Estradiol increases expression of the brain-derived neurotrophic factor after acute administration of ethanol in the neonatal rat cerebellum

European Journal of Pharmacology

Volumn 732, Issue 1, 2014, Pages 1-11

  Firozan, Bita ^a   Goudarzi, Iran ^a   Elahdadi Salmani, Mahmoud ^a   Lashkarbolouki, Taghi ^a   Rezaei, Arezou ^a   Abrari, Kataneh ^a  

^a DAMGHAN UNIVERSITY   (Iran)

Author keywords

17 estradiol; Brain derived neurotrophic factor; Ethanol; Neuroprotection; Purkinje cell

Indexed keywords

ALCOHOL; BRAIN DERIVED NEUROTROPHIC FACTOR; COMPLEMENTARY DNA; ESTRADIOL; MESSENGER RNA; CENTRAL DEPRESSANT AGENT; NEUROPROTECTIVE AGENT;

ALCOHOL BLOOD LEVEL; ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; CELL LOSS; CEREBELLUM; CONTROLLED STUDY; DNA SYNTHESIS; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL LOCOMOTOR ACTIVITY TEST; FEMALE; HISTOLOGY; MALE; MOTOR DYSFUNCTION; NEUROPROTECTION; NEWBORN; NONHUMAN; OPEN FIELD TEST; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; ROTAROD TEST; ANIMAL; BLOOD; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PSYCHOMOTOR PERFORMANCE; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CEREBELLUM; ESTRADIOL; ETHANOL; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; PSYCHOMOTOR PERFORMANCE; RATS; SIGNAL TRANSDUCTION;

EID: 84897356952     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.02.041     Document Type: Article

References (65)

