Protein phosphatase 1, protein phosphatase 2A, and calcineurin play a role in estrogen-mediated neuroprotection

Endocrinology

Volumn 149, Issue 10, 2008, Pages 5235-5243

  Kun, Don Yi ^a   Simpkins, James W ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

7 OXABICYCLO[2.2.1]HEPTANE 2,3 DICARBOXYLIC ACID DISODIUM; CALCINEURIN; CYCLOSPORIN A; ESTRADIOL; ESTROGEN; GLUTAMIC ACID; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PHOSPHOSERINE; PHOSPHOTHREONINE; SERINE; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG INHIBITION; ENZYME ACTIVITY; EXCITOTOXICITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STROKE;

ANIMALS; BRAIN NEOPLASMS; CALCINEURIN; CELL LINE, TUMOR; CELL SURVIVAL; CYCLOSPORINE; DICARBOXYLIC ACIDS; DRUG INTERACTIONS; ENZYME INHIBITORS; ESTROGENS; GLIOMA; GLUTAMIC ACID; MICE; NEURONS; NEUROPROTECTIVE AGENTS; NEUROTOXINS; OKADAIC ACID; OXIDATIVE STRESS; PROTEIN PHOSPHATASE 1; PROTEIN PHOSPHATASE 2; RATS; STROKE;

EID: 53249130976     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0610     Document Type: Article

References (67)

