Estradiol Attenuates Programmed Cell Death after Stroke-Like Injury

Journal of Neuroscience

Volumn 23, Issue 36, 2003, Pages 11420-11426

  Rau, Shane W ^a   Dubal, Dena B ^c   Böttner, Martina ^b   Gerhold, Lynnette M ^b   Wise, Phyllis M ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Caspase; Estrogen (estradiol); Ischemia; Middle cerebral artery occlusion; Stroke; TUNEL

Indexed keywords

CALPAIN; CASPASE; DNA FRAGMENT; ESTRADIOL; SPECTRIN; SPECTRIN BREAKDOWN PRODUCT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN ISCHEMIA; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; STROKE;

EID: 0348109349     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-36-11420.2003     Document Type: Article

References (78)

1. Alkayed NJ, Harukuni I, Kimes AS, London ED, Traystman RJ, Hurn PD (1998) Gender-linked brain injury in experimental stroke. Stroke 29:159-166.
2. Alkayed NJ, Murphy SJ, Traystman RJ, Hurn PD (2000) Neuroprotective effects of female gonadal steroids in reproductively senescent female rats. Stroke 31:161-168.
3. Asahi M, Hoshimaru M, Uemura Y, Tokime T, Kojima M, Ohtsuka T, Matsuura N, Aoki T, Shibahara K, Kikuchi H (1997) Expression of interleukin-1β converting enzyme gene family and bcl-2 gene family in the rat brain following permanent occlusion of the middle cerebral artery. J Cereb Blood Flow Metab 17:11-18.
4. 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.
5. Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski HM (1986) Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17:1304-1308.
6. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, Holsboer F (1997) Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535-541.
7. Brinton RD (2001) Cellular and molecular mechanisms of estrogen regulation of memory function and neuroprotection against Alzheimer's disease: recent insights and remaining challenges. Learn Mem 8:121-133.
8. Calakos N, Scheller RH (1994) Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J Biol Chem 269:24534-24537.
9. Choi DW (1996) Ischemia-induced neuronal apoptosis. Curr Opin Neurobiol 6:667-672.
10. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647-656.
11. Crowder RJ, Freeman RS (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J Neurosci 18:2933-2943.
12. Culmsee C, Vedder H, Ravati A, Junker V, Otto D, Ahlemeyer B, Krieg J-C, Krieglstein J (1999) Neuroprotection by estrogens in a mouse model of focal cerebral ischemia and in cultured neurons: evidence for a receptor-independent antioxidative mechanism. J Cereb Blood Flow Metab 19:1263-1269.
13. Davoli MA, Fourtounis J, Tam J, Xanthoudakis S, Nicholson D, Robertson GS, Xu D (2002) Immunohistochemical and biochemical assessment of caspase-3 activation and DNA fragmentation following transient focal ischemia in the rat. J Neurosci 115:125-136.
14. Dubal DB, Wise PM (2001) Neuroprotective effects of estradiol in middle-aged female rats. Endocrinology 142:43-48.
15. 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.
16. Dubal DB, Shughrue PJ, Wilson ME, Merchenthaler I, Wise PM (1999) Estradiol modulates Bcl-2 in cerebral ischemia: a potential role for estrogen receptors. J Neurosci 19:6385-6393.
17. Endres M, Namura S, Shimizu-Sasamata M, Waeber C, Zhang L, Gomez-Isla T, Hyman BT, Moskowitz MA (1998) Attenuation of delayed neuronal death after mild focal ischemia in mice by inhibition of the caspase family. J Cereb Blood Flow Metab 18:238-247.
18. Fillit H (1994) Estrogens in the pathogenesis and treatment of Alzheimer's disease in postmenopausal women. Ann NY Acad Sci 743:233-239.
19. Friedlander RM, Gagliardini V, Hara H, Fink KB, Li W, MacDonald G, Fishman MC, Greenberg AH, Moskowitz MA, Yuan J (1997) Expression of a dominant negative mutant of interleukin-1 beta converting enzyme in transgenic mice prevents neuronal cell death induced by tropic factor withdrawal and ischemic brain injury. J Exp Med 185:933-940.
20. Garcia-Segura LM, Azcoitia I, DonCarlos LL (2001) Neuroprotection by estradiol. Prog Neurobiol 63:29-60.
21. Green PS, Simpkins JW (2000) Neuroprotective effects of estrogens: potential mechanisms of action. Int J Dev Neurosci 18:347-358.
22. Guegan C, Sola B (2000) Early and sequential recruitment of apoptotic effectors after focal permanent ischemia in mice. Brain Res 856:93-100.
23. Hall ED, Pazara KE, Linseman KL (1991) Sex differences in postischemic neuronal necrosis in gerbils. J Cereb Blood Flow Metab 11:292-298.