1. S. Asimiadou, P. Bittigau, U. Felderhoff-Mueser, D. Manthey, M. Sifringer, S. Pesditschek, M. Dzietko, A.M. Kaindl, M. Pytel, D. Studniarczyk, J.W. Mozrzymas, and C. Ikonomidou Protection with estradiol in developmental models of apoptotic neurodegeneration Ann. Neurol. 58 2005 266 276
2. I. Ben Amara, H. Fetoui, F. Guermazi, and N. Zeghal Dietary selenium addition improves cerebrum and cerebellum impairments induced by methimazole in suckling rats Int. J. Dev. Neurosci.: Off. J. Int. Soc. Dev. Neurosci. 27 2009 719 726
3. N.C. Berchtold, J.P. Kesslak, C.J. Pike, P.A. Adlard, and C.W. Cotman Estrogen and exercise interact to regulate brain-derived neurotrophic factor mRNA and protein expression in the hippocampus Eur. J. Neurosci. 14 2001 1992 2002
4. R.F. Berman, and J.H. Hannigan Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy Hippocampus 10 2000 94 110
5. C. Beyer Estrogen and the developing mammalian brain Anat. Embryol. 199 1999 379 390
6. P. Breton, J.C. Bizot, J. Buee, and I. De La Manche Brain neurotoxicity of Penitrem A: electrophysiological, behavioral and histopathological study Toxicon: Off. J. Int. Soc. Toxinol. 36 1998 645 655
7. M.E. Burger, R. Fachinetto, G. Zeni, and J.B. Rocha Ebselen attenuates haloperidol-induced orofacial dyskinesia and oxidative stress in rat brain Pharmacol. Biochem. Behav. 81 2005 608 615
8. J.D. Chaudhuri Alcohol and the developing fetus - a review Med. Sci. Monit.: Int. Med. J. Exp. Clin. Res. 6 2000 1031 1041
9. S.Y. Chen, and K.K. Sulik Free radicals and ethanol-induced cytotoxicity in neural crest cells Alcohol. Clin. Exp. Res. 20 1996 1071 1076
10. P.D. Connor, P.D. Sampson, A.P. Streissguth, F.L. Bookstein, and H.M. Barr Effects of prenatal alcohol exposure on fine motor coordination and balance: a study of two adult samples Neuropsychologia 44 2006 744 751
11. S.R. Datta, H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M.E. Greenberg Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery Cell 91 1997 231 241
12. Wei Dong, Wei Ning, and Cui-zhen Zhang et al. Effects of estrogen on brain derived neurotrophic factor and neuropeptide Y levels in cerebellar cortex of ovariectomized rats Chin. J. Rehabil. Theory Pract. 11 2008
13. L.M. Ellerby, H.M. Ellerby, S.M. Park, A.L. Holleran, A.N. Murphy, G. Fiskum, D.J. Kane, M.P. Testa, C. Kayalar, and D.E. Bredesen Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2 J. Neurochem. 67 1996 1259 1267
14. W. Fiers, R. Beyaert, W. Declercq, and P. Vandenabeele More than one way to die: apoptosis, necrosis and reactive oxygen damage Oncogene 18 1999 7719 7730
15. W.Q. Gao, J.L. Zheng, and M. Karihaloo Neurotrophin-4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation J. Neurosci.: Off. J. Soc. Neurosci. 15 1995 2656 2667
16. L.M. Garcia-Segura, J.A. Chowen, A. Parducz, and F. Naftolin Gonadal hormones as promoters of structural synaptic plasticity: cellular mechanisms Prog. Neurobiol. 44 1994 279 307
17. Y. Ge, S.M. Belcher, and K.E. Light Alterations of cerebellar mRNA specific for BDNF, p75NTR, and TrkB receptor isoforms occur within hours of ethanol administration to 4-day-old rat pups Brain Res. Dev. Brain Res. 151 2004 99 109
18. 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. 21 1997 738 744
19. C.R. Goodlett, and K.H. Horn Mechanisms of alcohol-induced damage to the developing nervous system Alcohol Res. Health: J. Natl Inst. Alcohol Abuse Alcohol. 25 2001 175 184
20. 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
21. P.S. Green, and J.W. Simpkins Neuroprotective effects of estrogens: potential mechanisms of action Int. J. Dev. Neurosci.: Off. J. Int. Soc. Dev. Neurosci. 18 2000 347 358
22. C. Guegan, I. Ceballos-Picot, E. Chevalier, A. Nicole, B. Onteniente, and B. Sola Reduction of ischemic damage in NGF-transgenic mice: correlation with enhancement of antioxidant enzyme activities Neurobiol. Dis. 6 1999 180 189
