Estradiol is a potent protective, restorative, and trophic factor after brain injury

Seminars in Reproductive Medicine

Volumn 27, Issue 3, 2009, Pages 240-249

  Brown, Candice M ^a,b   Suzuki, Shotaro ^a   Jelks, Karen A B ^c   Wise, Phyllis M ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cerebral ischemia; Estradiol; Estrogen therapy; Neuroprotection; Stroke

Indexed keywords

ESTRADIOL; ESTROGEN;

APOPTOSIS; BRAIN INJURY; BRAIN ISCHEMIA; CELL DEATH; DICHOTIC LISTENING; DRUG EFFICACY; DRUG MECHANISM; ESTROGEN THERAPY; GENITAL SYSTEM; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NEUROPROTECTION; NONHUMAN; REVIEW; RISK FACTOR;

ANIMALS; APOPTOSIS; BRAIN INJURIES; CEREBROVASCULAR DISORDERS; ENCEPHALITIS; ESTRADIOL; FEMALE; HUMANS; MALE; MODELS, ANIMAL; NEUROGENESIS; NEUROPROTECTIVE AGENTS; RECEPTORS, ESTROGEN;

EID: 67649657689     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0029-1216277     Document Type: Review

References (54)

1. Turgeon JL, Carr MC, Maki PM, Mendelsohn ME, Wise PM. Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: insights from basic science and clinical studies. Endocr Rev 2006;27:575-605 (Pubitemid 44582052)
2. Behl C. Oestrogen as a neuroprotective hormone. Nat Rev Neurosci 2002;3:433-442 (Pubitemid 135711799)
3. McCullough LD, Hurn PD. Estrogen and ischemic neuroprotection: an integrated view. Trends Endocrinol Metab 2003;14:228-235 (Pubitemid 36841481)
4. Anderson GL, Limacher M, Assaf AR, et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004;291:1701-1712 (Pubitemid 38489892)
5. Rosamond W, Flegal K, Furie K, et al. Heart disease and stroke statistics-2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2008;117:e25-e146
6. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999; 22:391-397 (Pubitemid 29453643)
7. Gibson CL, Gray LJ, Murphy SP, Bath PM. Estrogens and experimental ischemic stroke: a systematic review. J Cereb Blood Flow Metab 2006;26:1103-1113 (Pubitemid 44268172)
8. Dubal DB, Kashon M, Pettigrew L, et al. Estradiol protects against ischemic injury. J Cereb Blood Flow Metab 1998; 18:1253-1258 (Pubitemid 28509840)
9. Dubal DB, Zhu H, Yu J, et al. Estrogen receptor alpha, not beta is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci U S A 2001;98:1952-1957 (Pubitemid 32165604)
10. Levin ER. Integration of the extranuclear and nuclear actions of estrogen 210/me.2004-0390. Mol Endocrinol 2005;19: 1951-1959
11. Dubal DB, Rau SW, Shughrue PJ, et al. Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ER{alpha} in estradiol-mediated protection against delayed cell death. Endocrinology 2006;147:3076-3084 (Pubitemid 43764643)
12. Dubal DB, Shughrue PJ, Wilson ME, Merchenthaler I, Wise PM. Estradiol modulates bcl-2 in cerebral ischemia: a potential role for estrogen receptors. J Neurosci 1999;19: 6385-6393 (Pubitemid 29347438)
13. Suzuki S, Brown CM, Dela Cruz CD, et al. Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions. Proc Natl Acad Sci U S A 2007;104:6013-6018 (Pubitemid 47175650)
14. Suzuki S, Gerhold LM, Bottner M, et al. Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J Comp Neurol 2007;500:1064-1075 (Pubitemid 46110642)
15. Zhang F, Yin W, Chen J. Apoptosis in cerebral ischemia: executional and regulatory signaling mechanisms. Neurol Res 2004;26:835-845 (Pubitemid 39628561)
16. Rau SW, Dubal DB, Bottner M, Gerhold LM, Wise PM. Estradiol attenuates programmed cell death after stroke-like injury. J Neurosci 2003;23:11420-11426 (Pubitemid 37549698)
17. Rau SW, Dubal DB, Bottner M, Wise PM. Estradiol differentially regulates c-Fos after focal cerebral ischemia. J Neurosci 2003;23:10487-10494 (Pubitemid 37485261)
18. Taupin P, Gage FH. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 2002;69:745-749 (Pubitemid 34984691)
19. Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci 2002;22:629-634 (Pubitemid 34141742)
20. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994;264:1145-1148 (Pubitemid 24210676)
21. Tonchev AB, Yamashima T, Sawamoto K, Okano H. Enhanced proliferation of progenitor cells in the subventricular zone and limited neuronal production in the striatum and neocortex of adult macaque monkeys after global cerebral ischemia. J Neurosci Res 2005;81:776-788 (Pubitemid 41532143)
22. Goings GE, Sahni V, Szele FG. Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury. Brain Res 2004;996:213-226 (Pubitemid 38022018)
23. Arvidsson A, Collin T, Krik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002;8:963-970 (Pubitemid 35033700)
24. Paganini-Hill A. Hormone replacement therapy and stroke: risk, protection or no effect? Maturitas 2001;38:243-261
25. Wassertheil-Smoller S, Hendrix SL, Limacher M, et al. Effect of estrogen plus progestin on stroke in postmenopausal women. JAMA 2003;289:2673-2684
26. Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321-333 (Pubitemid 34761611)
27. Viscoli CM, Brass LM, Kernan WN, et al. A clinical trial of estrogen-replacement therapy after ischemic stroke. N Engl J Med 2001;345:1243-1249 (Pubitemid 34951488)
28. Bushnell CD, Hurn P, Colton C, et al. Advancing the study of stroke in women: summary and recommendations for future research from an NINDS-sponsored multidisciplinary working group. Stroke 2006;37:2387-2399 (Pubitemid 44337191)
29. Turgeon JL, McDonnell DP, Martin KA, Wise PM. Hormone therapy: physiological complexity belies therapeutic simplicity. Science 2004;304:1269-1273 (Pubitemid 38697412)
30. Bushnell CD. Hormone replacement therapy and stroke: the current state of knowledge and directions for future research. Semin Neurol 2006;26:123-130 (Pubitemid 43277370)
31. Miller VM, Clarkson TB, Harman SM, et al. Women, hormones, and clinical trials: a beginning, not an end. J Appl Physiol 2005;99:381-383 (Pubitemid 41061128)
32. Harman SM, Naftolin F, Brinton EA, Judelson DR. Is the estrogen controversy over? Deconstructing the Women's Health Initiative study: a critical evaluation of the evidence Ann N Y Acad Sci 2005;1052:43-56
33. Rossouw JE, Prentice RL, Manson JE, et al. Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. JAMA 2007;297:1465-1477 (Pubitemid 46556472)
34. Vegeto E, Benedusi V, Maggi A. Estrogen anti-inflammatory activity in brain: a therapeutic opportunity for menopause and neurodegenerative diseases. Front Neuroendocrinol 2008;29: 507-519
35. VegetoE,Bonincontro C, PollioG, et al. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J Neurosci 2001;21:1809-1818 (Pubitemid 32221364)
36. Czlonkowska A, Ciesielska A, Gromadzka G, Kurkowska- Jastrzebska I. Gender differences in neurological disease. Endocrine 2006;29:243-256
37. Tiwari-Woodruff S, Morales LB, Lee R, Voskuhl RR. Differential neuroprotective and antiinflammatory effects of estrogen receptor (ER)alpha and ERbeta ligand treatment. Proc Natl Acad Sci U S A 2007;104:14813-14818 (Pubitemid 350003225)
38. Vegeto E, Belcredito S, Etteri S, et al. Estrogen receptor-α mediates the brain antiinflammatory activity of estradiol. Proc Natl Acad Sci U S A 2003;100:9614-9619 (Pubitemid 37033976)
39. Lewis DK, Johnson AB, Stohlgren S, Harms A, Sohrabji F. Effects of estrogen receptor agonists on regulation of the inflammatory response in astrocytes from young adult and middle-aged female rats. J Neuroimmunol 2008;195:47-59
40. Baker AE, Brautigam VM, Watters JJ. Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor beta. Endocrinology 2004;145:5021-5032 (Pubitemid 39551121)
41. Brown CM, Dela Cruz CD, Yang E, Wise PM. Inducible nitric oxide synthase and estradiol exhibit complementary neuroprotective roles after ischemic brain injury. Exp Neurol 2008;210:782-787
42. Toran-Allerand CD. Organotypic culture of the developing cerebral cortex and hypothalamus: relevance to sexual differentiation. Psychoneuroendocrinology 1991;16:7-24
43. Toran-Allerand CD. Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res 1976;106: 407-412
44. Woolley CS, McEwen BS. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 1992;12:2549-2554
45. Woolley CS, Gould E, Frankfurt M, McEwen BS. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 1990;10:4035-4039
46. Murphy DD, Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 1996;16:4059-4068 (Pubitemid 26192402)
47. Brinton RD, Tran J, Proffitt P, Montoya M. 17 beta- Estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochem Res 1997;22:1339-1351 (Pubitemid 27461133)
48. Lee SJ, McEwen BS. Neurotrophic and neuroprotective actions of estrogens and their therapeutic implications. Annu Rev Pharmacol Toxicol 2001;41:569-591 (Pubitemid 32385899)
49. Brann DW, Dhandapani K, Wakade C, Mahesh VB, Khan MM. Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids 2007;72: 381-405 (Pubitemid 46602478)
50. Dominguez R, Liu R, Baudry M. 17-beta-Estradiolmediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-D-aspartate receptor phosphorylation in cortical synaptoneurosomes. J Neurochem 2007;101:232-240 (Pubitemid 46426479)
51. 2+ transients in spines of CA1 pyramidal neurons from hippocampal slices. J Neurophysiol 1999;81:1404-1411 (Pubitemid 29272456)
52. Jelks KB, Wylie R, Floyd CL, McAllister AK, Wise P. Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-alpha. J Neurosci 2007;27:6903-6913 (Pubitemid 47015894)
53. McEwen B, Akama K, Alves S, et al. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc Natl Acad Sci U S A 2001;98:7093-7100 (Pubitemid 32567908)
54. McCollum AT, Nasr P, Estus S. Calpain activates caspase-3 during UV-induced neuronal death but only calpain is necessary for death. J Neurochem 2002;82:1208-1220 (Pubitemid 34966633)