Neuroprotection and sex steroid hormones: Evidence of estradiol- mediated protection in hypertensive encephalopathy

Mini-Reviews in Medicinal Chemistry

Volumn 12, Issue 11, 2012, Pages 1081-1089

  de Nicola, A F ^a,b   Brocca, M E ^a   Pietranera, L ^a,b   Garcia Segura, L M ^c  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c INSTITUTO CAJAL   (Spain)

Author keywords

Estradiol; Hippocampus; Hypertension; Hypothalamus; Neuroprotection

Indexed keywords

ARGININE; AROMATASE; BRAIN DERIVED NEUROTROPHIC FACTOR; BROXURIDINE; DOUBLECORTIN; ESTRADIOL; ESTRADIOL RECEPTOR; MESSENGER RNA; VASOPRESSIN; VASOPRESSIN V1B RECEPTOR;

AGING; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BLOOD PRESSURE; BRAIN CELL; DENTATE GYRUS; DIABETES MELLITUS; ESSENTIAL HYPERTENSION; HIPPOCAMPUS; HUMAN; HYPERTENSION ENCEPHALOPATHY; HYPOTHALAMUS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; SPONTANEOUSLY HYPERTENSIVE RAT;

ANIMALS; BLOOD PRESSURE; BRAIN; ESTRADIOL; HUMANS; HYPERTENSIVE ENCEPHALOPATHY; NEUROPROTECTIVE AGENTS;

EID: 84866981760     PISSN: 13895575     EISSN: 18755607     Source Type: Journal    
DOI: 10.2174/138955712802762121     Document Type: Article

References (90)

