Differential effects of ethanol on c-jun N-terminal kinase, 14-3-3 proteins, and Bax in postnatal day 4 and postnatal day 7 rat cerebellum

Brain Research

Volumn 1432, Issue , 2012, Pages 15-27

  Heaton, Marieta Barrow ^a,b,c   Paiva, Michael ^a,b,c   Kubovic, Stacey ^a   Kotler, Alexandra ^a   Rogozinski, Jonathan ^a   Swanson, Eric ^a   Madorsky, Vladimir ^a   Posados, Michelle ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b McKnight Brain Institute   (United States)

^c Center for Alcohol Research   (United States)

Author keywords

Apoptosis; Cerebellum; Ethanol; Fetal alcohol syndrome

Indexed keywords

ALCOHOL; HETERODIMER; PROTEIN 14 3 3; PROTEIN BAX; STRESS ACTIVATED PROTEIN KINASE;

ALCOHOL BLOOD LEVEL; ALCOHOL INTOXICATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOSOL; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GRANULE CELL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUROTOXICITY; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

14-3-3 PROTEINS; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CEREBELLUM; ETHANOL; FEMALE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; PRIMARY CELL CULTURE; PROTEIN KINASE INHIBITORS; RATS; RATS, LONG-EVANS;

ANIMALIA; RATTUS;

EID: 84655169841     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.11.010     Document Type: Article

References (62)

