Ethanol withdrawal acts as an age-specific stressor to activate cerebellar P38 kinase

Neurobiology of Aging

Volumn 32, Issue 12, 2011, Pages 2266-2278

  Jung, Marianna E ^a   Ju, Xiaohua ^a   Simpkins, James W ^a   Metzger, Daniel B ^a   Yan, Liang Jun ^a   Wen, Yi ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

17 estradiol; Age; Brain aging changes; Cerebellum; Ethanol withdrawal; Female rats; Mitochondrial protein carbonyls; Phosphor P38 (pP38); Purkinje neurons; Reactive oxygen species

Indexed keywords

ALCOHOL; CARBONYL DERIVATIVE; ESTRADIOL; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE;

AGE DISTRIBUTION; AGED; AGING; ALCOHOL WITHDRAWAL; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN REGION; CELL LEVEL; CELL STRESS; CEREBELLUM; CONTROLLED STUDY; DIETARY INTAKE; DRUG MECHANISM; ENZYME ACTIVATION; FEMALE; MALE; MITOCHONDRIAL RESPIRATION; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RAT; TASK PERFORMANCE;

AGING; ANIMALS; CEREBELLUM; ENZYME ACTIVATION; ETHANOL; FEMALE; MALE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 80053636032     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2010.01.005     Document Type: Article

References (52)