1. Wise, P. M. Estrogen therapy: does it help or hurt the adult and aging brain? Insights derived from animal models. Neuroscience, 2006, 138, 831-835.
2. Goodman, Y.; Bruce, A. J.; Cheng, B.; Mattson, M. P. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J Neurochem., 1996, 66, 1836-1844.
3. McEwen, B. S. Estrogen actions throughout the brain. Re.c Prog. Horm. Res., 2002, 57, 357-384.
4. McCullough, L. D.; Hurn, P. D. Estrogen and ischemic neuroprotection: an integrated view. Trends Endocrinol. Metab., 2003, 14, 228-235.
5. Garcia-Segura, L. M.; Melcangi, R. C. Steroids and glial cell function. Glia, 2006, 54, 485-498.
6. Suzuki, S.; Gerhold, L. M.; Bottner, M.; Rau, S. W.; Dela, C. C.; Yang, E.; Zhu, H.; Yu, J.; Cashion, A. B.; Kindy, M. S.; Merchenthaler, I.; Gage, F. H.; Wise, P. M. Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J. Comp. Neurol., 2007, 500, 1064-1075.
7. Shughrue, P. J.; Lane, M. V.; Scrimo, P. J.; Merchenthaler, I. Comparative distribution of estrogen receptor-alpha (ER-alpha) and beta (ER-beta) mRNA in the rat pituitary, gonad, and reproductive tract. Steroids, 1998, 63, 498-504.
8. Garcia-Segura L.M., Arévalo, M.A., Azcoitia, I. Interactions of estradiol and insulin-like growth factor-I signalling in the nervous system: new advances. Prog. Brain Res., 2010, 181, 251-72.
9. Gould, E.; Tanapat, P.; Rydel, T.; Hastings, N. Regulation of hippocampal neurogenesis in adulthood. Biol. Psychiatry, 2000, 48, 715-720.
10. McEwen, B.; Akama, K.; Alves, S.; Brake, W. G.; Bulloch, K.; Lee, S.; Li, C.; Yuen, G.; Milner, T. A. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc. Natl. Acad Sci U. S. A, 2001, 98, 7093-7100.
11. Behl, C. Oestrogen as a neuroprotective hormone. Nat. Rev. Neurosci., 2002, 3, 433-442.
12. Scharfman, H. E.; MacLusky, N. J. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front. Neuroendocrinol., 2006, 27, 415-435.
13. De Nicola, A. F.; Saravia, F. E.; Beauquis, J.; Pietranera, L.; Ferrini, M. G. Estrogens and neuroendocrine hypothalamicpituitary-adrenal axis function. Front. Horm. Re.s, 2006, 35157-168.
14. Manthey, D; Behl, C. From structural biochemistry to expression profiling: neuroprotective activities of estrogen. Neuroscience, 2006, 138, 845-850.
15. Saravia, F.; Revsin, Y.; Lux-Lantos, V.; Beauquis, J.; Homo-Delarche, F.; De Nicola, A. F. Oestradiol restores cell proliferation in dentate gyrus and subventricular zone of streptozotocin-diabetic mice. J. Neuroendocrinol., 2004, 16, 704-710.
16. Saravia, F.; Beauquis, J.; Pietranera, L.; De Nicola, A. F. Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice. Psychoneuroendocrinology, 2007, 32, 480-492.
17. Mulvany, M. J. Small artery remodeling and significance in the development of hypertension. News Physiol. Sci., 2002, 17, 105-109.
18. Rigsby, C. S.; Cannady, W. E.; Dorrance, A. M. Aldosterone: good guy or bad guy in cerebrovascular disease? Trends Endocrinol. Metab., 2005, 16, 401-406.
19. Skoog, I.; Lernfelt, B.; Landahl, S.; Palmertz, B.; Andreasson, L. A.; Nilsson, L.; Persson, G.; Oden, A.; Svanborg, A. 15-year longitudinal study of blood pressure and dementia. Lancet, 1996, 347, 1141-1145.
20. Korf, E. S.; White, L. R.; Scheltens, P.; Launer, L. J. Midlife blood pressure and the risk of hippocampal atrophy: the Honolulu Asia Aging Study. Hypertension, 2004, 44, 29-34.
21. Petrovitch, H.; White, L. R.; Izmirilian, G.; Ross, G. W.; Havlik, R. J.; Markesbery, W.; Nelson, J.; Davis, D. G.; Hardman, J.; Foley, D. J.; Launer, L. J. Midlife blood pressure and neuritic plaques, neurofibrillary tangles, and brain weight at death: the HAAS. Honolulu-Asia aging Study. Neurobiol. Aging, 2000, 21, 57-62.
22. Paglieri, C.; Bisbocci, D.; Caserta, M.; Rabbia, F.; Bertello, C.; Canade, A.; Veglio, F. Hypertension and cognitive function. Clin. Exp. Hypertens., 2008, 30, 701-710.
23. Tomassoni, D.; Avola, R.; Di Tullio, M. A.; Sabbatini, M.; Vitaioli, L.; Amenta, F. Increased expression of glial fibrillary acidic protein in the brain of spontaneously hypertensive rats. Clin. Exp. Hypertens., 2004, 26, 335-350.
24. Pietranera, L.; Saravia, F.; Roig, P.; Lima, A.; De Nicola, A. F. Mineralocorticoid treatment upregulates the hypothalamic vasopressinergic system of spontaneously hypertensive rats. Neuroendocrinology, 2004, 80, 100-110.