1. D.L. Andrews, G.S. Williams, J.C. Mahoney, and J.R. West DNA fragmentation during exposure of rat cerebella to ethanol under hypoxia imposed in vitro J. Neurobiol. 8 1999 82 92 (Pubitemid 29016816)
2. M. Ankarcrona, J.M. Dypbukt, E. Bonfoco, B. Zhivotovsky, S. Orrenius, S.A. Lipton, and P. Nicotera Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function Neuron 15 1995 961 973
3. B.L. Bennett, D.T. Sasaki, B.W. Murray, E.C. O'Leary, S.T. Sakata, W. Xu, J.C. Leisten, A. Motiwala, S. Pierce, Y. Satoh, S.S. Bhagwat, A.M. Manning, and D.W. Anderson SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase Proc. Natl. Acad. Sci. U. S. A. 98 2001 13681 13686 (Pubitemid 33115958)
4. D.J. Bonthius, and J.R. West Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt Teratology 44 1991 147 163
5. S.M. de la Monte, N. Ganju, K. Banerjee, N.V. Brown, T. Luong, and J.R. Wands Partial rescue of ethanol-induced neuronal apoptosis by growth factor activation of phosphoinositol-3-kinase Alcohol. Clin. Exp. Res. 24 2000 716 726 (Pubitemid 30337768)
6. R.J. Ferl 14-3-3 Proteins and signal transduction Annu Rev Plant Physiol Plant Mol Biol. 47 1996 49 73
7. G. Gao, and Q.P. Duo N-terminal cleavage of Bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes Bcl-2-independent cytochrome C release and apoptotic cell death J. Cell. Biochem. 80 2000 53 72
8. Y. Gao, A.P. Signore, W. Yin, G. Cao, X.M. Yin, F. Sun, Y. Luo, S.H. Graham, and J. Chen Neuroprotection against focal ischemic brain injury by inhibition of c-jun N-terminal kinase and attenuation of the mitochondrial apoptosis-signaling pathway J. Cereb. Blood Flow Metab. 25 2005 694 712 (Pubitemid 40705605)
9. Y. Ge, S.M. Belcher, D.R. Pierce, and K.E. Light Altered expression of Bcl-2, Bad and Bax mRNA occurs in the rat cerebellum within hours after ethanol exposure on postnatal day 4 but not on postnatal day 9 Mol. Brain Res. 129 2004 124 134 (Pubitemid 39304256)
10. C.R. Goodlett, and A.T. Eilers Alcohol-induced Purkinje cell loss with a single binge exposure in neonatal rats: a stereological study of temporal windows of vulnerability Alcohol. Clin. Exp. Res. 2 1997 738 744 (Pubitemid 27272806)
11. C.R. Goodlett, B.L. Marcussen, and J.R. West A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss Alcohol 7 1990 107 114 (Pubitemid 20155636)
12. A. Gross, J.M. McDonnell, and S.T. Korsmeyer Bcl-2 family members and the mitochondria in apoptosis Genes Dev. 12 1999 1899 1911 (Pubitemid 29407357)
13. J.Y. Han, J.Y. Jeong, Y.K. Lee, G.S. Roh, H.J. Kim, S.S. Kang, G.J. Cho, and W.S. Choi Suppression of survival kinases and activation of JNK mediate ethanol-induced cell death in the developing rat brain Neurosci. Lett. 39 2006 113 117
14. J.Y. Han, E.Y. Jeong, Y.S. Kim, G.S. Roh, H.J. Kim, S.S. Kang, G.J. Cho, and W.S. Choi C-jun N-terminal kinase regulates the interaction between 14-3-3 and Bad in ethanol-induced cell death J. Neurosci. Res. 86 2008 3221 3229
15. M.B. Heaton, J.J. Mitchell, M. Paiva, and D.W. Walker Ethanol-induced alterations in the expression of neurotrophic factors in the developing rat central nervous system Brain Res. Dev. Brain Res. 121 2000 97 107 (Pubitemid 30317420)
16. M.B. Heaton, D.B. Moore, M. Paiva, I. Madorsky, J. Mayer, and G. Shaw The role of neurotrophic factors, apoptosis-related proteins, and endogenous antioxidants in the differential temporal vulnerability of neonatal cerebellum to ethanol Alcohol. Clin. Exp. Res. 27 2003 657 669 (Pubitemid 36460705)
17. M.B. Heaton, M. Paiva, I. Madorsky, and G. Shaw Ethanol effects on neonatal rat cortex: comparative analyses of neurotrophic factors, apoptosis-related proteins, and oxidative processes during vulnerable and resistant periods Brain Res. Dev. Brain Res. 145 2003 249 262 (Pubitemid 37357134)
18. M.B. Heaton, M. Paiva, I. Madorsky, J. Mayer, and D.B. Moore Effects of ethanol on neurotrophic factors, apoptosis-related proteins, endogenous antioxidants, and reactive oxygen species in neonatal striatum: relationship to periods of vulnerability Brain Res. Dev. Brain Res. 140 2003 237 252 (Pubitemid 36173981)
19. M.B. Heaton, M. Paiva, I. Madorsky, K. Siler-Marsiglio, and G. Shaw The effect of Bax deletion on ethanol sensitivity in the neonatal rat cerebellum J. Neurobiol. 66 2006 95 101 (Pubitemid 41829031)