1. Arimoto K., Fukuda H., Imajoh-Ohmi S., Saito H., Takekawa M. Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat. Cell. Biol. 2008, 10:1324-1332.
2. Aydin M.V., Sen O., Kayaselcuk F., Bolat F., Tufan K., Caner H., Altinors N. Analysis and prevalence of inflammatory cells in subtypes of lumbar disc herniations under cyclooxygenase-2 inhibitor therapy. Neurol. Res. 2005, 27:609-612.
3. Barca O., Costoya J.A., Senaris R.M., Arce V.M. Interferon-beta protects astrocytes against tumour necrosis factor-induced apoptosis via activation of p38 mitogen-activated protein kinase. Exp. Cell. Res. 2008, 314:2231-2237.
4. Becker E.B., Oliver P.L., Glitsch M.D., Banks G.T., Achilli F., Hardy A., Nolan P.M., Fisher E.M., Davies K.E. A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proc. Natl. Acad. Sci. USA 2009, 106:6706-6711.
5. Campos C.B., Bedard P.A., Linden R. Requirement of p38 stress-activated MAP kinase for cell death in the developing retina depends on the stage of cell differentiation. Neurochem. Int. 2006, 49:494-499.
6. Drechsler Y., Dolganiuc A., Norkina O., Romics L., Li W., Kodys K., Bach F.H., Mandrekar P., Szabo G. Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 MAPK activation in monocytes. J. Immunol. 2006, 177:2592-2600.
7. Du J., Yang S., Wang Z., Zhai C., Yuan W., Lei R., Zhang J., Zhu T. Bone morphogenetic protein 6 inhibit stress-induced breast cancer cells apoptosis via both Smad and p38 pathways. J. Cell. Biochem. 2008, 103:1584-1597.
8. Galluzzi L., Blomgren K., Kroemer G. Mitochondrial membrane permeabilization in neuronal injury. Nat. Rev. Neurosci. 2009, 10:481-494.
9. Giordano G., Klintworth H.M., Kavanagh T.J., Costa L.G. Apoptosis induced by domoic acid in mouse cerebellar granule neurons involves activation of p38 and JNK MAP kinases. Neurochem. Int. 2008, 52:1100-1105.
10. Guarnieri C., Muscari C., Caldarera C.M. Mitochondrial production of oxygen free radicals in the heart muscle during the life span of the rat: peak at middle age. EXS 1992, 62:73-77.
11. Hensley K., Floyd R.A., Zheng N.Y., Nael R., Robinson K.A., Nguyen X., Pye Q.N., Stewart C.A., Geddes J., Markesbery W.R. p38 kinase is activated in the Alzheimer's disease brain. J. Neurochem. 1999, 72:2053-2058.
12. Hsu J.T., Hsieh Y.C., Kan W.H., Chen J.G., Choudhry M.A., Schwacha M.G., Bland K.I., Chaudry I.H. Role of p38 mitogen-activated protein kinase pathway in estrogen-mediated cardioprotection following trauma-hemorrhage. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H2982-2987.
13. Huot J., Houle F., Marceau F., Landry J. Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ. Res. 1997, 80:383-392.
14. Jakubowski W., Bartosz G. 2,7-dichlorofluorescin oxidation and reactive oxygen species: what does it measure?. Cell. Biol. Int. 2000, 24:757-760.
15. Jiang Y., Chen C., Li Z., Guo W., Gegner J.A., Lin S., Han J. Characterization of the structure and function of a new mitogen-activated protein kinase (p38beta). J. Biol. Chem. 1996, 271:17920-17926.
16. Jiang Y., Gram H., Zhao M., New L., Gu J., Feng L., Di Padova F., Ulevitch R.J., Han J. Characterization of the structure and function of the fourth member of p38 group mitogen-activated protein kinases, p38delta. J. Biol. Chem. 1997, 272:30122-30128.
17. Jung M.E., Yan L.J., Forster M.J., Simpkins J.W. Ethanol withdrawal provokes mitochondrial injury in an estrogen preventable manner. J. Bioenerg. Biomembr. 2008, 40:35-44.
18. Jung M.E., Wilson A.M., Ju X., Wen Y., Metzger D.B., Simpkins J.W. Ethanol withdrawal provokes opening of the mitochondrial membrane permeability transition pore in an estrogen-preventable manner. J. Pharmacol. Exp. Ther. 2009, 328:692-698.
19. Jung M.E., Yang S.H., Brun-Zinkernagel A.M., Simpkins J.W. Estradiol protects against cerebellar damage and motor deficit in ethanol-withdrawn rats. Alcohol 2002, 26:83-93.
20. Kelleher I., Garwood C., Hanger D.P., Anderton B.H., Noble W. Kinase activities increase during the development of tauopathy in htau mice. J. Neurochem. 2007, 103:2256-2267.
21. Kovarik P., Stoiber D., Eyers P.A., Menghini R., Neininger A., Gaestel M., Cohen P., Decker T. Stress-induced phosphorylation of STAT1 at Ser727 requires p38 mitogen-activated protein kinase whereas IFN-gamma uses a different signaling pathway. Proc. Natl. Acad. Sci. USA 1999, 96:13956-13961.
22. Ku B.M., Lee Y.K., Jeong J.Y., Mun J., Han J.Y., Roh G.S., Kim H.J., Cho G.J., Choi W.S., Yi G.S., Kang S.S. Ethanol-induced oxidative stress is mediated by p38 MAPK pathway in mouse hippocampal cells. Neurosci. Lett. 2007, 419:64-67.
23. Lechner C., Zahalka M.A., Giot J.F., Moller N.P., Ullrich A. ERK6, a mitogen-activated protein kinase involved in C2C12 myoblast differentiation. Proc. Natl. Acad. Sci. USA 1996, 93:4355-4359.
24. Lee J.C., Laydon J.T., McDonnell P.C., Gallagher T.F., Kumar S., Green D., McNulty D., Blumenthal M.J., Heys J.R., Landvatter S.W. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 1994, 372:739-746.
25. Lee S.H., Park J., Che Y., Han P.L., Lee J.K. Constitutive activity and differential localization of p38alpha and p38beta MAPKs in adult mouse brain. J. Neurosci. Res. 2000, 60:623-631.
