Deletion of puma protects hippocampal neurons in a model of severe status epilepticus

Neuroscience

Volumn 168, Issue 2, 2010, Pages 443-450

  Engel, T ^a   Hatazaki, S ^a,b   Tanaka, K ^a,b   Prehn, J H M ^a   Henshall, D C ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b MIE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Bcl 2; Caspase; Epilepsy; Hippocampal sclerosis; Necrosis

Indexed keywords

CASPASE; DNA; KAINIC ACID; LORAZEPAM; PROTEIN BCL 2; PUMA PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DAMAGE; CELL DEATH; CELL NUCLEUS; CELL PROTECTION; CELL STRUCTURE; CELL SURVIVAL; CHROMATIN CONDENSATION; CONTROLLED STUDY; DISEASE DURATION; DISEASE MODEL; DISEASE SEVERITY; DNA FRAGMENTATION; DRUG TARGETING; ELECTROENCEPHALOGRAPHY; EPILEPTIC STATE; GENE DELETION; HETEROZYGOSITY; HIPPOCAMPUS; MALE; MICROSCOPY; MOUSE; NERVE CELL; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; HIPPOCAMPUS; KAINIC ACID; MICE; MICE, KNOCKOUT; NEURONS; STATUS EPILEPTICUS; TUMOR SUPPRESSOR PROTEINS;

EID: 77952883652     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.03.057     Document Type: Article

References (62)

1. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995, 15:961-973.
2. Araki T., Simon R.P., Taki W., Lan J.-Q., Henshall D.C. Characterization of neuronal death induced by focally evoked limbic seizures in the C57BL/6 mouse. J Neurosci Res 2002, 69:614-621.
3. Araujo I.M., Gil J.M., Carreira B.P., Mohapel P., Petersen A., Pinheiro P.S., Soulet D., Bahr B.A., Brundin P., Carvalho C.M. Calpain activation is involved in early caspase-independent neurodegeneration in the hippocampus following status epilepticus. J Neurochem 2008, 105:666-676.
4. Barth M., Oulmi Y., Ehrenreich H., Schilling L. Pre-embedding immunogold labeling of TUNEL stain enables evaluation of DNA strand breaks and ultrastructural alterations in individual cells of neuronal tissue. Acta Neuropathol 2002, 104:621-636.
5. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A 1995, 92:7162-7166.
6. Cartron P.F., Gallenne T., Bougras G., Gautier F., Manero F., Vusio P., Meflah K., Vallette F.M., Juin P. The first alpha helix of Bax plays a necessary role in its ligand-induced activation by the BH3-only proteins Bid and PUMA. Mol Cell 2004, 16:807-818.
7. Cherian K.A., Weidenheim K., Legatt A.D., Shifteh K., Abbott I.R., Moshe S.L. Extensive apoptosis in a case of intractable infantile status epilepticus. Epilepsy Res 2009, 85:305-310.
8. Cheung E.C., Melanson-Drapeau L., Cregan S.P., Vanderluit J.L., Ferguson K.L., McIntosh W.C., Park D.S., Bennett S.A., Slack R.S. Apoptosis-inducing factor is a key factor in neuronal cell death propagated by BAX-dependent and BAX-independent mechanisms. J Neurosci 2005, 25:1324-1334.
9. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988, 1:623-634.
10. Concannon C.G., Ward M.W., Bonner H.P., Kuroki K., Tuffy L.P., Bonner C.T., Woods I., Engel T., Henshall D.C., Prehn J.H. NMDA receptor-mediated excitotoxic neuronal apoptosis in vitro and in vivo occurs in an ER stress and PUMA independent manner. J Neurochem 2007, 105:891-903.
11. Culmsee C., Zhu C., Landshamer S., Becattini B., Wagner E., Pellecchia M., Blomgren K., Plesnila N. Apoptosis-inducing factor triggered by poly(ADP-ribose) polymerase and Bid mediates neuronal cell death after oxygen-glucose deprivation and focal cerebral ischemia. J Neurosci 2005, 25:10262-10272.
12. Dong Z., Saikumar P., Weinberg J.M., Venkatachalam M.A. Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am J Pathol 1997, 151:1205-1213.
13. Du C., Hu R., Csernansky C.A., Hsu C.Y., Choi D.W. Very delayed infarction after mild focal cerebral ischemia: a role for apoptosis?. J Cereb Blood Flow Metab 1996, 16:195-201.
14. Engel T., Henshall D.C. Apoptosis, Bcl-2 family proteins and caspases: the ABCs of seizure-damage and epileptogenesis?. Int J Physiol Pathophysiol Pharmacol 2009, 1:97-115.
15. Engel T., Murphy B.M., Hatazaki S., Jimenez-Mateos E.M., Concannon C.G., Woods I., Prehn J.H., Henshall D.C. Reduced hippocampal damage and epileptic seizures after status epilepticus in mice lacking proapoptotic Puma. FASEB J 2010, 24:853-861.
16. Faherty C.J., Xanthoudakis S., Smeyne R.J. Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res Mol Brain Res 1999, 70:159-163.
17. Fujikawa D.G. Prolonged seizures and cellular injury: understanding the connection. Epilepsy Behav 2005, 7(Suppl 3):S3-S11.
18. Fujikawa D.G., Itabashi H.H., Wu A., Shinmei S.S. Status epilepticus-induced neuronal loss in humans without systemic complications or epilepsy. Epilepsia 2000, 41:981-991.
19. Fujikawa D.G., Shinmei S.S., Cai B. Kainic acid-induced seizures produce necrotic, not apoptotic, neurons with internucleosomal DNA cleavage: implications for programmed cell death mechanisms. Neuroscience 2000, 98:41-53.
20. Fujikawa D.G., Shinmei S.S., Zhao S., Aviles E.R. Caspase-dependent programmed cell death pathways are not activated in generalized seizure-induced neuronal death. Brain Res 2007, 1135:206-218.
21. Fujikawa D.G., Zhao S., Ke X., Shinmei S.S., Allen S.G. Mild as well as severe insults produce necrotic, not apoptotic, cells: evidence from 60-min seizures. Neurosci Lett 2010, 469:333-337.
