17β-Estradiol protects the neonatal brain from hypoxia-ischemia

Experimental Neurology

Volumn 208, Issue 2, 2007, Pages 269-276

  Nuñez, Joseph ^a   Yang, Zhengang ^b   Jiang, Yuhui ^b   Grandys, Theresa ^a   Mark, Ilana ^a   Levison, Steven W ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Amygdala; Basal ganglia; Hippocampus; Sex difference; Steroid hormones

Indexed keywords

ESTRADIOL; NEUROPROTECTIVE AGENT; SEX HORMONE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN DAMAGE; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN MATURATION; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HORMONE BLOOD LEVEL; HYPOTHESIS; MALE; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; RISK ASSESSMENT; SEX DIFFERENCE; SINGLE DRUG DOSE; ANIMAL; BRAIN; DENTATE GYRUS; DRUG ADMINISTRATION; DRUG EFFECT; PATHOLOGY;

AMYGDALA; ANIMALS; ANIMALS, NEWBORN; BASAL GANGLIA; BRAIN; BRAIN ISCHEMIA; DENTATE GYRUS; DRUG ADMINISTRATION SCHEDULE; ESTRADIOL; FEMALE; HIPPOCAMPUS; HYPOXIA, BRAIN; MALE; NEUROPROTECTIVE AGENTS; RATS;

EID: 36048934367     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.08.020     Document Type: Article

References (69)

