Alcohol
Volume 31, Issue 1 , Pages 39-48 , August 2003

Role of protein kinase C in estrogen protection against apoptotic cerebellar cell death in ethanol-withdrawn rats

  • Marianna E. Jung

      Affiliations

    • Department of Pharmacology and Neuroscience, University of North Texas HSC at Fort Worth, 3500 Camp Bowie Boulevard, Fort Worth, TX 76107-2699, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1-817-735-0156; fax: +1-817-735-2091.
    • ,
  • David G. Watson

      Affiliations

    • Department of The Air Force, 59th Clinical Research Squadron, Lackland Air Force Base, TX 78236, USA
    • ,
  • Yi Wen

      Affiliations

    • Department of Pharmacology and Neuroscience, University of North Texas HSC at Fort Worth, 3500 Camp Bowie Boulevard, Fort Worth, TX 76107-2699, USA
    • ,
  • James W. Simpkins

      Affiliations

    • Department of Pharmacology and Neuroscience, University of North Texas HSC at Fort Worth, 3500 Camp Bowie Boulevard, Fort Worth, TX 76107-2699, USA

Received 19 February 2003 ,Revised 16 June 2003 ,Accepted 6 July 2003.

References 

  1. Allsop J, Turner B. Cerebellar degeneration associated with chronic alcoholism. J Neurol Sci. 1966;3:238–258
  2. Andrews DL, Williams GS, Mahoney JC, West JR. DNA fragmentation during exposure of rat cerebella to ethanol under hypoxia imposed in vitro. J Neurobiol. 1999;38:82–92
  3. Araki S, Simada Y, Kaji K, Hayashi H. Role of protein kinase C in the inhibition by fibroblast growth factor of apoptosis in serum-depleted endothelial cells. Biochem Biophys Res Commun. 1990;172:1081–1085
  4. Behl C, Widmann M, Trapp T, Holsboer F. 17-β estradiol protects neurons from oxidative stress–induced cell death in vitro. Biochem Biophys Res Commun. 1995;216:473–482
  5. Cartwright MM, Tessmer LL, Smith SM. Ethanol-induced neural crest apoptosis is coincident with their endogenous death, but is mechanistically distinct. Alcohol Clin Exp Res. 1998;22:142–149
  6. Castoldi AF, Barni S, Randine G, Costa LG, Manzo L. Ethanol selectively interferes with the trophic action of NMDA and carbachol on cultured cerebellar granule neurons undergoing apoptosis. Brain Res Dev Brain Res. 1998;111:279–289
  7. Chen C-H, Mochly-Rosen D. Opposing effects of δ and ξ PKC in ethanol-induced cardioprotection. J Mol Cell Cardiol. 2001;33:581–585
  8. Chen N, Ma W-Y, Huang C, Dong Z. Translocation of protein kinase Cε and protein kinase Cδ to membrane is required for ultraviolet B–induced activation of mitogen-activated protein kinases and apoptosis. J Biol Chem. 1999;274:15389–15394
  9. Choi K-C, Kang SK, Tai C-J, Auersperg N, Leung PCK. Estradiol up-regulates antiapoptotic bcl-2 messenger ribonucleic acid and protein in tumorigenic ovarian surface epithelium cells. Endocrinology. 2001;142:2351–2360
  10. Cross TG, Scheel-Toellner D, Henriquez NV, Deacon E, Salmon M, Lord JM. Serine/threonine protein kinases and apoptosis. Exp Cell Res. 2000;256:34–41
  11. Csukai M, Mochly-Rosen D. Pharmacologic modulation of protein kinase C isozymes: the role of RACKs and subcellular localisation. Pharmacol Res. 1999;39:253–259
  12. Dekker LV, Parker PJ. Protein kinase C—a question of specificity. Trends Biochem Sci. 1994;19:73–77
  13. D'Mello SR, Galli C, Ciotti T, Calissano P. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci U S A. 1993;90:10989–10993
  14. Dodd H, Shorey-Kutschke RL. Ethanol lowers heart carnitine in the methionine and choline deficient rat. Alcohol. 1987;4:395–399
