Deletion of the c-Jun N-terminal kinase 3 gene protects neonatal mice against cerebral hypoxic-ischaemic injury

Journal of Cerebral Blood Flow and Metabolism

Volumn 27, Issue 5, 2007, Pages 1022-1032

  Pirianov, Grisha ^a,b   Brywe, Katarina G ^c   Mallard, Carina ^c   Edwards, David ^b   Flavell, Richard A ^d   Hagberg, Henrik ^c   Mehmet, Huseyin ^a,b  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Brain; c Jun N terminal kinase; Hypoxia ischaemia; Neonatal

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BIM PROTEIN; CASPASE 3; MITOGEN ACTIVATED PROTEIN KINASE 10; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN MATURATION; CAROTID ARTERY OBSTRUCTION; CELL LOSS; COMPARATIVE STUDY; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; GENE DELETION; HIPPOCAMPUS; KNOCKOUT MOUSE; MOUSE; NERVE CELL; NERVOUS TISSUE; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; THALAMUS; WILD TYPE;

ACTIVATING TRANSCRIPTION FACTOR 2; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN; HYPOXIA-ISCHEMIA, BRAIN; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 10; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 34247503156     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600413     Document Type: Article

References (40)

1. Back SA, Gan X, Li Y, Rosenberg PA, Volpe JJ (1998) Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 18:6241-53
2. Becker EB, Howell J, Kodama Y, Barker PA, Bonni A (2004) Characterization of the c-Jun N-terminal kinase-BimEL signaling pathway in neuronal apoptosis. J Neurosci 24:8762-70
3. Borsello T, Clarke PG, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischaemia. Nat Med 9:1180-6
4. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96(6):857-68
5. Brywe KG, Leverin AL, Gustavsson M, Mallard C, Granata R, Destefanis S, Volante M, Hagberg H, Ghigo E, Isgaard J (2005a) Growth hormone-releasing peptide hexarelin reduces neonatal brain injury and alters Akt/glycogen synthase kinase-3beta phosphorylation. Endocrinology 146(11):4665-72
6. Brywe KG, Mallard C, Gustavsson M, Hedtjarn M, Leverin AL, Wang X, Blomgren K, Isgaard J, Hagberg H (2005b) IGF-I neuroprotection in the immature brain after hypoxia-ischemia, involvement of Akt and GSK3beta? Eur J Neurosci 21(6):1489-502
7. Buschmann T, Potapova O, Bar-Shira A, Ivanov VN, Fuchs SY, Henderson S, Fried VA, Minamoto T, Alarcon-Vargas D, Pincus MR, Gaarde WA, Holbrook NJ, Shiloh Y, Ronai Z (2001) Jun NH2-terminal kinase phosphorylation of p53 on Thr-81 is important for p53 stabilization and transcriptional activities in response to stress. Mol Cell Biol 21(8):2743-54
8. Carboni S, Antonsson B, Gaillard P, Gotteland JP, Gillon JY, Vitte PA (2005) Control of death receptor and mitochondrial-dependent apoptosis by c-Jun N-terminal kinase in hippocampal CA1 neurones followingglobal transient ischaemia. J Neurochem 92(5):1054-60
9. Davis RJ (2000) Signal transduction by the JNK group of MAPK. Cell 103:239-52
10. Derijard M, Hibi LH, Wu T, Barrett B, Su T, Deng M, Karin M, Davis RJ (1994) JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates c-Jun activation domain. Cell 76:1025-37
11. Dreskin SC, Thomas GW, Dale SN, Heasley LE (2001) Isoforms of JNK kinase are differentially expressed and activated in human monocyte/microphage (THP-1) cells. J Immunol 166:5646-53
12. Edwards AD, Mehmet H (1996) Apoptosis in perinatal hypoxic-ischaemic cerebral damage. Neuropathol Appl Neurobiol 22(6):494-8
13. Essers MA, Weijzen S, de Vries-Smits AM, Saarloos I, de Ruiter ND, Bos JL, Burgering B (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 23(24):4802-12
14. Ham J, Eilders A, Whifield J, Neame S, Shah B (2000) C-jun and transcriptional control of neuronal apoptosis. Biochem Pharmacol 60:1015-21
15. Han B, Choi J, Holtzman DM (2002) Evidence that p38 mitogen-activated protein kinase contributes to neonatal hypoxic-ischemic brain injury. Dev Neurosci 24(5):405-10
16. Harrington AW, Kim JY, Yoon SO (2002) Activation of Rac GTPase by p75 is necessary for c-Jun N-terminal kinase-mediated apoptosis. J Neurosci 22(1):156-66