1. Abrahám I.M., and Herbison A.E. Major sex differences in non-genomic estrogen actions on intracellular signaling in mouse brain in vivo. Neuroscience 131 (2005) 945-951
2. Amateau S.K., Alt J.J., Stamps C.L., and McCarthy M.M. Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 145 (2004) 2906-2917
3. Andine P., Thordstein M., Kjellmer I., Nordborg C., Thiringer K., Wennberg E., and Hagberg H. Evaluation of brain damage in a rat model of neonatal hypoxic-ischemia. J. Neurosci. Methods 35 (1990) 253-260
4. Ardeshiri A., Kelley M.H., Korner I.P., Hurn P.D., and Herson P.S. Mechanisms of progesterone neuroprotection of rat cerebellar Purkinje cells following oxygen-glucose deprivation. Eur. J. Neurosci. 24 (2006) 2567-2574
5. Arnold A.P., and Gorski R.A. Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 7 (1984) 413-442
6. Balthazart J., Cornil C.A., Taziaux M., Charlier T.D., Baillien M., and Ball G.F. Rapid changes in production and behavioral action of estrogens. Neuroscience 138 (2006) 783-791
7. Basu A., Krady J.K., O'Malley M., Stryen S.D., DeKosky S.T., and Levison S.W. The type 1 interleukin-1 receptor is essential for the efficient activation of microglia in response to brain injury and the expression of specific pre-inflammatory mediators. J. Neurosci. 22 (2002) 6071-6082
8. Bi R., Broutman G., Foy M.R., Thompson R.F., and Baudry M. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3602-3607
9. Billiards S.S., Pierson C.R., Haynes R.L., Folkerth R.D., and Kinney H.C. Is the late preterm infant more vulnerable to gray matter injury than the term infant?. Clin. Perinatol. 33 (2006) 915-933
10. Brazel C.Y., Rosti R.T., Boyce S., Rothstein R.P., and Levison S.W. Perinatal hypoxia-ischemia damages and depletes progenitors from the mourse subventricular zone. Dev. Neurosci. 26 (2004) 266-274
11. Chen J., Adachi N., Liu K., and Arai T. The effects of 17beta-estradiol on ischemia-induced neuronal damage in the gerbil hippocampus. Neuroscience 87 (1998) 817-822
12. Chen S., Nilsen J., and Brinton R.D. Dose and temporal pattern of estrogen exposure determines neuroprotective outcome in hippocampal neurons: therapeutic implications. Endocrinology 147 (2006) 5303-5313
13. Clancy B., Finlay B.L., Darlington R.B., and Anand K.J. Extrapolating brain development from experimental species to humans. Neurotoxicology 28 (2007) 892-898
14. Corbier P., Edwards D.A., and Roffi J. The neonatal testosterone surge: a comparative study. Arch. Int. Physiol. Biochim. Biophys. 100 (1992) 127-131
15. Culmsee C., Vedder H., Ravati A., Junker V., Otto D., Ahlemeyer B., Krieg J.C., and Krieglstein J. 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 (1999) 1263-1269
16. Cutler S.M., VanLandingham J.W., Murphy A.Z., and Stein D.G. Slow-release and injected progesterone treatments enhance acute recovery after traumatic brain injury. Pharmacol. Biochem. Behav. 84 (2006) 420-428
17. De Butte-Smith M., Nguyen A.P., Zukin R.S., Etgen A.M., and Colbourne F. Failure of estradiol to ameliorate global ischemia-induced CA1 sector injury in middle-aged female gerbils. Brain Res. 1153 (2007) 214-220
18. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 3 (1979) 79-83
19. Dohler K.D., and Wuttke W. Changes with age in levels of serum gonadotropins, prolactin and gonadal steroids in prepubertal male and female rats. Endocrinology 97 (1975) 898-907
20. Dubal D.B., Shughrue P.J., Wilson M.E., Merchenthaler I., and Wise P.M. Estradiol modulates bcl-2 in cerebral ischemia: a potential role for estrogen receptors. J. Neurosci. 19 (1999) 6385-6393
21. Dzhala V.I., Talos D.M., Sdrulla D.A., Brumback A.C., Mathews G.C., Benke T.A., Delpire E., Jensen F.E., and Staley K.J. NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11 (2005) 1205-1213
22. Forest M.G. Plasma androgens (testosterone and 4-androstenedione) and 17-hydroxyprogesterone in the neonatal and peripubertal periods in the human and rat: differences between species. J. Steroid Biochem. 11 (1979) 543-548
23. Fugger H.N., Kumar A., Lubahn D.B., Korach K.S., and Foster T.C. Examination of estradiol effects on the rapid estradiol mediated increase in hippocampal synaptic transmission in estrogen receptor alpha knockout mice. Neurosci. Lett. 309 (2001) 207-209