25. Saavedra, J. M. Opportunities and limitations of genetic analysis of hypertensive rat strains. J. Hypertens., 2009, 27, 1129-1133.
26. Rahmouni, K.; Barthelmebs, M.; Grima, M.; Imbs, J. L.; deJong, W. Involvement of brain mineralocorticoid receptor in saltenhanced hypertension in spontaneously hypertensive rats. Hypertension, 2001, 38, 902-906.
27. Kronenberg, G.; Lippoldt, A.; Kempermann, G. Two genetic rat models of arterial hypertension show different mechanisms by which adult hippocampal neurogenesis is increased. Dev. Neurosci., 2007, 29, 124-133.
28. Pietranera, L.; Saravia, F. E.; Roig, P.; Lima, A.; De Nicola, A. F. Protective effects of estradiol in the brain of rats with genetic or mineralocorticoid-induced hypertension. Psychoneuroendocrinology, 2008, 33, 270-281.
29. Pietranera, L.; Saravia, F.; Gonzalez Deniselle, M. C.; Roig, P.; Lima, A.; De Nicola, A. F. Abnormalities of the hippocampus are similar in deoxycorticosterone acetate-salt hypertensive rats and spontaneously hypertensive rats. J Neuroendocrinol., 2006, 18, 466-474.
30. Dorrance, A. M.; Rupp, N. C.; Nogueira, E. F. Mineralocorticoid receptor activation causes cerebral vessel remodeling and exacerbates the damage caused by cerebral ischemia. Hypertension, 2006, 47, 590-595.
31. Koch, B.; Sakly, M.; Lutz-Bucher, B. Specific mineralocorticoid receptors in the hippocampus of spontaneously hypertensive (SH) rats. I. Evidence for a sex difference. Horm. Metab Res., 1982, 14, 166-166.
32. Gomez-Sanchez, E. P. Brain mineralocorticoid receptors: orchestrators of hypertension and end-organ disease. Curr. Opin. Nephrol. Hypertens., 2004, 13, 191-196.
33. Mirshahi, M.; Nicolas, C.; Agarwal, M. K. Enhanced activation of the mineralocorticoid receptor in genetically hypertensive rats. Biochem. Biophys. Res. Commun., 1998, 244, 120-125.
34. Garcia-Segura, L. M.; Azcoitia, I.; DonCarlos, L. L. Neuroprotection by estradiol. Prog. Neurobiol., 2001, 63, 29-60.
35. Cherney, A.; Edgell, H.; Krukoff, T. L. NO mediates effects of estrogen on central regulation of blood pressure in restrained, ovariectomized rats. Am. J Physiol Regul. Integr. Comp. Physiol., 2003, 285, R842-R849.
36. Peng, N.; Clark, J. T.; Wei, C. C.; Wyss, J. M. Estrogen depletion increases blood pressure and hypothalamic norepinephrine in middle-aged spontaneously hypertensive rats. Hypertension, 2003, 41, 1164-1167.
37. Belo, N. O.; Silva-Barra, J.; Carnio, E. C.; Antunes-Rodrigues, J.; Gutkowska, J.; Dos Reis, A. M. Involvement of atrial natriuretic peptide in blood pressure reduction induced by estradiol in spontaneously hypertensive rats. Regul. Pept., 2004, 117, 53-60.
38. Xue, B.; Pamidimukkala, J.; Lubahn, D. B.; Hay, M. Estrogen receptor-alpha mediates estrogen protection from angiotensin IIinduced hypertension in conscious female mice. Am. J. Physiol. Heart Circ. Physiol., 2007, 292, H1770-H1776.
39. McEwen, B. S.; Milner, T. A. Hippocampal formation: Shedding light on the influence of sex and stress on the brain. Brain Res. Rev., 2007, 55, 343-355.
40. Spencer, J. L.; Waters, E. M.; Romeo, R. D.; Wood, G. E.; Milner, T. A.; McEwen, B. S. Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol., 2008, 29, 219-237.
41. Nomura, M.; McKenna, E.; Korach, K. S.; Pfaff, D. W.; Ogawa, S. Estrogen receptor-beta regulates transcript levels for oxytocin and arginine vasopressin in the hypothalamic paraventricular nucleus of male mice. Brain Res. Mol. Brain Res., 2002, 109, 84-94.
42. Pietranera, L.; Lima, A.; Roig, P.; De Nicola, A. F. Involvement of brain-derived neurotrophic factor and neurogenesis in oestradiol neuroprotection of the hippocampus of hypertensive rats. J. Neuroendocrinol., 2010, 22, 1082-1092.
43. Van Tol, H. H.; van den Buuse, M.; deJong, W.; Burbach, J. P. Vasopressin and oxytocin gene expression in the supraoptic and paraventricular nucleus of the spontaneously hypertensive rat (SHR) during development of hypertension. Brain Res., 1988, 464, 303-311.
44. De Wandener, H. E. The hypothalamus and hypertension. Physiol. Rev., 2001, 81, 1599-1658.
45. Burrell, L. M.; Philips, P. A.; Risvanis, J.; Aldred, K. L.; Hutchins, A. M.; Johnston, C. I. Attenuation of genetic hypertension after short-term vasopressin V1A receptor antagonism. Hypertension, 1995, 26, 828-834.