22. Hatazaki S., Bellver-Estelles C., Jimenez-Mateos E.M., Meller R., Bonner C., Murphy N., Matsushima S., Taki W., Prehn J.H., Simon R.P., Henshall D.C. Microarray profile of seizure damage-refractory hippocampal CA3 in a mouse model of epileptic preconditioning. Neuroscience 2007, 150:467-477.
23. Henshall D.C., Murphy B.M. Modulators of neuronal cell death in epilepsy. Curr Opin Pharmacol 2008, 8:75-81.
24. Henshall D.C., Sinclair J., Simon R.P. Spatio-temporal profile of DNA fragmentation and its relationship to patterns of epileptiform activity following focally evoked limbic seizures. Brain Res 2000, 858:290-302.
25. Heo K., Cho Y.J., Cho K.J., Kim H.W., Kim H.J., Shin H.Y., Lee B.I., Kim G.W. Minocycline inhibits caspase-dependent and -independent cell death pathways and is neuroprotective against hippocampal damage after treatment with kainic acid in mice. Neurosci Lett 2006, 398:195-200.
26. Ishimaru M.J., Ikonomidou C., Tenkova T.I., Der T.C., Dikranian K., Sesma M.A., Olney J.W. Distinguishing excitotoxic from apoptotic neurodegeneration in the developing rat brain. J Comp Neurol 1999, 408:461-476.
27. Joza N., Susin S.A., Daugas E., Stanford W.L., Cho S.K., Li C.Y., Sasaki T., Elia A.J., Cheng H.Y., Ravagnan L., Ferri K.F., Zamzami N., Wakeham A., Hakem R., Yoshida H., Kong Y.Y., Mak T.W., Zuniga-Pflucker J.C., Kroemer G., Penninger J.M. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 2001, 410:549-554.
28. Kane D.J., Ord T., Anton R., Bredesen D.E. Expression of bcl-2 inhibits necrotic neural cell death. J Neurosci Res 1995, 40:269-275.
29. Kondratyev A., Gale K. Latency to onset of status epilepticus determines molecular mechanisms of seizure-induced cell death. Brain Res Mol Brain Res 2004, 121:86-94.
30. Kroemer G., Martin S.J. Caspase-independent cell death. Nat Med 2005, 11:725-730.
31. Kuida K., Haydar T.F., Kuan C.Y., Gu Y., Taya C., Karasuyama H., Su M.S., Rakic P., Flavell R.A. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 1998, 94:325-337.
32. Kuroki K., Virard I., Concannon C.G., Engel T., Woods I., Taki W., Plesnila N., Henshall D.C., Prehn J.H. Effects of transient focal cerebral ischemia in mice deficient in puma. Neurosci Lett 2009, 451:237-240.
33. Landshamer S., Hoehn M., Barth N., Duvezin-Caubet S., Schwake G., Tobaben S., Kazhdan I., Becattini B., Zahler S., Vollmar A., Pellecchia M., Reichert A., Plesnila N., Wagner E., Culmsee C. Bid-induced release of AIF from mitochondria causes immediate neuronal cell death. Cell Death Differ 2008, 15:1553-1563.
34. Liou A.K., Zhou Z., Pei W., Lim T.M., Yin X.M., Chen J. BimEL up-regulation potentiates AIF translocation and cell death in response to MPTP. FASEB J 2005, 19:1350-1352.
35. Liou A.K.F., Clark R.S., Henshall D.C., Yin X.M., Chen J. To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways. Prog Neurobiol 2003, 69:103-142.
36. Meldrum B. Excitotoxicity and epileptic brain damage. Epilepsy Res 1991, 10:55-61.
37. Meldrum B.S. Excitotoxicity and selective neuronal loss in epilepsy. Brain Pathol 1993, 3:405-412.
38. Meldrum B.S. Implications for neuroprotective treatments. Prog Brain Res 2002, 135:487-495.
39. Mikati M.A., Zeinieh M., Habib R.A., El Hokayem J., Rahmeh A., El Sabban M., Usta J., Dbaibo G. Changes in sphingomyelinases, ceramide, Bax, Bcl(2), and caspase-3 during and after experimental status epilepticus. Epilepsy Res 2008, 81:161-166.
40. Murphy B., Dunleavy M., Shinoda S., Schindler C., Meller R., Bellver-Estelles C., Hatazaki S., Dicker P., Yamamoto A., Koegel I., Chu X., Wang W., Xiong Z., Prehn J., Simon R., Henshall D. Bcl-w protects hippocampus during experimental status epilepticus. Am J Pathol 2007, 171:1258-1268.
41. Murphy B.M., Engel T., Paucard A., Hatazaki S., Mouri G., Tanaka K., Tuffy L.P., Jimenez-Mateos E.M., Woods I., Dunleavy M., Bonner H.P., Meller R., Simon R.P., Strasser A., Prehn J.H., Henshall D.C. Contrasting patterns of Bim induction and neuroprotection in Bim-deficient mice between hippocampus and neocortex after status epilepticus. Cell Death Differ 2010, 17:459-468.