20. M.B. Heaton, M. Paiva, and K. Siler-Marsiglio Ethanol influences on Bax translocation, mitochondrial membrane potential, and reactive oxygen species generation are modulated by vitamin E and brain-derived neurotrophic factor Alcohol. Clin. Exp. Res. 35 2011 1122 1133
21. Y.T. Hsu, and R.J. Youle Nonionic detergents induce dimerization among members of the Bcl-2 family J. Biol. Chem. 272 1997 13829 13834 (Pubitemid 27224822)
22. Y.T. Hsu, and R.J. Youle Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations J. Biol. Chem. 273 1998 10777 10783 (Pubitemid 28227695)
23. M. Inoue, K. Nakamura, K. Iwahashi, K. Ameno, M. Itoh, and H. Suwaki Changes of Bcl-2 and Bax mRNA expressions in the ethanol-treated mouse brain Nihon Arukoru Yakubutsu Igakkai Zasshi 37 2002 120 129
24. Y.T. Ip, and R.J. Davis Signal transduction by the c-jun N-terminal kinase (JNK) - from inflammation to development Curr. Opin. Cell Biol. 10 1998 205 219 (Pubitemid 28174763)
25. K.L. Jones, and D.W. Smith Recognition of the fetal alcohol syndrome in early infancy Lancet 1973 999 1000
26. Y.J. Lee, and S.D. Shukla Pro- and anti-apoptotic roles of c-Jun N-terminal kinase (JNK) in ethanol and acetaldehyde exposed rat hepatocytes Eur. J. Pharmacol. 508 2005 31 45 (Pubitemid 40169900)
27. H.Y. Lee, N. Naha, J.H. Kim, M.J. Jo, K.S. Min, H.H. Seong, D.H. Shin, and M.O. Kim Age- and area-dependent distinct effects of ethanol on Bax and Bcl-2 expression in prenatal rat brain J. Microbiol. Biotechnol. 18 2008 1590 1598
28. B. Lindblad, and R. Olsson Unusually high levels of blood alcohol? JAMA 236 1976 1600 1602
29. Y. Liu, R.F. Tian, Y.M. Li, W.P. Liu, L. Cao, X.L. Yang, W.D. Cao, and X. Zhang The expression of seven 14-3-3 isoforms in human meningioma Brain Res. 1336 2010 98 102
30. M. Manthorpe, R. Fagnani, S.D. Skaper, and S. Varon An automated colorimetric microassay for neuronotrophic factors Brain Res. 390 1986 191 198 (Pubitemid 16188172)
31. I. Marzo, C. Brenner, N. Zamzami, J.M. Jurgensmeier, S.A. Susin, H.L.A. Vieira, M.-C. Prevost, Z. Xie, S. Matsuyama, J.C. Reed, and G. Kroemer Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis Science 281 1998 2027 2031 (Pubitemid 28475490)
32. S.C. Masters, and H. Fu 14-3-3 proteins mediate an essential anti-apoptotic signal J. Biol. Chem. 276 2001 45193 45200
33. R.E. McAlhany, J.R. West, and R.C. Miranda Glial-derived neurotrophic factor (GDNF) prevents ethanol-induced apoptosis and jun kinase phosphorylation Brain Res. Dev. Brain Res. 119 2000 209 216 (Pubitemid 30089811)
34. J.J. Mitchell, M. Paiva, and M.B. Heaton Optimal 96-well plate set-up to avoid ethanol volatility when assessing ethanol cytotoxicity Alcohol 15 1998 137 139 (Pubitemid 28099245)
35. J.J. Mitchell, M. Paiva, D.W. Walker, and M.B. Heaton BDNF and NGF afford in vitro neuroprotection against ethanol combined with acute ischemia and chronic hypoglycemia Dev. Neurosci. 21 1999 68 75 (Pubitemid 29121752)
36. B.W. Moore, and V.J. Perez Specific acidic proteins of the nervous system F.D. Carlson, Physiological and Biochemical Aspects of Nervous Integration 1967 Prentice-Hall 343 359
37. D.B. Moore, D.W. Walker, and M.B. Heaton Neonatal ethanol exposure alters Bcl-2 family mRNA levels in the rat cerebellar vermis Alcohol. Clin. Exp. Res. 23 1999 1251 1261 (Pubitemid 29352815)
38. T. Mosmann Rapid colorimetric assay for cellular growth and survival: applications to proliferation and cytotoxicity assays J. Immunol. Methods 65 1983 55 63 (Pubitemid 14203433)
39. Y. Muller, K. Tangre, and J. Clos Autocrine regulation of apoptosis and Bcl-2 expression by nerve growth factor in early differentiating cerebellar granule neurons involves low affinity neurotrophin receptor Neurochem. Int. 31 1997 177 191 (Pubitemid 27267958)
40. A.J. Muslin, J.W. Tanner, P.M. Allen, and A.S. Shaw Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine Cell 84 1996 889 897 (Pubitemid 26106858)
41. K. Namikawa, Q. Su, S. Kiryu-Seo, and H. Kiyama Enhanced expression of 14-3-3 family members in injured motoneurons Mol. Brain Res. 55 1998 315 320 (Pubitemid 28248048)
42. Y. Nishitani, and H. Matsumoto Ethanol rapidly causes activation of JNK associated with ER stress under inhibition of ADH FEBS Lett. 580 2006 9 14 (Pubitemid 43005304)