1. Butterfield DA 2006 Oxidative stress in neurodegenerative disorders. Antioxid Redox Signal 8:1971-1973
2. Van Den Bosch L, Van Damme P, Bogaert E, Robberecht W 2006 The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim Biophys Acta 1762:1068-1082
3. Jenner P, Olanow CW 2006 The pathogenesis of cell death in Parkinson's disease. Neurology 66:S24-S36
4. Liu Q, Xie F, Rolston R, Moreira PI, Nunomura A, Zhu X, Smith MA, Perry G 2007 Prevention and treatment of Alzheimer disease and aging: antioxidants. Mini Rev Med Chem 7:171-180
5. Perry G, Cash AD, Smith MA 2002 Alzheimer disease and oxidative stress. J Biomed Biotechnol 2:120-123
6. McNaught KS, Olanow CW, Halliwell B, Isacson O, Jenner P 2001 Failure of the ubiquitin-proteasome system in Parkinson's disease. Nat Rev Neurosci 2:589-594
7. Keller JN, Hanni KB, Markesbery WR 2000 Impaired proteasome function in Alzheimer's disease. J Neurochem 75:436-439
8. Choi J, Levey AI, Weintraub ST, Rees HD, Gearing M, Chin LS, Li L 2004 Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J Biol Chem 279:13256-13264
9. Reddy PH, Beal MF 2005 Are mitochondria critical in the pathogenesis of Alzheimer's disease? Brain Res Brain Res Rev 49:618-632
10. Zeevalk GD, Bernard LP, Song C, Gluck M, Ehrhart J 2005 Mitochondrial inhibition and oxidative stress: reciprocating players in neurodegeneration. Antioxid Redox Signal 7:1117-1139
11. Ferrer I, Barrachina M, Tolnay M, Rey MJ, Vidal N, Carmona M, Blanco R, Puig B 2003 Phosphorylated protein kinases associated with neuronal and glial tau deposits in argyrophilic grain disease. Brain Pathol 13:62-78
12. Alessandrini A, Namura S, Moskowitz MA, Bonventre JV 1999 MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc Natl Acad Sci USA 96:12866-12869
13. Zhu JH, Kulich SM, Oury TD, Chu CT 2002 Cytoplasmic aggregates of phosphorylated extracellular signal-regulated protein kinases in Lewy body diseases. Am J Pathol 161:2087-2098
14. Lian Q, Ladner CJ, Magnuson D, Lee JM 2001 Selective changes of calcineurin (protein phosphatase 2B) activity in Alzheimer's disease cerebral cortex. Exp Neurol 167:158-165
15. Vogelsberg-Ragaglia V, Schuck T, Trojanowski JQ, Lee VM 2001 PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus. Exp Neurol 168:402-412
16. Zhu X, Lee HG, Raina AK, Perry G, Smith MA2002 The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals 11:270-281
17. Slevin M, Krupinski J, Slowik A, Rubio F, Szczudlik A, Gaffney J 2000 Activation of MAP kinase (ERK-1/ERK-2), tyrosine kinase and VEGF in the human brain following acute ischaemic stroke. Neuroreport 11:2759-2764
18. Gong CX, Singh TJ, Grundke-Iqbal I, Iqbal K 1993 Phosphoprotein phosphatase activities in Alzheimer disease brain. J Neurochem 61:921-927
19. Ohkura T, Isse K, Akazawa K, Hamamoto M, Yaoi Y, Hagino N 1994 Evaluation of estrogen treatment in female patients with dementia of the Alzheimer type. Endocr J 41:361-371
20. Paganini-Hill A, Ross RK, Henderson BE 1988 Postmenopausal oestrogen treatment and stroke: a prospective study. BMJ 297:519-522
21. Paganini-Hill A, Henderson VW 1994 Estrogen deficiency and risk of Alzheimer's disease in women. Am J Epidemiol 140:256-261
22. Tang MX, Jacobs D, Stern Y, Marder K, Schofield P, Gurland B, Andrews H, Mayeux R 1996 Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 348:429-432
23. Henderson VW, Buckwalter JG 1994 Cognitive deficits of men and women with Alzheimer's disease. Neurology 44:90-96
24. Green PS, Gridley KE, Simpkins JW 1996 Estradiol protects against β-amyloid (25-35)-induced toxicity in SK-N-SH human neuroblastoma cells. Neurosci Lett 218:165-168
25. Green PS, Gordon K, Simpkins JW 1997 Phenolic A ring requirement for the neuroprotective effects of steroids. J Steroid Biochem Mol Biol 63:229-235
26. Green PS, Bishop J, Simpkins JW 1997 17α-Estradiol exerts neuroprotective effects on SK-N-SH cells. J Neurosci 17:511-515
27. Green PS, Gridley KE, Simpkins JW 1998 Nuclear estrogen receptor-independent neuroprotection by estratrienes: a novel interaction with glutathione. Neuroscience 84:7-10