  15. Fiers W, Beyaert R, Declercq W, Vandenabeele P. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene. 1999;18:7719–7730
  16. Finco TS, Baldwin AS. Mechanistic aspects of NF-κB regulation: the emerging role of phosphorylation and proteolysis. Immunity. 1995;3:263–272
  17. Freund G. Apoptosis and gene expression: perspectives on alcohol-induced brain damage. Alcohol. 1994;11:385–387
  18. Gatch MB, Lal H. Pharmacological treatment of alcoholism. Prog Neuropsychopharmacol Biol Psychiatry. 1998;22:917–944
  19. Goldman H, Sapirstein LA, Murphy S, Moore J. Alcohol and regional blood flow in brains of rats. Proc Soc Exp Biol Med. 1973;144:983–988
  20. Goldstein DB, Pal N. Alcohol dependence produced in mice by inhalation of ethanol: grading the withdrawal reaction. Science. 1971;172:288–290
  21. Goodnight J, Mischak H, Kolch W, Mushinski JF. Immunocytochemical localization of eight protein kinase C isozymes overexpressed in NIH 3T3 fibroblasts: isoform-specific association with microfilaments, Golgi, endoplasmic reticulum, and nuclear and cell membranes. J Biol Chem. 1995;270:9991–10001
  22. Green PS, Simpkins JW. Neuroprotective effects of estrogens: potential mechanisms of action. Int J Dev Neurosci. 2000;18:347–358
  23. Gursoy E, Cardounel A, Al-khlaiwi T, Al-drees A, Kalimi M. Tamoxifen protects clonal mouse hippocampal (HT-22) cells against neurotoxins-induced cell death. Neurochem Int. 2002;40:405–412
  24. Hodge CW, Mehmert KK, Kelley SP, McMahon T, Haywood A, Olive MF, et al. Supersensitivity to allosteric GABAA receptor modulators and alcohol in mice lacking PKCε. Nat Neurosci. 1999;2:997–1002
  25. Hofmann J. The potential for isoenzyme-selective modulation of protein kinase C. FASEB J. 1997;11:649–669
  26. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, et al. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 2000;287:1056–1060
  27. Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council . Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press; 1996;
  28. Jaffe J, Kranzler H, Ciraulo D. Drugs used in the treatment of alcoholism. In:  Mendelson J,  Mello N editor. Medical Treatment and Diagnosis of Alcoholism. New York: McGraw-Hill; 1992;p. 421–461
  29. Jung ME, Wallis CJ, Gatch MB, Lal H. Sex differences in the pentylenetetrazol-like stimulus induced by ethanol withdrawal. J Pharmacol Exp Ther. 1999;291:576–582
  30. Jung ME, Yang SH, Brun-Zinkernagel A-M, Simpkins JW. Estradiol protects against cerebellar damage and motor deficit in ethanol-withdrawn rats. Alcohol. 2002;26:83–93
  31. Kanter P, Leister KJ, Tomei LD, Wenner PA, Wenner CE. Epidermal growth factor and tumor promoters prevent DNA fragmentation by different mechanisms. Biochem Biophys Res Commun. 1984;118:392–399
  32. Karhunen PJ, Erkinjuntti T, Laippala P. Moderate alcohol consumption and loss of cerebellar Purkinje cells. BMJ. 1994;308:1663–1667
  33. Karin M, Smeal T. Control of transcription factors by signal transduction pathways: the beginning of the end. Trends Biochem Sci. 1992;17:418–422
  34. Knauf JA, Elisei R, Mochly-Rosen D, Liron T, Chen X-N, Gonsky R, et al. Involvement of protein kinase Cε (PKCε) in thyroid cell death: a truncated chimeric PKCε cloned from a thyroid cancer cell line protects thyroid cells from apoptosis. J Biol Chem. 1999;274:23414–23425
  35. Krebs JF, Armstrong RC, Srinivasan A, Aja T, Wong AM, Aboy A, et al. Activation of membrane-associated procaspase-3 is regulated by Bcl-2. J Cell Biol. 1999;144:915–926