46. Alonso, R.; Griebel, G.; Pavone, G.; Stemmelin, J.; Le Fur, G.; Soubrie, P. Blockade of CRF(1) or V(1b) receptors reverses stressinduced suppression of neurogenesis in a mouse model of depression. Mol. Psychiatry, 2004, 9, 278-286.
47. Ito, K.; Hirooka, Y.; Kimura, Y.; Sagara, Y.; Sunagawa, K. Ovariectomy augments hypertension through rho-kinase activation in the brain stem in female spontaneously hypertensive rats. Hypertension, 2006, 48, 651-657.
48. Wang, D. D.; Bordey, A. The astrocyte odyssey. Prog. Neurobiol., 2008, 86, 342-367.
49. Sofroniew, M. V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci., 2009, 32, 638-647.
50. Bezzi, P., Volterra, A. A neuron-glia signalling network in the active brain. Curr. Opin. Neurobiol., 2001, 11, 387-394.
51. Sofroniew, M. V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci., 2009, 32, 638-647.
52. Hu, R.; Zhou, J.; Luo, C.; Lin, J.; Wang, X.; Li, X.; Bian, X.; Li, Y.; Wan, Q.; Yu, Y.; Feng, H. Glial scar and neuroregeneration: histological, functional, and magnetic resonance imaging analysis in chronic spinal cord injury. J. Neurosurg. Spine, 2010, 13, 169-180.
53. Goss, J. R.; Finch, C. E.; Morgan, D. G. Age-related changes in glial fibrillary acidic protein mRNA in the mouse brain. Neurobiol. Aging, 1991, 12, 165-170.
54. Nichols, N. R.; Day, J. R.; Laping, N. J.; Johnson, S. A.; Finch, C. E. GFAP mRNA increases with age in rat and human brain. Neurobiol. Aging, 1993, 14, 421-429.
55. Revsin, Y.; Saravia, F.; Roig, P.; Lima, A.; De Kloet, E. R.; Homo-Delarche, F.; De Nicola, A. F. Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes. Brain Res., 2005, 1038, 22-31.
56. Day, J. R.; Laping, N. J.; Lampert-Etchells, M.; Brown, S. A.; O'Callaghan, J. P.; McNeill, T. H.; Finch, C. E. Gonadal steroids regulate the expression of glial fibrillary acidic protein in the adult male rat hippocampus. Neuroscience, 1993, 55, 435-443.
57. Garcia-Ovejero, D.; Veiga, S.; Garcia-Segura, L. M.; DonCarlos, L. L. Glial expression of estrogen and androgen receptors after rat brain injury. J. Comp. Neurol., 2002, 450, 256-271.
58. Rozovsky, I.; Wei, M.; Stone, D. J.; Zanjani, H.; Anderson, C. P.; Morgan, T. E.; Finch, C. E. Estradiol (E2) enhances neurite outgrowth by repressing glial fibrillary acidic protein expression and reorganizing laminin. Endocrinology, 2002, 143, 636-646.
59. Larsson, A.; Wilhelmsson, U.; Pekna, M.; Pekny, M. Increased cell proliferation and neurogenesis in the hippocampal dentate gyrus of old GFAP(-/-)Vim(-/-) mice. Neurochem. Res., 2004, 29, 2069-2073.
60. Pekny, M.; Nilsson, M. Astrocyte activation and reactive gliosis. Glia, 2005, 50, 427-434.
61. Daniel, J. M. Effects of oestrogen on cognition: what have we learned from basic research? J. Neuroendocrinol., 2006, 18, 787-795.
62. Woolley, C. S. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol., 2007, 47, 657-680.
63. Tanapat, P.; Hastings, N. B.; Gould, E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J. Comp. Neurol., 2005, 481, 252-265.
64. Tanapat, P.; Hastings, N. B.; Reeves, A. J.; Gould, E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci., 1999, 19, 5792-5801.
65. Kempermann, G.; Gast, D.; Gage, F. H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by longterm environmental enrichment. Ann. Neurol., 2002, 52, 135-143.
66. Isgor, C.; Watson, S. J. Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone. Neuroscience, 2005, 134, 847-856.
67. Seri, B., García-Verdugo, J.M., McEwen, B.S., Alvarez-Buylla, A. Astrocytes give riseto new neurons in the adult mammalian hippocampus. J. Neurosci., 2001, 21, 7153-7160.
68. Sohrabji, F.; Miranda, R. C.; Toran-Allerand, C. D. Identification of a putative estrogen response element in the gene encoding brainderived neurotrophic factor. Proc. Natl. Acad. Sci. U. S. A, 1995, 92, 11110-11114.
69. Sato, K.; Akaishi, T.; Matsuki, N.; Ohno, Y.; Nakazawa, K. beta-Estradiol induces synaptogenesis in the hippocampus by enhancing brain-derived neurotrophic factor release from dentate gyrus granule cells. Brain Res., 2007, 1150, 108-120.
70. Chan, J. P.; Cordeira, J.; Calderon, G. A.; Iyer, L. K.; Rios, M. Depletion of central BDNF in mice impedes terminal differentiation of new granule neurons in the adult hippocampus. Mol. Cell Neurosci., 2008, 39, 372-383.