26. Levin S.I., Khaliq Z.M., Aman T.K., Grieco T.M., Kearney J.A., Raman I.M., Meisler M.H. Impaired motor function in mice with cell-specific knockout of sodium channel Scn8a (NaV1.6) in cerebellar purkinje neurons and granule cells. J. Neurophysiol. 2006, 96:785-793.
27. Li H.L., Wu S., Rottenberg H. Alcohol inhibits the depolarization-induced stimulation of oxidative phosphorylation in synaptosomes. J. Neurochem. 1996, 66:1691-1697.
28. Markowska A.L. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J. Neurosci. 1999, 19:8122-8133.
29. Mausset A.L., de Seze R., Montpeyroux F., Privat A. Effects of radiofrequency exposure on the GABAergic system in the rat cerebellum: clues from semi-quantitative immunohistochemistry. Brain Res. 2001, 912:33-46.
30. 2. J. Biol. Chem. 1996, 271:26981-26988.
31. Nonaka Y., Miyajima M., Ogino I., Nakajima M., Arai H. Analysis of neuronal cell death in the cerebral cortex of H-Tx rats with compensated hydrocephalus. J. Neurosurg. Pediatr. 2008, 1:68-74.
32. Norkina O., Dolganiuc A., Shapiro T., Kodys K., Mandrekar P., Szabo G. Acute alcohol activates STAT3, AP-1, and Sp-1 transcription factors via the family of Src kinases to promote IL-10 production in human monocytes. J. Leukoc. Biol. 2007, 82:752-762.
33. Peart J.N., Gross E.R., Headrick J.P., Gross G.J. Impaired p38 MAPK/HSP27 signaling underlies aging-related failure in opioid-mediated cardioprotection. J. Mol. Cell. Cardiol. 2007, 42:972-980.
34. Ramadoss J., Lunde E.R., Chen W.J., West J.R., Cudd T.A. Temporal vulnerability of fetal cerebellar Purkinje cells to chronic binge alcohol exposure: ovine model. Alcohol Clin. Exp. Res. 2007, 31:1738-1745.
35. Rewal M., Jung M.E., Simpkins J.W. Role of the GABA-A system in estrogen-induced protection against brain lipid peroxidation in ethanol-withdrawn rats. Alcohol Clin. Exp. Res. 2004, 28:1907-1915.
36. Rewal M., Jung M.E., Wen Y., Brun-Zinkernagel A.M., Simpkins J.W. Role of the GABAA system in behavioral, motoric, and cerebellar protection by estrogen during ethanol withdrawal. Alcohol 2003, 31:49-61.
37. Santucci A.C., Cortes C., Bettica A., Cortes F. Chronic ethanol consumption in rats produces residual increases in anxiety 4 months after withdrawal. Behav. Brain Res. 2008, 188:24-31.
38. Smolen A., Marks M.J., Smolen T.N., Collins A.C. Dose and route of administration alter the relative elimination of ethanol by long-sleep and short-sleep mice. Alcohol. Clin. Exp. Res. 1986, 10:198-204.
39. Stein B., Yang M.X., Young D.B., Janknecht R., Hunter T., Murray B.W., Barbosa M.S. p38-2, a novel mitogen-activated protein kinase with distinct properties. J. Biol. Chem. 1997, 272:19509-19517.
40. Svensson C.I., Marsala M., Westerlund A., Calcutt N.A., Campana W.M., Freshwater J.D., Catalano R., Feng Y., Protter A.A., Scott B., Yaksh T.L. Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J. Neurochem. 2003, 86:1534-1544.
41. Tan S., Wood M., Maher P. Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J. Neurochem. 1998, 71:95-105.
42. Valles S.L., Borras C., Gambini J., Furriol J., Ortega A., Sastre J., Pallardo F.V., Vina J. Oestradiol or genistein rescues neurons from amyloid beta-induced cell death by inhibiting activation of p38. Aging Cell. 2008, 7:112-118.
43. van Eickels M., Grohe C., Cleutjens J.P., Janssen B.J., Wellens H.J., Doevendans P.A. 17beta-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 2001, 104:1419-1423.
44. Vereker E., O'Donnell E., Lynch M.A. The inhibitory effect of interleukin-1beta on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J. Neurosci. 2000, 20:6811-6819.
45. Wang M., Tsai B.M., Reiger K.M., Brown J.W., Meldrum D.R. 17-beta-Estradiol decreases p38 MAPK-mediated myocardial inflammation and dysfunction following acute ischemia. J. Mol. Cell. Cardiol. 2006, 40:205-212.
46. Watanabe M. Molecular mechanisms governing competitive synaptic wiring in cerebellar Purkinje cells. Tohoku J. Exp. Med. 2008, 214:175-190.
47. Williamson D., Gallagher P., Harber M., Hollon C., Trappe S. Mitogen-activated protein kinase (MAPK) pathway activation: effects of age and acute exercise on human skeletal muscle. J. Physiol. 2003, 547:977-987.
48. Wu M., Han M., Li J., Xu X., Li T., Que L., Ha T., Li C., Chen Q., Li Y. 17beta-estradiol inhibits angiotensin II-induced cardiac myofibroblast differentiation. Eur. J. Pharmacol. 2009, 616:155-159.
49. Xiong W., Kojic L.Z., Zhang L., Prasad S.S., Douglas R., Wang Y., Cynader M.S. Anisomycin activates p38 MAP kinase to induce LTD in mouse primary visual cortex. Brain Res. 2006, 1085:68-76.
50. Yan L.J., Levine R.L., Sohal R.S. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. USA 1997, 94:11168-11172.
51. Yang S.H., He Z., Wu S.S., He Y.J., Cutright J., Millard W.J., Day A.L., Simpkins J.W. 17-beta estradiol can reduce secondary ischemic damage and mortality of subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 2001, 21:174-181.
52. Zaulyanov L.L., Green P.S., Simpkins J.W. Glutamate receptor requirement for neuronal death from anoxia-reoxygenation: an in Vitro model for assessment of the neuroprotective effects of estrogens. Cell Mol. Neurobiol. 1999, 19:705-718.