24. Henderson VW, Paganini-Hill A (1997) Estrogen and Alzheimer's disease. J Obstet Gynaecol Can 19:21-28.
25. Henderson VW, Watt L, Buckwalter JG (1996) Cognitive skills associated with estrogen replacement in women with Alzheimer's disease. Psychoneuroendocrinology 21:421-430.
26. Hurn PD, Macrae IM (2000) Estrogen as a neuroprotectant in stroke. J Cereb Blood Flow Metab 20:631-652.
27. Jover T, Tanaka H, Calderone A, Oguro K, Bennett MVL, Etgen AM, Zukin RS (2002) Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. J Neurosci 22:2115-2124.
28. Kawas C, Resnick S, Morrison A, Brookmeyer R, Corrada M, Zonderman A, Bacal C, Lingle D, 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.
29. Kim H, Bang OY, Jung MW, Ha SD, Hong HS, Huh K, Kim SU, Mook-Jung I (2001) Neuroprotective effects of estrogen against beta-amyloid toxicity are mediated by estrogen receptors in cultured neuronal cells. Neurosci Lett 302:58-62.
30. Kitagawa H, Hayashi T, Mitsumoto Y, Koga N, Itoyama Y, Abe K (1998a) Reduction of ischemic brain injury by topical application of glial cell line-derived neurotrophic factor after permanent middle cerebral artery occlusion in rats. Stroke 29:1417-1422.
31. Kitagawa K, Matsumoto M, Tsujimoto Y, Ohtsuki T, Kuwabara K, Matsushita K, Yang G, Tanabe H, Martinou J-C, Hori M, Yanagihara T (1998b) Amelioration of hippocampal neuronal damage after global ischemia by neuronal overexpression of BCL-2 in transgenic mice. Stroke 29:2616-2621.
32. Komesaroff PA, Esler MD, Sudhir K (1999) Estrogen supplementation attenuates glucocorticoid and catecholamine responses to mental stress in perimenopausal women. J Clin Endocrinol Metab 84:606-610.
33. Krajewski S, Mai JK, Krajewska M, Sikorska M, Mossakowski MJ, Reed JC (1995) Upregulation of bax protein levels in neurons following cerebral ischemia. J Neurosci 15:6364-6375.
34. Li Y, Chopp M, Jiang N, Yao F, Zaloga C (1995) Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 15:389-397.
35. Li Y, Chopp M, Powers C, Jiang N (1997) Apoptosis and protein expression after focal cerebral ischemia in the rat. Brain Res 765:301-312.
36. Linford NJ, Dorsa DM (2002) 17beta-estradiol and the phytoestrogen genistein attenuate neuronal apoptosis induced by the endoplasmic reticulum calcium-ATPase inhibitor thapsigargin. Steroids 67:1029-1040.
37. Liu Z, Gastard M, Verina T, Bora S, Mouton PR, Koliatsos VE (2001) Estrogens modulate experimentally induced apoptosis of granule cells in the adult hippocampus. J Comp Neurol 441:1-8.
38. Luo Y, Cao G, Pei W, O'Horo C, Graham SH, Chen J (2002) Induction of caspase-activated deoxyribonuclease activity after focal cerebral ischemia and reperfusion. J Cereb Blood Flow Metab 22:15-22.
39. Marder K, Sano M (2000) Estrogen to treat Alzheimer's disease: too little, too late? So what's a woman to do? Neurology 54:2035-2037.
40. Martinou JC, Dubois-Dauphin M, Staple JK, Rodriguez I, Frankowski H, Missotten M, Albertini P, Talabot D, Catsicas S, Pietra C, Huarte J (1994) Overexpression of bcl-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017-1030.
41. McCollum AT, Nasr P, Estus S (2002) Calpain activates caspase-3 during UV-induced neuronal death but only calpain is necessary for death. J Neurochem 82:1208-1220.
42. Mendelowitsch A, Ritz MF, Ros J, Langemann H, Gratzl O (2001) 17beta-estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate: a new neuroprotective pathway. Brain Res 901:230-236.
43. Miller DB, Ali SF, O'Callaghan JP, Laws SC (1998) The impact of gender and estrogen on striatal dopaminergic neurotoxicity. Ann NY Acad Sci 844:153-165.
44. Monroe DG, Berger RR, Sanders MM (2002) Tissue-protective effects of estrogen involve regulation of caspase gene expression. Mol Endocrinol 16:1322-1331.
45. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli KJ, Yuan J, Moskowitz MA (1998) Activation and cleavage of caspase-3 in apoptosis induced by cerebral ischemia. J Neurosci 18:3659-3668.
46. Nath R, Scott M, Nadimpalli R, Gupta R, Wang KK (2000) Activation of apoptosis-linked caspase(s) in NMDA-injured brains of neonatal rats. Neurochem Int 36:119-126.
47. Paganini-Hill A (1995) Estrogen replacement therapy and stroke. Prog Cardiovasc Dis 38:223-242.
48. Paganini-Hill A, Henderson VW (1994) Estrogen deficiency and risk of Alzheimer's disease in women. Am J Epidemiol 140:256-261.
49. Paganini-Hill A, Henderson VW (1996) Estrogen replacement therapy and risk of Alzheimer disease. Arch Intern Med 156:2213-2217.