43. Y. Nishitani, S. Okazaki, K. Imabayashi, R. Katada, and H. Matsumoto Ethanol-induced JNK activation suppressed via active akt in hepatocytes Nihon Arukoru Yakubutsu Igakkai Zasshi 43 2008 35 43
44. M. Nomura, S. Shimizu, T. Sugiyama, M. Narita, T. Ito, H. Matsuda, and Y. Tsujimoto 14-3-3 interacts directly with and negatively regulates pro-apoptotic Bax J. Biol. Chem. 278 2003 2058 2065 (Pubitemid 36801450)
45. L. Nowoslawski, B.J. Klocke, and K.A. Roth Molecular regulation of acute ethanol-induced neuron apoptosis J. Neuropathol. Exp. Neurol. 64 2005 490 497 (Pubitemid 40781151)
46. J. Oberdoerster, and R.A. Rabin Enhanced caspase activity during ethanol-induced apoptosis in rat cerebellar granule cells Eur. J. Pharmacol. 385 1999 273 282
47. J.W. Olney, D.F. Wozniak, V. Jevtovic-Todorovic, and C. Ikonomidou Glutamate signaling and the fetal alcohol syndrome Ment. Retard. Dev. Disabil. Res. Rev. 7 2001 267 275 (Pubitemid 33108265)
48. J.W. Olney, T. Tenkova, K. Dikranian, L.J. Muglia, W.J. Jermakowicz, C. D'Sa, and A. Roth Ethanol-induced caspase-3 activation in the in vivo developing mouse brain Neurobiol. Dis. 9 2002 205 219 (Pubitemid 34261215)
49. E.S. Papadakis, K.G. Finegan, X. Wang, A.C. Robinson, C. Guo, M. Kayahara, and C. Tournier The regulation of Bax by c-jun N-terminal protein kinase (JNK) is a prerequisite to the mitochondrial-induced apoptotic pathway FEBS Lett. 580 2006 1320 1326 (Pubitemid 43221994)
50. D.R. Pierce, D.K. Williams, and K.E. Light Purkinje cell vulnerability to developmental ethanol exposure in the rat cerebellum Alcohol. Clin. Exp. Res. 23 1999 1650 1659 (Pubitemid 29498651)
51. G. Pimienta, and J. Pascual Canonical and alternative MAPK signaling Cell Cycle 6 2007 2628 2632 (Pubitemid 350224045)
52. B.M. Polster, and G. Fiskum Mitochondrial mechanisms of neural cell apoptosis J. Neurochem. 90 2004 1281 1289 (Pubitemid 39223632)
53. X. Roucou, P.N. Giannopoulos, Y. Zhang, J. Jodoin, C.G. Goodyer, and A. LeBlanc Cellular prion protein inhibits proapoptotic Bax conformational change in human neurons and in breast carcinoma MCF-7 cells Cell Death Differ. 12l 2005 783 795 (Pubitemid 40945985)
54. C.K. Schindler, S. Shinoda, R.P. Simon, and D.C. Henshall Subcellular distribution of Bcl-2 family proteins and 14-3-3 within the hippocampus during seizure-induced neuronal death in the rat Neurosci. Lett. 356 2004 163 166 (Pubitemid 38186677)
55. K.I. Siler-Marsiglio, G. Shaw, and M.B. Heaton Pycnogenol and vitamin E inhibit ethanol-induced apoptosis in rat cerebellar granule cells J. Neurobiol. 59 2004 261 271 (Pubitemid 38656990)
56. K.I. Siler-Marsiglio, M. Paiva, I. Madorsky, Q. Pan, G. Shaw, and M.B. Heaton Functional mechanisms of apoptosis-related proteins in neonatal rat cerebellum are differentially influenced by ethanol at postnatal day 4 and 7 J. Neurosci. Res. 81 2005 632 643 (Pubitemid 41532159)
57. K.I. Siler-Marsiglio, Q. Pan, M. Paiva, A.W. Neeley, G. Shaw, and M.B. Heaton Effects of acute ethanol exposure on regulatory mechanisms of Bcl-2-associated apoptosis promoter, Bad, in neonatal rat cerebellum: differential effects during vulnerable and resistant developmental periods Alcohol. Clin. Exp. Res. 30 2006 1031 1038 (Pubitemid 43823265)
58. C.J. Stephens Alcohol consumption during pregnancy among southern city women Drug Alcohol Depend. 16 1985 19 29 (Pubitemid 16256173)
59. J. Sunayama, F. Tsuruta, N. Masuyama, and Y. Gotoh JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3 J. Cell Biol. 170 2005 295 304 (Pubitemid 41043811)
60. F. Tsuruta, J. Sunayama, Y. Mori, S. Hattori, S. Shimizu, Y. Tsujimoto, K. Yoshioka, N. Masuyama, and Y. Gotoh JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins EMBO J. 23 2004 1889 1899 (Pubitemid 38649651)
61. M. Watanabe, T. Isobe, T. Ichimura, R. Kuwano, Y. Takahashi, H. Kondo, and Y. Inoue Molecular cloning of rat cDNAs for the zeta and theta subtypes of 14-3-3 protein and differential distributions of their mRNAs in the brain Brain Res. Mol. Brain Res. 25 1994 113 121
62. C. Young, B.J. Klocke, T. Tenkova, J. Choi, J. Labruyere, Y.Q. Qin, D.M. Holtzman, K.A. Roth, and J.W. Olney Ethanol-induced neuronal apoptosis in vivo requires Bax in the developing mouse brain Cell Death Differ. 10 2003 1148 1155 (Pubitemid 37258580)