23. K.M. Hamre, and J.R. West The effects of the timing of ethanol exposure during the brain growth spurt on the number of cerebellar Purkinje and granule cell nuclear profiles Alcohol. Clin. Exp. Res. 17 1993 610 622
24. 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
25. M.B. Heaton, M. Paiva, D.J. Swanson, and D.W. Walker Modulation of ethanol neurotoxicity by nerve growth factor Brain Res. 620 1993 78 85
26. R. Heumann Neurotrophin signalling Curr. Opin. Neurobiol. 4 1994 668 679
27. A. Hochman, H. Sternin, S. Gorodin, S. Korsmeyer, I. Ziv, E. Melamed, and D. Offen Enhanced oxidative stress and altered antioxidants in brains of Bcl-2-deficient mice J. Neurochem. 71 1998 741 748
28. S.W. Jacobson, M.E. Stanton, C.D. Molteno, M.J. Burden, D.S. Fuller, H.E. Hoyme, L.K. Robinson, N. Khaole, and J.L. Jacobson Impaired eyeblink conditioning in children with fetal alcohol syndrome Alcohol. Clin. Exp. Res. 32 2008 365 372
29. D.R. Kaplan, and F.D. Miller Neurotrophin signal transduction in the nervous system Curr. Opin. Neurobiol. 10 2000 381 391
30. R. Klein, D. Conway, L.F. Parada, and M. Barbacid The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain Cell 61 1990 647 656
31. S.J. Lee, and B.S. McEwen Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications Annu. Rev. Pharmacol. Toxicol. 41 2001 569 591
32. Y. Lee, J. Rowe, K. Eskue, J.R. West, and S.E. Maier Alcohol exposure on postnatal day 5 induces Purkinje cell loss and evidence of Purkinje cell degradation in lobule I of rat cerebellum Alcohol 42 2008 295 302
33. K.E. Light, S.M. Belcher, and D.R. Pierce Time course and manner of Purkinje neuron death following a single ethanol exposure on postnatal day 4 in the developing rat Neuroscience 114 2002 327 337
34. K.E. Light, D.P. Brown, B.W. Newton, S.M. Belcher, and C.J. Kane Ethanol-induced alterations of neurotrophin receptor expression on Purkinje cells in the neonatal rat cerebellum Brain Res. 924 2002 71 81
35. K.E. Light, Y. Ge, and S.M. Belcher Early postnatal ethanol exposure selectively decreases BDNF and truncated TrkB-T2 receptor mRNA expression in the rat cerebellum. Brain research Mol. Brain Res. 93 2001 46 55
36. K.E. Light, C.J. Kane, D.R. Pierce, D. Jenkins, Y. Ge, G. Brown, H. Yang, and N. Nyamweya Intragastric intubation: important aspects of the model for administration of ethanol to rat pups during the postnatal period Alcohol. Clin. Exp. Res. 22 1998 1600 1606
37. D. Lindholm, S. Hamner, and U. Zirrgiebel Neurotrophins and cerebellar development Perspect. Dev. Neurobiol. 5 1997 83 94
38. J. Luo, J.R. West, and N.J. Pantazis Nerve growth factor and basic fibroblast growth factor protect rat cerebellar granule cells in culture against ethanol-induced cell death Alcohol. Clin. Exp. Res. 21 1997 1108 1120
39. J.C. Marcus Neurological findings in the fetal alcohol syndrome Neuropediatrics 18 1987 158 160
40. B.L. Marcussen, C.R. Goodlett, J.C. Mahoney, and J.R. West Developing rat Purkinje cells are more vulnerable to alcohol-induced depletion during differentiation than during neurogenesis Alcohol 11 1994 147 156
41. M.P. Mattson, M.A. Lovell, K. Furukawa, and W.R. Markesbery Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons J. Neurochem. 65 1995 1740 1751
42. R.E. McAlhany Jr., J.R. West, and R.C. Miranda Glial-derived neurotrophic factor rescues calbindin-D28k-immunoreactive neurons in alcohol-treated cerebellar explant cultures J. Neurobiol. 33 1997 835 847
43. R.E. McAlhany Jr., J.R. West, and R.C. Miranda Glial-derived neurotrophic factor (GDNF) prevents ethanol-induced apoptosis and JUN kinase phosphorylation. Brain research Dev. Brain Res. 119 2000 209 216
44. L.D. McCullough, and P.D. Hurn Estrogen and ischemic neuroprotection: an integrated view Trends Endocrinol. Metab. 14 2003 228 235
45. T.N. McGoey, J.N. Reynolds, and J.F. Brien Chronic prenatal ethanol exposure-induced decrease of guinea pig hippocampal CA1 pyramidal cell and cerebellar Purkinje cell density Can. J. Physiol. Pharmacol. 81 2003 476 484