28. Gridley KE, Green PS, Simpkins JW 1997 Low concentrations of estradiol reduce β-amyloid (25-35)-induced toxicity, lipid peroxidation and glucose utilization in human SK-N-SH neuroblastoma cells. Brain Res 778:158-165
29. Behl C, Widmann M, Trapp T, Holsboer F 1995 17β-Estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun 216:473-482
30. Lee SJ, McEwen BS 2001 Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications. Annu Rev Pharmacol Toxicol 41:569-591
31. Alkayed NJ, Harukuni I, Kimes AS, London ED, Traystman RJ, Hurn PD 1998 Gender-linked brain injury in experimental stroke. Stroke 29:159-165; discussion 166
32. Dubal DB, Kashon ML, Pettigrew LC, Ren JM, Finklestein SP, Rau SW, Wise PM 1998 Estradiol protects against ischemic injury. J Cereb Blood Flow Metab 18:1253-1258
33. Yang SH, Shi J, Day AL, Simpkins JW 2000 Estradiol exerts neuroprotective effects when administered after ischemic insult. Stroke 31:745-749; discussion 749-750
34. Sudo S, Wen TC, Desaki J, Matsuda S, Tanaka J, Arai T, Maeda N, Sakanaka M 1997β-Estradiol protects hippocampal CA1 neurons against transient forebrain ischemia in gerbil. Neurosci Res 29:345-354
35. Fukuda K, Yao H, Ibayashi S, Nakahara T, Uchimura H, Fujishima M, Hall ED 2000 Ovariectomy exacerbates and estrogen replacement attenuates photothrombotic focal ischemic brain injury in rats. Stroke 31:155-160
36. Mendelowitsch A, Ritz MF, Ros J, Langemann H, Gratzl O 2001 17β-Estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate: a new neuroprotective pathway. Brain Res 901:230-236
37. Yang SH, He Z, Wu SS, He YJ, Cutright J, Millard WJ, Day AL, Simpkins JW 2001 17β-Estradiol can reduce secondary ischemic damage and mortality of subarachnoid hemorrhage. J Cereb Blood Flow Metab 21:174-181
38. Yi KD, Chung J, Pang P, Simpkins JW 2005 Role of protein phosphatases in estrogen-mediated neuroprotection. J Neurosci 25:7191-7198
39. Sidhu JS, Omiecinski CJ 1997 An okadaic acid-sensitive pathway involved in the phenobarbital-mediated induction of CYP2B gene expression in primary rat hepatocyte cultures. J Pharmacol Exp Ther 282:1122-1129
40. Tian Y, Ke S, Thomas T, Meeker RJ, Gallo MA 1998 Transcriptional suppression of estrogen receptor gene expression by 2,3,7,8-tetrachlorodibenzo- p-dioxin (TCDD). J Steroid Biochem Mol Biol 67:17-24
41. Takahashi N, Kawanishi-Tabata R, Haba A, Tabata M, Haruta Y, Tsai H, Seon BK 2001 Association of serum endoglin with metastasis in patients with colorectal, breast, and other solid tumors, and suppressive effect of chemotherapy on the serum endoglin. Clin Cancer Res 7:524-532
42. Green PS, Yang SH, Nilsson KR, Kumar AS, Covey DF, Simpkins JW 2001 The nonfeminizing enantiomer of 17β-estradiol exerts protective effects in neuronal cultures and a rat model of cerebral ischemia. Endocrinology 142:400-406
43. Perez E, Liu R, Yang SH, Cai ZY, Covey DF, Simpkins JW 2005 Neuroprotective effects of an estratriene analog are estrogen receptor independent in vitro and in vivo. Brain Res 1038:216-222
44. Yi KD, Cai ZY, Covey DF, Simpkins JW 2008 Estrogen receptor-independent neuroprotection via protein phosphatase preservation and attenuation of persistent extracellular signal-regulated kinase 1/2 activation. J Pharmacol Exp Ther 324:1188-1195
45. Espeland MA, Rapp SR, Shumaker SA, Brunner R, Manson JE, Sherwin BB, Hsia J, Margolis KL, Hogan PE, Wallace R, Dailey M, Freeman R, Hays J 2004 Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291:2959-2968
46. Rapp SR, Espeland MA, Shumaker SA, Henderson VW, Brunner RL, Manson JE, Gass ML, Stefanick ML, Lane DS, Hays J, Johnson KC, Coker LH, Dailey M, Bowen D 2003 Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289:2663-2672
47. Shumaker SA, Legault C, Rapp SR, Thal L, Wallace RB, Ockene JK, Hendrix SL, Jones 3rd BN, Assaf AR, Jackson RD, Kotchen JM, Wassertheil-Smoller S, Wactawski-Wende J 2003 Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289:2651-2662