42. Narkilahti S., Jutila L., Alafuzoff I., Karkola K., Paljarvi L., Immonen A., Vapalahti M., Mervaala E., Kalviainen R., Pitkanen A. Increased expression of caspase 2 in experimental and human temporal lobe epilepsy. Neuromolecular Med 2007, 9:129-144.
43. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2001, Elsevier, San Diego, CA. 2nd ed.
44. Portera-Cailliau C., Price D.L., Martin L.J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 1997, 378:70-87.
45. Schindler C.K., Pearson E.G., Bonner H.P., So N.K., Simon R.P., Prehn J.H., Henshall D.C. Caspase-3 cleavage and nuclear localization of caspase-activated DNase in human temporal lobe epilepsy. J Cereb Blood Flow Metab 2006, 26:583-589.
46. Shinoda S., Araki T., Lan J.Q., Schindler C.K., Simon R.P., Taki W., Henshall D.C. Development of a model of seizure-induced hippocampal injury with features of programmed cell death in the BALB/c mouse. J Neurosci Res 2004, 76:121-128.
47. Shinoda S., Schindler C.K., Meller R., So N.K., Araki T., Yamamoto A., Lan J.Q., Taki W., Simon R.P., Henshall D.C. Bim regulation may determine hippocampal vulnerability after injurious seizures and in temporal lobe epilepsy. J Clin Invest 2004, 113:1059-1068.
48. Single B., Leist M., Nicotera P. Differential effects of bcl-2 on cell death triggered under ATP-depleting conditions. Exp Cell Res 2001, 262:8-16.
49. Sloviter R.S. Hippocampal epileptogenesis in animal models of mesial temporal lobe epilepsy with hippocampal sclerosis: the importance of the "latent period" and other concepts. Epilepsia 2008, 49(Suppl 9):85-92.
50. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
51. Tanaka K., Jimenez-Mateos E.M., Matsushima S., Taki W., Henshall D.C. Hippocampal damage after intra-amygdala kainic acid-induced status epilepticus and seizure preconditioning-mediated neuroprotection in SJL mice. Epilepsy Res 2010, 88:151-161.
52. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008, 9:231-241.
53. Villunger A., Michalak E.M., Coultas L., Mullauer F., Bock G., Ausserlechner M.J., Adams J.M., Strasser A. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003, 302:1036-1038.
54. Wang S., Wang S., Shan P., Song Z., Dai T., Wang R., Chi Z. Mu-calpain mediates hippocampal neuron death in rats after lithium-pilocarpine-induced status epilepticus. Brain Res Bull 2008, 76:90-96.
55. Wang Y.F., Jiang C.C., Kiejda K.A., Gillespie S., Zhang X.D., Hersey P. Apoptosis induction in human melanoma cells by inhibition of MEK is caspase-independent and mediated by the Bcl-2 family members PUMA, Bim, and Mcl-1. Clin Cancer Res 2007, 13:4934-4942.
56. Ward M.W., Huber H.J., Weisova P., Dussmann H., Nicholls D.G., Prehn J.H. Mitochondrial and plasma membrane potential of cultured cerebellar neurons during glutamate-induced necrosis, apoptosis, and tolerance. J Neurosci 2007, 27:8238-8249.
57. Wasterlain C.G., Fujikawa D.G., Penix L., Sankar R. Pathophysiological mechanisms of brain damage from status epilepticus. Epilepsia 1993, 34:S37-S53.
58. Willis S.N., Fletcher J.I., Kaufmann T., van Delft M.F., Chen L., Czabotar P.E., Ierino H., Lee E.F., Fairlie W.D., Bouillet P., Strasser A., Kluck R.M., Adams J.M., Huang D.C. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007, 315:856-859.
59. Yamamoto A., Murphy N., Schindler C.K., So N.K., Stohr S., Taki W., Prehn J.H., Henshall D.C. Endoplasmic reticulum stress and apoptosis signaling in human temporal lobe epilepsy. J Neuropathol Exp Neurol 2006, 65:217-225.
60. Yang T., Hsu C., Liao W., Chuang J.S. Heat shock protein 70 expression in epilepsy suggests stress rather than protection. Acta Neuropathol 2008, 115:219-230.
61. Zhao S., Aviles E.R., Fujikawa D.G. Nuclear translocation of mitochondrial cytochrome c, lysosomal cathepsins B and D, and three other death-promoting proteins within the first 60 minutes of generalized seizures. J Neurosci Res 2010, in press.
62. Zhong L.T., Sarafian T., Kane D.J., Charles A.C., Mah S.P., Edwards R.H., Bredesen D.E. bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl Acad Sci U S A 1993, 90:4533-4537.