24. Galindo R., Zamudio P.A., and Valenzuela C.F. Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J. Neurochem. 94 (2005) 1500-1511
25. George F.W., and Ojeda S.R. Changes in aromatase activity in the rat brain during embryonic, neonatal, and infantile development. Endocrinology 111 (1982) 522-529
26. Gerall A.A., Moltz H., and Ward I.L. Handbook of behavioral neurobiology: sexual differentiation. In: Gerall, Moltz, and Ward (Eds). Handbook of Behavioral Neurobiology vol. 11 (1991), Plenum Press, New York
27. Golub M.S., Kaufman F.L., Campbell M.A., Li L.H., and Donald J.M. "Natural" progesterone: information on fetal effects. Birth Defects Ser. 77 (2006) 455-470
28. Green P.S., Yang S.H., Nilsson K.R., Kumar A.S., Covey D.F., and Simpkins J.W. The nonfeminizing enantiomer of 17beta-estradiol exerts protective effects in neuronal cultures and a rat model of cerebral ischemia. Endocrinology 142 (2001) 400-406
29. Hall E.D., Pazara K.E., and Linseman K.L. Sex differences in postischemic neuronal necrosis in gerbils. J. Cereb. Blood Flow Metab. 11 (1991) 292-298
30. Harms C., Lautenschlager M., Bergk A., Katchanov J., Freyer D., Kapinya K., Herwig U., Megow D., Dirnagl U., Weber J.R., and Hortnagl H. Differential mechanisms of neuroprotection by 17 beta-estradiol in apoptotic versus necrotic neurodegeneration. J. Neurosci. 21 (2001) 2600-2609
31. Heyer A., Hasselblatt M., von Ahsen N., Häfner H., Sirén A.L., and Ehrenreich H. In vitro gender differences in neuronal survival on hypoxia and in 17beta-estradiol-mediated neuroprotection. J. Cereb. Blood Flow Metab. 25 (2005) 427-430
32. Hilton G.D., Nuñez J.L., Bambrick L.L., Thompson S.M., and McCarthy M.M. Glutamate-mediated excitotoxicity in neonatal hippocampal neurons is mediated by mGluR-induced release of calcium from intracellular stores and is prevented by estradiol. Eur. J. Neurosci. 24 (2006) 3008-3016
33. Huang Y., Huang Y.L., Zhang S., Zhu Y.C., and Yao T. Estradiol acutely attenuates glutamate-induced calcium overload in primarily cultured rat hippocampal neurons through a membrane receptor-dependent mechanism. Brain Res. 1026 (2004) 254-260
34. Jensen F.E. Developmental factors regulating susceptibility to perinatal brain injury and seizures. Curr. Opin. Pediatr. 18 (2006) 628-633
35. Jover T., Tanaka H., Calderone A., Oguro K., Bennett M.V., Etgen A.M., and Zukin R.S. Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. J. Neurosci. 22 (2002) 2115-2124
36. Khalilov I., Le Van Quyen M., Gozlan H., and Ben-Ari Y. Epileptogenic actions of GABA and fast oscillations in the developing hippocampus. Neuron 48 (2005) 787-796
37. Knickermeyer R.C., and Baron-Cohen S. Fetal testosterone and sex differences. Early Hum. Dev. 82 (2006) 755-760
38. Lauterbach M.D., Raz S., and Sander C.J. Neonatal hypoxic risk in preterm birth infants: the influence of sex and severity of respiratory distress on cognitive recovery. Neuropsychology 15 (2001) 411-420
39. Linford N., Wade C., and Dorsa D. The rapid effects of estrogen are implicated in estrogen-mediated neuroprotection. J. Neurocytol. 29 (2000) 367-374
40. Marin R., Guerra B., Alonso R., Ramírez C.M., and Díaz M. Estrogen activates classical and alternative mechanisms to orchestrate neuroprotection. Curr. Neurovasc. Res. 2 (2005) 287-301
41. Mattson M.P., Guthrie P.B., and Kater S.B. A role for Na+-dependent Ca2+ extrusion in protection against neuronal excitotoxicity. FASEB J. 3 (1989) 2519-2526
42. Mize A.L., Shapiro R.A., and Dorsa D.M. Estrogen receptor-mediated neuroprotection from oxidative stress requires activation of the mitogen-activated protein kinase pathway. Endocrinology 144 (2003) 306-312
43. Musa M.A., Khan M.O., and Cooperwood J.S. Medicinal chemistry and emerging strategies applied to the development of selective estrogen receptor modulators (SERMs). Curr. Med. Chem. 14 (2007) 1249-1261
44. Nuñez J.L., Bambrick L.L., Krueger B.K., and McCarthy M.M. Prolongation and enhancement of gamma-aminobutyric acid receptor mediated excitation by chronic treatment with estradiol in developing rat hippocampal neurons. Eur. J. Neurosci. 21 (2005) 3251-3261
45. Nuñez J.L., and McCarthy M.M. Estradiol exacerbates hippocampal damage in a model of preterm infant brain injury. Endocrinology 144 (2003) 2350-2359
