletion after renal ischemia-reperfusion: protective role of a p53 inhibitor. J Am Soc Nephrol 14:128-138.
15. Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57-69.
16. Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, Chernov MV, Gudkov AV (1999) A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285:1733-1737.
17. Leist M, Kühnle S, Single B, Nicotera P (1998) Differentiation between apoptotic and necrotic cell death by means of the BM cell death detection ELISA or annexin V staining. Biochemica 2:25-28.
18. Leker RR, Aharonowiz M, Greig NH, Ovadia H (2004) The role of p53-induced apoptosis in cerebral ischemia: effects of the p53 inhibitor pifithrin α. Exp Neurol 187:478-486.
19. Levine AJ (1997) p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
20. Li Y, Chopp M, Zhang ZG, Zaloga C, Niewenhuis L, Gautam S (1994) p53-immunoreactive protein and p53 mRNA expression after transient middle cerebral artery occlusion in rats. Stroke 25:849-855.
21. Marchenko ND, Zaika A, Moll UM (2000) Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 275:16202-16212.
22. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM (2003) p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11:577-590.
23. Miyashita T, Reed JC (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299.
24. Murakami K, Kondo T, Epstein CJ, Chan PH (1997) Overexpression of CuZn-superoxide dismutase reduces hippocampal injury after global ischemia in transgenic mice. Stroke [Erratum (1997) 28:2573] 28:1797-1804.
25. Nakano K, Vousden KH (2001) PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7:683-694.
26. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, Tanaka N (2000a) Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288:1053-1058.
27. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tokino T, Nakamura Y, Taya Y (2000b) p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102:849-862.
28. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-498.
29. Saito A, Hayashi T, Okuno S, Ferrand-Drake M, Chan PH (2003) Overexpression of copper/zinc superoxide dismutase in transgenic mice protects against neuronal cell death after transient focal ischemia by blocking activation of the Bad cell death signaling pathway. J Neurosci 23:1710-1718.
30. Saito A, Hayashi T, Okuno S, Nishi T, Chan PH (2005) Modulation of p53 degradation via MDM2-mediated ubiquitylation and the ubiquitin-proteasome system during reperfusion after stroke: role of oxidative stress. J Cereb Blood Flow Metab 25:267-280.
31. Sansome C, Zaika A, Marchenko ND, Moll UM (2001) Hypoxia death stimulus induces translocation of p53 protein to mitochondria. Detection by immunofluorescence on whole cells. FEBS Lett 488:110-115.
32. Sax JK, El-Deiry WS (2003) p53 downstream targets and chemosensitivity. Cell Death Differ 10:413-417.
33. Smith ML, Bendek G, Dahlgren N, Rosen I, Wieloch T, Siesjö BK (1984) Models for studying long-term recovery following forebrain ischemia in the rat. 2. A 2-vessel occlusion model. Acta Neurol Scand 69:385-401.
34. Sugawara T, Fujimura M, Morita-Fujimura Y, Kawase M, Chan PH (1999) Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J Neurosci 19:RC39(1-6).
35. Sugawara T, Noshita N, Lewén A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y, Chan PH (2002) Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 22:209-217.
36. WAF1/Cip1 are not markers of neuronal death following transient global cerebral ischemia. Neuroscience 90:781-792.
37. WAF1/Cip1 and PAG608/Wig-1 in ischemic preconditioning. Mol Brain Res 70:304-313.
38. Xiang H, Hochman DW, Saya H, Fujiwara T, Schwartzkroin PA, Morrison RS (1996) Evidence for p53-mediated modulation of neuronal viability. J Neurosci 16:6753-6765.
39. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS (1998) Bax involvement in p53-mediated neuronal cell death. J Neurosci 18:1363-1373.
40. Yonekura I, Takai K, Asai A, Kawahara N, Kirino T (2006) p53 potentiates hippocampal neuronal death caused by global ischemia. J Cereb Blood Flow Metab, in press.
41. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B (2001) PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7:673-682.