46. R.C. Miranda, F. Sohrabji, and D. Toran-Allerand Interactions of estrogen with the neurotrophins and their receptors during neural development Horm. Behav. 28 1994 367 375
47. K. Nguon, M.G. Baxter, and E.M. Sajdel-Sulkowska Perinatal exposure to polychlorinated biphenyls differentially affects cerebellar development and motor functions in male and female rat neonates Cerebellum 4 2005 112 122
48. A.L. Norman, N. Crocker, S.N. Mattson, and E.P. Riley Neuroimaging and fetal alcohol spectrum disorders Dev. disabil. Res. Rev. 15 2009 209 217
49. H. Ogura, T. Mikami, N. Takamura, Y. Suzuki, and T. Chiba [Development of behavioral function of cerebellar hypoplasia rats as induced by cytosine arabinoside (ara-C) (author's transl)]. Nihon yakurigaku zasshi Folia Pharmacol. Japonica 76 1980 33 44
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
51. F. Rahimi Shourmasti, G.I. Lashkarbolouki, T. Abrari, K. Elahdadi Salmani, and M. Goudarzi A Effects of riluzole on harmaline induced tremor and ataxia in rats: biochemical, histological and behavioral studies Eur. J. Pharmacol. 695 2012 40 47
52. A. Ramezani, I. Goudarzi, T. Lashkarbolouki, M.T. Ghorbanian, M.E. Salmani, and K. Abrari Neuroprotective effects of the 17beta-estradiol against ethanol-induced neurotoxicity and oxidative stress in the developing male rat cerebellum: biochemical, histological and behavioral changes Pharmacol. Biochem. Behav. 100 2011 144 151
53. P. Rong, A.M. Bennie, W.R. Epa, and G.L. Barrett Nerve growth factor determines survival and death of PC12 cells by regulation of the bcl-x, bax, and caspase-3 genes J. Neurochem. 72 1999 2294 2300
54. D. Sampath, G.R. Jackson, K. Werrbach-Perez, and J.R. Perez-Polo Effects of nerve growth factor on glutathione peroxidase and catalase in PC12 cells J. Neurochem. 62 1994 2476 2479
55. K. Sasahara, H. Shikimi, S. Haraguchi, H. Sakamoto, S. Honda, N. Harada, and K. Tsutsui Mode of action and functional significance of estrogen-inducing dendritic growth, spinogenesis, and synaptogenesis in the developing Purkinje cell J. Neurosci.: Off. J. Soc. Neurosci. 27 2007 7408 7417
56. J.B. Schulz, D. Bremen, J.C. Reed, J. Lommatzsch, S. Takayama, U. Wullner, P.A. Loschmann, T. Klockgether, and M. Weller Cooperative interception of neuronal apoptosis by BCL-2 and BAG-1 expression: prevention of caspase activation and reduced production of reactive oxygen species J. Neurochem. 69 1997 2075 2086
57. M. Singh, E.M. Meyer, and J.W. Simpkins The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats Endocrinology 136 1995 2320 2324
58. F. Sohrabji, L.A. Greene, R.C. Miranda, and C.D. Toran-Allerand Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells J. Neurobiol. 25 1994 974 988
59. F. Sohrabji, R.C. Miranda, and C.D. Toran-Allerand Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons J. Neurosci.: Off. J. Soc. Neurosci. 14 1994 459 471
60. D.T. Solum, and R.J. Handa Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus J. Neurosci.: Off. J. Soc. Neurosci. 22 2002 2650 2659
61. C.D. Toran-Allerand Mechanisms of estrogen action during neural development: mediation by interactions with the neurotrophins and their receptors? J. Steroid. Biochem. Mol. Biol. 56 1996 169 178
62. C.D. Toran-Allerand, R.C. Miranda, W.D. Bentham, F. Sohrabji, T.J. Brown, R.B. Hochberg, and N.J. MacLusky Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain Proc. Natl. Acad. Sci. U. S. A. 89 1992 4668 4672
63. C.D. Toran-Allerand, R.C. Miranda, R.B. Hochberg, and N.J. MacLusky Cellular variations in estrogen receptor mRNA translation in the developing brain: evidence from combined [125I]estrogen autoradiography and non-isotopic in situ hybridization histochemistry Brain Res. 576 1992 25 41
64. C.D. Toran-Allerand, M. Singh, and G. Setalo Jr. Novel mechanisms of estrogen action in the brain: new players in an old story Front. Neuroendocrinol. 20 1999 97 121
65. J.R. West, W.J. Chen, and N.J. Pantazis Fetal alcohol syndrome: the vulnerability of the developing brain and possible mechanisms of damage Metab. Brain Dis. 9 1994 291 322