50. Paganini-Hill A, Ross RK, Henderson BE (1988) Postmenopausal oestrogen treatment and stroke: a prospective study. BMJ 297:519-522.
51. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. New York: Academic.
52. Plesnila N, Zinkel S, Le DA, Amin-Hanjani S, Wu Y, Qui J, Chiarugi A, Thomas SS, Kohane DS, Korsmeyer SJ, Moskowitz MA (2001) BID mediates neuronal cell death after oxygen/glucose deprivation and focal cerebral ischemia. Proc Natl Acad Sci USA 98:15318-15323.
53. Roof RL, Hall ED (2000) Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J Neurotrauma 17:367-388.
54. Rusa R, Alkayed NJ, Crain BJ, Traystman RJ, Kimes AS, London ED, Klaus JA, Hurn PD (1999) 17beta-estradiol reduces stroke injury in estrogen-deficient female animals. Stroke 30:1665-1670.
55. Sato S, Gobbel GT, Honkaniemi J, Li Y, Kondo T, Murakami K, Sato M, Copin J-C, Sharp FR, Chan PH (1998) Decreased expression of bcl-2 and bcl-x mRNA coincides with apoptosis following intracerebral administration of 3-nitropropionic acid. Brain Res 808:56-64.
56. Sawada H, Shimohama S (2000) Neuroprotective effects of estradiol in mesencephalic dopaminergic neurons. Neurosci Biobehav Rev 24:143-147.
57. Schmidt R, Fazekas F, Reinhart B, Kapeller P, Fazekas G, Offenbacher H, Eber B, Schumacher M, Freidl W (1996) Estrogen replacement therapy in older women: a neuropsychological and brain MRI study. J Am Geriatr Soc 44:1307-1313.
58. Sherwin BB (1999) Can estrogen keep you smart? Evidence from clinical studies. J Psychiatry Neurosci 24:315-321.
59. Shibata M, Yamawaki T, Sasaki T, Hattori H, Hamada J, Fukuuchi Y, Okano H, Miura M (2002) Upregulation of Akt phosphorylation at the early stage of middle cerebral artery occlusion in mice. Brain Res 942:1-10.
60. Shughrue PJ, Merchenthaler I (2003) Estrogen prevents the loss of CAI hippocampal neurons in gerbils after ischemic injury. Neuroscience 116:851-861.
61. Simpkins JW, Rajakumar G, Zhang Y-Q, 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.
62. Singh M (2001) Ovarian hormones elicit phosphorylation of Akt and extracellular-signal regulated kinase in explants of cerebral cortex. Endocrine 14:407-415.
63. Smith MS, Freeman ME, Neill JD (1975) The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96:219-226.
64. 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.
65. Toran-Allerand CD, Singh M, Setalo Jr G (1999) Novel mechanisms of estrogen action in the brain: new players in an old story. Front Neuroendocrinol 20:97-121.
66. Toung TJK, Traystman RJ, Hurn PD (1998) Estrogen-mediated neuroprotection after experimental stroke in male rats. Stroke 29:1666-1670.
67. Wang KKW (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23:20-26.
68. Wang PN, Liao SQ, Liu RS, Liu CY, Chao HT, Lu SR, Yu HY, Wang SJ, Liu HC (2000) Effects of estrogen on cognition, mood, and cerebral blood flow in AD: a controlled study. Neurology 54:2061-2066.
69. Wang X, Wang H, Xu L, Rozanski DJ, Sugawara T, Chan PH, Trzaskos JM, Feuerstein GZ (2003) Significant neuroprotection against ischemic brain injury by inhibition of the MEK1 protein kinase in mice: exploration of potential mechanisms associated with apoptosis. J Pharmacol Exp Ther 304:172-178.
70. Waring SC, Rocca WA, Petersen RC, O'Brien PC, Tangalos EG, Kokmen E (1999) Postmenopausal estrogen replacement therapy and risk of AD: a population-based study. Neurology 52:965-970.
71. Willingham MC (1999) Cytochemical methods for the detection of apoptosis. J Histochem Cytochem 47:1101-1109.
72. Wilson ME, Liu Y, Wise PM (2002) Estradiol enhances Akt activation in cortical explant cultures following neuronal injury. Brain Res Mol Brain Res 102:48-54.
73. Wise PM (2003) Neuroprotective actions of estradiol in brain injury. Endocr Rev, in press.
74. Wise PM, Dubal DB, Wilson ME, Rau SW, Liu Y (2001) Estrogens: trophic and protective factors in the adult brain. Front Neuroendocrinol 22:33-66.
75. Woolley CS (1999) Effect of estrogen in the CNS. Curr Opin Neurobiol 9:345-354.
76. Writing Group for the Women's Health Initiative Investigators (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288:321-333.
77. Yang L, Matthews RT, Schulz JB, Klockgether T, Liao AW, Martinou JC, Penney Jr JB, Hyman BT, Beal MF (1998) 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyride neurotoxicity is attenuated in mice overexpressing Bcl-2. J Neurosci 18:8145-8152.
78. Zhang Y-Q, Shi J, Rajakumar G, Day AL, Simpkins JW (1998) Effects of gender and estradiol treatment on focal brain ischemia. Brain Res 784: 321-324.