48. Shumaker SA, Legault C, Kuller L, Rapp SR, Thal L, Lane DS, Fillit H, Stefanick ML, Hendrix SL, Lewis CE, Masaki K, Coker LH 2004 Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291:2947-2958
49. Asthana S, Craft S, Baker LD, Raskind MA, Birnbaum RS, Lofgreen CP, Veith RC, Plymate SR 1999 Cognitive and neuroendocrine response to transdermal estrogen in postmenopausal women with Alzheimer's disease: results of a placebo-controlled, double-blind, pilot study. Psychoneuroendocrinology 24:657-677
50. Fillit H, Weinreb H, Cholst I, Luine V, McEwen B, Amador R, Zabriskie J 1986 Observations in a preliminary open trial of estradiol therapy for senile dementia-Alzheimer's type. Psychoneuroendocrinology 11:337-345
51. Ditkoff EC, Crary WG, Cristo M, Lobo RA 1991 Estrogen improves psychological function in asymptomatic postmenopausal women. Obstet Gynecol 78:991-995
52. Rauramo L, Lagerspetz K, Engblom P, Punnonen R 1975 The effect of castration and peroral estrogen therapy on some psychological functions. Front Horm Res 3:94-104
53. Kawas C, Resnick S, Morrison A, Brookmeyer R, Corrada M, Zonderman A, Bacal C, Lingle DD, Metter E 1997 A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore Longitudinal Study of Aging. Neurology 48:1517-1521
54. Liu R, Yang SH, Perez E, Yi KD, Wu SS, Eberst K, Prokai L, Prokai-Tatrai K, Cai ZY, Covey DF, Day AL, Simpkins JW 2002 Neuroprotective effects of a novel non-receptor-binding estrogen analogue: in vitro and in vivo analysis. Stroke 33:2485-2491
55. Simpkins JW, Rajakumar G, Zhang YQ, Simpkins CE, Greenwald D, Yu CJ, Bodor N, Day AL 1997 Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J Neurosurg 87:724-730
56. Park IK, DePaoli-Roach AA 1994 Domains of phosphatase inhibitor-2 involved in the control of the ATP-Mg-dependent protein phosphatase. J Biol Chem 269:28919-28928
57. Cohen PT, Berndt N 1991 Reactivation of protein phosphatase 1 expressed at high levels from recombinant baculovirus. Methods Enzymol 201:408-414
58. Li YM, Casida JE 1992 Cantharidin-binding protein: identification as protein phosphatase 2A. Proc Natl Acad Sci USA 89:11867-11870
59. Li YM, Mackintosh C, Casida JE 1993 Protein phosphatase 2A and its [3H]cantharidin/[3H]endothall thioanhydride binding site. Inhibitor specificity of cantharidin and ATP analogues. Biochem Pharmacol 46:1435-1443
60. Thiery JP, Blazsek I, Legras S, Marion S, Reynes M, Anjo A, Adam R, Misset JL 1999 Hepatocellular carcinoma cell lines from diethylnitrosamine phenobarbital-treated rats. Characterization and sensitivity to endothall, a protein serine/threonine phosphatase-2A inhibitor. Hepatology 29:1406-1417
61. Schwaninger M, Blume R, Oetjen E, Knepel W 1993 The immunosuppressive drugs cyclosporin A and FK506 inhibit calcineurin phosphatase activity and gene transcription mediated through the cAMP-responsive element in a nonimmune cell line. Naunyn Schmiedebergs Arch Pharmacol 348:541-545
62. Kung L, Batiuk TD, Palomo-Pinon S, Noujaim J, Helms LM, Halloran PF 2001 Tissue distribution of calcineurin and its sensitivity to inhibition by cyclosporine. Am J Transplant 1:325-333
63. Keen JC, Zhou Q, Park BH, Pettit C, Mack KM, Blair B, Brenner K, Davidson NE 2005 Protein phosphatase 2A regulates estrogen receptor (ER) α expression through modulation of ER mRNA stability. J Biol Chem 280:29519-29524
64. Lu Q, Surks HK, Ebling H, Baur WE, Brown D, Pallas DC, Karas RH 2003 Regulation of estrogen receptor α-mediated transcription by a direct interaction with protein phosphatase 2A. J Biol Chem 278:4639-4645
65. Liu H, Liu K, Bodenner DL 2005 Estrogen receptor inhibits interleukin-6 gene expression by disruption of nuclear factor B transactivation. Cytokine 31:251-257
66. Wen Y, Yang SH, Liu R, Perez EJ, Brun-Zinkernagel AM, Koulen P, Simpkins JW 2006 Cdk5 is involved in NFT-like tauopathy induced by transient cerebral ischemia in female rats. Biochim Biophys Acta 1772:473-483
67. Chen D, Xu X, Cheon YP, Bagchi MK, Bagchi IC 2004 Estrogen induces expression of secretory leukocyte protease inhibitor in rat uterus. Biol Reprod 71:508-514