17. Hedtjärn M, Leverin AL, Eriksson K, Blomgren K, Mallard C, Hagberg H (2002) Interleukin-18 involvement in hypoxic-ischaemic brain Injury. J Neurosci 22:5910-9
18. Herdegen T, Claret FX, Kallunki T, Martin-Villalba A, Winter C, Hunter T, Karin M (1998) Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N-terminal kinases after neuronal injury. J Neurosci 18:5124-35
19. Gill R, Soriano M, Blomgren K, Hagberg H, Wybrecht R, Miss MT, Hoefer S, Adam G, Niederhauser O, Kemp J, Loetscher H (2002) Role of caspase-3 activation in cerebral ischaemia-induced neurodegeneration in adult and neonatal brain. J Cereb Blood Flow Metab 22:420-30
20. Irving EA, Bamford M (2002) Role of mitogen- and stress-activated kinases in ischemic injury. J Cereb Blood Flow Metab 22:631-47
21. Jeffers JR, Parganas E, Lee Y, Yang C, Wang J, Brennan J, MacLean KH, Han J, Chittenden T, Ihle JN, McKinnon PJ, Cleveland JL, Zambetti GP (2003) Puma is an essential mediator of p53-dependent and -independent apoptotic pathway. Cancer Cell 4(4):321-8
22. Kuan CY, Whitmarsh AJ, Yang DD, Liao G, Schloemer AJ, Dong C, Bao J, Banasiak KJ, Haddad GG, Flavell RA, Davis RJ, Rakic P (2003) A critical role of neural-specific JNK3 for ischaemic apoptosis. Proc Natl Acad Sci USA 100:15184-9
23. Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA (1999) The role of cell death in regulating the size and shape of the mammalian forebrain. Neuron 22:667-76
24. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, Ahmad MF, Avruch J, Woodgett JR (1994) The stress-activated protein kinases subfamily of c-Jun kinases. Nature 369:156-60
25. Lei K, Davis RJ (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 100(5):2432-7
26. Noshita N, Lewen A, Sugawara T, Chan PH (2001) Evidence of phosphorylation of Akt and neuronal survival after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 21:1442-50
27. Nozaki K, Nishimora M, Hashimoto N (2001) MAPK in cerebral ischaemia. Mol Neurobiol 23(1):1-19
28. Ouyang YB, Tan Y, Comb M, Liu CL, Martone ME, Siesjo BK, Hu BR (1999) Survival- and death-promoting events after transient cerebral ischaemia: phosphorylation of Akt, release of cytochrome C and activation of caspase-like proteases. J Cereb Blood Flow Metab 19(10):1126-35
29. Pirianov G, Jesurasa A, Mehmet H (2006) Developmentally regulated changes in c-jun N-terminal kinase activation during stress-induced apoptosis of oligodendrocyte lineage cells. Cell Death Differ 13(3):531-3
30. Reimertz C, Kogel D, Rami A, Chittenden T, Prehn JH (2003) Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol 162:587-97
31. Rice JE, Vannucci RC, Brierley JB (1981) The influence of immaturity on hypoxic-ischaemic brain damage in the rat. Ann Neurol 9:131-41
32. Sanchez I, Hughes RT, Mayer BJ, Yee K, Woodgett JR, Avruch J, Kariakis JM, Zon LI (1994) Role of SAPK/ERK in stress-activated pathway regulating transcription factor c-jun. Nature 372:794-8
33. Song JJ, Lee YJ (2005) Dissociation of Akt1 from its negative regulator JIP1 is mediated through the ASK1-MEK-JNK signal transduction pathway during metabolic oxidative stress: a negative feedback loop. J Cell Biol 170:61-72
34. Takita M, Puka-Sundvall M, Miyakawa A, Hagberg H (2004) In vivo calcium imaging of cerebral cortex in hypoxia-ischaemia followed by developmental stage specific injury in rats. Neurosci Res 48:169-73
35. Volpe JJ (1981) Neurology of the newborn. Major Probl Clin Pediatr 22:1-648
36. Wagey RTE, Krieger C (1998) Abnormalities of protein kinases in neurodegenerative diseases. Prog Drug Res 51:158-64
37. Whitfield J, Neame SJ, Paquet L, Bernard O, Ham J (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29:629-43
38. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-31
39. Xu X, Raber J, Yang D, Su B, Mucke L (1997) Dynamic regulation of c-Jun N-terminal kinase activity in mouse brain by environmental stimuli. Proc Natl Acad Sci USA 94:12655-60
40. Yang DD, Kuan CY, Whitmarsh J, Rincon M, Zheng TS, Davis RJ, Rakic P, Flavell RA (1997) Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389:865-70