46. Nyakas C., Buwalda B., and Luiten P.G. Hypoxia and brain development. Prog. Neurobiol. 49 (1996) 1-51
47. Perez S.E., Chen E.Y., and Mufson E.J. Distribution of estrogen receptor alpha and beta immunoreative profiles in the postnatal rat brain. Dev. Brain Res. 145 (2003) 117-139
48. Prokai L., Prokai-Tatrai K., Perjesi P., Zharikova A.D., Perez E.J., Liu R., and Simpkins J.W. Quinol-based cyclic antioxidant mechanism in estrogen neuroprotection. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 11741-11746
49. Rice J.E., Vannucci R.C., and Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9 (1981) 131-141
50. Romijn H.J., Hofman M.A., and Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby?. Early Hum. Dev. 26 (1991) 61-67
51. Simon N.P. Long-term neurodevelopmental outcome of asphyxiated newborns. Clin. Perinatol. 26 (1999) 767-778
52. Singer C.A., Rogers K.L., and Dorsa D.M. Modulation of Bcl-2 expression: a potential component of estrogen protection in NT2 neurons. Neuroreport 9 (1998) 2565-2568
53. Solum D.T., and Handa R.J. Localization of estrogen receptor alpha in pyramidal neurons of the developing rat hippocampus. Dev. Brain Res. 128 (2001) 165-175
54. Stein D.G., Wright D.W., and Kellermann A.L. Does progesterone have neuroprotective properties. Ann. Emerg. Med. 50 (2007) 501-510
55. Stoltzner S.E., Berchtold N.C., Cotman C.W., and Pike C.J. Estrogen regulates bcl-x expression in rat hippocampus. Neuroreport 12 (2001) 2797-2800
56. Toung T.J., Traystman R.J., and Hurn P.D. Estrogen-mediated neuroprotection after experimental stroke in male rats. Stroke 29 (1998) 1666-1670
57. Vannucci R.C. Experimental biology of cerebral hypoxia-ischemia: relation to perinatal brain damage. Pediatr. Res. 27 (1990) 317-326
58. Vannucci R.C. Experimental models of perinatal hypoxic-ischemic brain damage. APMIS Suppl. 40 (1993) 89-95
59. Vannucci R.C., Christensen M.A., and Yager J.Y. Nature, time-course, and extent of cerebral edema in perinatal hypoxic-ischemic brain damage. Pediatr. Neurol. 9 (1993) 29-34
60. Warne G.L., Faiman C., Reyes F.I., and Winter J.S. Studies on human sexual development. V. Concentrations of testosterone, 17-hydroxyprogesterone and progesterone in human amniotic fluid through gestation. J. Clin. Endocrinol. Metab. 44 (1977) 934-939
61. Weisz J., and Ward I.L. Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology 106 (1980) 306-316
62. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Böttner M., and Rosewell K.L. Estradiol is a protective factor in the adult and aging brain: understanding of mechanisms derived from in vivo and in vitro studies. Brain Res. Brain Res. Rev. 37 (2001) 313-319
63. Xu L., Sapolsky R.M., and Giffard R.G. Differential sensitivity of murine astrocytes and neurons from different brain regions to injury. Exp. Neurol. 169 (2001) 416-424
64. Yager J.Y., Wright S., Armstrong E.A., Jahraus C.M., and Saucier D.M. A new model for determining the influence of age and sex on functional recovery following hypoxic-ischemic brain damage. Dev. Neurosci. 27 (2005) 112-120
65. Yokosuka M., Okamura H., and Hayashi S. Postnatal development and sex difference in neurons containing estrogen receptor alpha immunoreactivity in the preoptic brain, the diencephalon, and the amygdale in the rat. J. Comp. Neurol. 389 (1997) 81-93
66. Young C., Jevtovic-Todorovic V., Qin Y.Q., Tenkova T., Wang H., Labruyere J., and Olney J.W. Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain. Br. J. Pharmacol. 146 (2005) 189-197
67. Zhang Y., Milatovic D., Aschner M., Feustel P.J., and Kimelberg H.K. Neuroprotection by tamoxifen in focal cerebral ischemia is not mediated by an agonist action at estrogen receptors but is associated with antioxidant activity. Exp. Neurol. 204 (2007) 819-827
68. Zhao L., Wu T.W., and Brinton R.D. Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Res. 1010 (2004) 22-34
69. Zhao L., Chen S., Ming Wang J., and Brinton R.D. 17beta-estradiol induces Ca2+ influx, dendritic and nuclear Ca2+ rise and subsequent cyclic AMP response element-binding protein activation in hippocampal neurons: a potential initiation mechanism for estrogen neurotrophism. Neuroscience 132 (2005) 299-311