  36. Lal H, Harris CM, Benjamin D, Springfield AC, Bhadra S, Emmett-Oglesby MW. Characterization of a pentylenetetrazol-like interoceptive stimulus produced by ethanol withdrawal. J Pharmacol Exp Ther. 1988;247:508–518
  37. Li L, Shou Y, Borowitz JL, Isom GE. Reactive oxygen species mediate pyridostigmine-induced neuronal apoptosis: involvement of muscarinic and NMDA receptors. Toxicol Appl Pharmacol. 2001;177:17–25
  38. Maggi A, Vegeto E, Brusadelli A, Belcredito S, Pollio G, Ciana P. Identification of estrogen target genes in human neural cells. J Steroid Biochem Mol Biol. 2000;74:319–325
  39. Maher P. How protein kinase C activation protects nerve cells from oxidative stress–induced cell death. J Neurosci. 2001;21:2929–2938
  40. McConkey DJ, Hartzell P, Jondal M, Orrenius S. Inhibition of DNA fragmentation in thymocytes and isolated thymocyte nuclei by agents that stimulate protein kinase C. J Biol Chem. 1989;264:13399–13402
  41. Meda C, Vegeto E, Pollio G, Ciana P, Patrone C, Pellicciari C, et al. Oestrogen prevention of neural cell death correlates with decreased expression of mRNA for the pro-apoptotic protein nip-2. J Neuroendocrinol. 2000;12:1051–1059
  42. Miller NS. Pharmacotherapy in alcoholism. J Addict Dis. 1995;14:23–46
  43. Mochly-Rosen D, Gordon AS. Anchoring proteins for protein kinase C: a means for isozyme selectivity. FASEB J. 1998;12:35–42
  44. Mochly-Rosen D, Kauvar LM. Pharmacological regulation of network kinetics by protein kinase C localization. Semin Immunol. 2000;12:55–61
  45. Morley P, Whitfield JF, Vanderhyden BC, Tsang BK, Schwartz J-L. A new, nongenomic estrogen action: the rapid release of intracellular calcium. Endocrinology. 1992;131:1305–1312
  46. Myers RD. New drugs for the treatment of experimental alcoholism. Alcohol. 1994;11:439–451
  47. Newton AC. Protein kinase C: structure, function, and regulation. J Biol Chem. 1995;270:28495–28498
  48. Oberdoerster J, Rabin RA. Enhanced caspase activity during ethanol-induced apoptosis in rat cerebellar granule cells. Eur J Pharmacol. 1999;385:273–282
  49. Olive MF, Mehmert KK, Messing RO, Hodge CW. Reduced operant ethanol self-administration and in vivo mesolimbic dopamine responses to ethanol in PKCε-deficient mice. Eur J Neurosci. 2000;12:4131–4140
  50. Olive MF, Mehmert KK, Nannini MA, Camarini R, Messing RO, Hodge CW. Reduced ethanol withdrawal severity and altered withdrawal-induced c-fos expression in various brain regions of mice lacking protein kinase C-ε. Neuroscience. 2001;103:171–179
  51. Pascale A, Battaini F, Govoni S, Persichella M, De Salvia MA, Cuomo V. Chronic low doses of ethanol affect brain protein kinase C and ultrasonic calls in rats. Alcohol. 1997;14:557–561
  52. Phillips SC, Harper CG, Kril J. A quantitative histological study of the cerebellar vermis in alcoholic patients. Brain. 1987;110(Pt 2):301–314
  53. Pike CJ. Estrogen modulates neuronal Bcl-xL expression and β-amyloid-induced apoptosis: relevance to Alzheimer's disease. J Neurochem. 1999;72:1552–1563
  54. Ren J, Datta R, Shioya H, Li Y, Oki E, Biedermann V, et al. p73β is regulated by protein kinase Cδ catalytic fragment generated in the apoptotic response to DNA damage. J Biol Chem. 2002;277:33758–33765
  55. Román J, Giménez A, Lluis JM, Gassó M, Rubio M, Caballeria J, et al. Enhanced DNA binding and activation of transcription factors NF-κB and AP-1 by acetaldehyde in HEPG2 cells. J Biol Chem. 2000;275:14684–14690