71. Li, T.; Jiang, L.; Zhang, X.; Chen, H. In-vitro effects of brainderived neurotrophic factor on neural progenitor/stem cells from rat hippocampus. Neuroreport, 2009, 20, 295-300.
72. Hennigan, A.; Callaghan, C. K.; Kealy, J.; Rouine, J.; Kelly, A. M. Deficits in LTP and recognition memory in the genetically hypertensive rat are associated with decreased expression of neurotrophic factors and their receptors in the dentate gyrus. Behav. Brain Res., 2009, 197, 371-377.
73. Lee, T. H.; Yang, J. T.; Kato, H.; Wu, J. H. Hypertension downregulates the expression of brain-derived neurotrophic factor in the ischemia-vulnerable hippocampal CA1 and cortical areas after carotid artery occlusion. Brain Res., 2006, 1116, 31-38.
74. Kageyama, H.; Nemoto, K.; Nemoto, F.; Sekimoto, M.; Nara, Y.; Nabika, T.; Iwayama, Y.; Fukamachi, K.; Tomita, I.; Senba, E.; Forehand, C. J.; Hendley, E. D.; Ueyama, T. Mutation of the trkB gene encoding the high-affinity receptor for brain-derived neurotrophic factor in stroke-prone spontaneously hypertensive rats. Biochem. Biophys. Res. Commun., 1996, 229, 713-718.
75. Schaaf, M. J.; De Kloet, E. R.; Vreugdenhil, E. Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation. Stress., 2000, 3, 201-208.
76. Herrick, S. P.; Waters, E. M.; Drake, C. T.; McEwen, B. S.; Milner, T. A. Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Res., 2006, 1121, 46-58.
77. Altar, C. A.; Cai, N.; Bliven, T.; Juhasz, M.; Conner, J. M.; Acheson, A. L.; Lindsay, R. M.; Wiegand, S. J. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature, 1997, 389, 856-860.
78. Naftolin, F.; Horvath, T. L.; Jakab, R. L.; Leranth, C.; Harada, N.; Balthazart, J. Aromatase immunoreactivity in axon terminals of the vertebrate brain. An immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology, 1996, 63, 149-155.
79. Balthazart, J.; Baillien, M.; Ball, G. F. Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology, 2006, 147, 359-366.
80. Yague, J. G.; Azcoitia, I.; DeFelipe, J.; Garcia-Segura, L. M.; Munoz, A. Aromatase expression in the normal and epileptic human hippocampus. Brain Res., 2010, 131, 541-552.
81. Yilmaz, M. B.; Wolfe, A.; Cheng, Y. H.; Glidewell-Kenney, C.; Jameson, J. L.; Bulun, S. E. Aromatase promoter I.f is regulated by estrogen receptor alpha (ESR1) in mouse hypothalamic neuronal cell lines. Biol. Reprod., 2009, 81, 956-965.
82. Hojo, Y.; Higo, S.; Ishii, H.; Ooishi, Y.; Mukai, H.; Murakami, G.; Kominami, T.; Kimoto, T.; Honma, S.; Poirier, D.; Kawato, S. Comparison between hippocampus-synthesized and circulationderived sex steroids in the hippocampus. Endocrinology, 2009, 150, 5106-5112.
83. Rune, G. M.; Lohse, C.; Prange-Kiel, J.; Fester, L.; Frotscher, M. Synaptic plasticity in the hippocampus: effects of estrogen from the gonads or hippocampus? Neurochem. Res., 2006, 31, 145-155.
84. Azcoitia, I.; Sierra, A.; Veiga, S.; Garcia-Segura, L. M. Aromatase expression by reactive astroglia is neuroprotective. Ann. N. Y. Acad. Sci., 2003, 1007, 298-305.
85. Zhao, C.; Fujinaga, R.; Yanai, A.; Kokubu, K.; Takeshita, Y.; Watanabe, Y.; Shinoda, K. Sex-steroidal regulation of aromatase mRNA expression in adult male rat brain: a quantitative nonradioactive in situ hybridization study. Cell Tissue Res., 2008, 332, 381-391.
86. Iivonen, S.; Heikkinen, T.; Puolivali, J.; Helisalmi, S.; Hiltunen, M.; Soininen, H.; Tanila, H. Effects of estradiol on spatial learning, hippocampal cytochrome P450 19, and estrogen alpha and beta mRNA levels in ovariectomized female mice. Neuroscience, 2006, 137, 1143-1152.
87. Pietranera, L.; Bellini, M. J.; Arevalo, M. A.; Goya, R.; Brocca, M. E.; Garcia-Segura, L. M.; De Nicola, A. F. Increased aromatase expression in the hippocampus of spontaneously hypertensive rats: effects of estradiol administration. Neuroscience, 2011, 174, 151-159.
88. Garcia-Segura, L. M. Aromatase in the brain: not just for reproduction anymore. J. Neuroendocrinol., 2008, 20, 705-712.
89. Resnick, S. M.; Maki, P. M.; Rapp, S. R.; Espeland, M. A.; Brunner, R.; Coker, L. H.; Granek, I. A.; Hogan, P.; Ockene, J. K.; Shumaker, S. A. Effects of combination estrogen plus progestin hormone treatment on cognition and affect. J Clin. Endocrinol. Metab., 2006, 91, 1802-1810.
90. Sherwin, B. B.; Henry, J. F. Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: a critical review. Front. Neuroendocrinol., 2008, 29, 88-113.