  56. Schmidt R, Fazekas F, Reinhart B, Kapeller P, Fazekas G, Offenbacher H, et al. Estrogen replacement therapy in older women: a neuropsychological and brain MRI study. J Am Geriatr Soc. 1996;44:1307–1313
  57. Shao H, Zhou J, Ewald SJ. Regulation of signal transduction and DNA fragmentation in thymocytes by ethanol. Cell Immunol. 1995;164:11–19
  58. Shinomura T, Asaoka Y, Oka M, Yoshida K, Nishizuka Y. Synergistic action of diacylglycerol and unsaturated fatty acid for protein kinase C activation: its possible implications. Proc Natl Acad Sci U S A. 1991;88:5149–5153
  59. Siebenlist U, Franzoso G, Brown K. Structure, regulation and function of NF-κB. Annu Rev Cell Biol. 1994;10:405–455
  60. Simpkins JW, Green PS, Gridley JS, Monck EK. Neuroprotective effects of estrogens. In:  Bellino FL editors. Biology of Menopause. New York: Springer-Verlag; 2000;p. 103–111
  61. Simpkins JW, Rajakumar G, Zhang YQ, Simpkins CE, Greenwald D, Yu CJ, et al. Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J Neurosurg. 1997;87:724–730
  62. Singhal PC, Reddy K, Ding G, Kapasi A, Franki N, Ranjan R, et al. Ethanol-induced macrophage apoptosis: the role of TGF-β. J Immunol. 1999;162:3031–3036
  63. Slomiany BL, Piotrowski J, Slomiany A. Suppression of caspase-3 and nitric-oxide synthase-2 during buccal mucosal ulcer healing: effect of chronic alcohol ingestion. IUBMB Life. 1999;48:121–125
  64. Sudoh N, Toba K, Akishita M, Ako J, Hashimoto M, Iijima K, et al. Estrogen prevents oxidative stress–induced endothelial cell apoptosis in rats. Circulation. 2001;103:724–729
  65. Tanaka C, Nishizuka Y. The protein kinase C family for neuronal signaling. Annu Rev Neurosci. 1994;17:551–567
  66. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science. 1998;281:1312–1316
  67. Victor M, Adams RD, Collins GH. The Wernicke-Korsakoff syndrome. A clinical and pathological study of 245 patients, 82 with post-mortem examinations. Contemp Neurol Ser. 1971;7:1–206
  68. Walker DW, Barnes DE, Riley JN, Hunter BE, Zornetzer SF. The neurotoxicity of chronic alcohol consumption: an animal model. In:  Sandler M editors. Psychopharmacology of Ethanol. New York: Raven Press; 1980;p. 17
  69. Walker DW, Hunter BE, Abraham WC. Neuroanatomical and functional deficits subsequent to chronic ethanol administration in animals. Alcohol Clin Exp Res. 1981;5:267–282
  70. Wang KK. Calpain and caspase: can you tell the difference?. Trends Neurosci. 2000;23:20–26
  71. Watson DG, Fiola C, Simpkins JW. Inhibition or down-regulation of protein kinase C enhances estrogen-induced neuroprotection in an in vitro model. Abstr Soc Neurosci. 2000;26:773; (Abstract)
  72. Watson DG, Simpkins JW. Estradiol exposure inhibits PKCε activation and ERK1/2 phosphorylation: potential mechanisms for its neuroprotective effects. Abstr Soc Neurosci. 2001;27:572; (Abstract)
  73. Wise PM. Estrogens and neuroprotection. Trends Endocrinol Metab. 2002;13:229–230
  74. Yang S-H, He Z, Wu SS, He Y-J, Cutright J, Millard WJ, et al. 17-β Estradiol can reduce secondary ischemic damage and mortality of subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2001;21:174–181
  75. Yang X, Stennicke HR, Wang B, Green DR, Jänicke RU, Srinivasan A, et al. Granzyme B mimics apical caspases: description of a unified pathway for trans-activation of executioner caspase-3 and -7. J Biol Chem. 1998;273:34278–34283

PII: S0741-8329(03)00186-1

doi: 10.1016/j.alcohol.2003.07.004

Alcohol
Volume 31, Issue 1 , Pages 39-48 , August 2003

Article Tools

* Image Usage & Resolution