Aromatase expression by astrocytes after brain injury: Implications for local estrogen formation in brain repair

Neuroscience

Volumn 89, Issue 2, 1999, Pages 567-578

  Garcia Segura, L M ^a,c   Wozniak, A ^a   Azcoitia, I ^b,c   Rodriguez, J R ^c   Hutchison, R E ^a   Hutchison, J B ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c INSTITUTO CAJAL   (Spain)

Author keywords

Aromatase; Astroglia; Brain lesion; Estradiol; Gliosis; Hippocampus

Indexed keywords

AROMATASE; ESTRADIOL; ESTROGEN; KAINIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN INJURY; CELL REGENERATION; FEMALE; GLIOSIS; HIPPOCAMPUS; IMMUNOCOMPETENT CELL; IMMUNOCYTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION;

ANIMALS; AROMATASE; ASTROCYTES; BRAIN; BRAIN DISEASES; BRAIN INJURIES; ESTROGENS; FEMALE; KAINIC ACID; MALE; MICE; MICE, INBRED BALB C; RATS; RATS, WISTAR; WOUND HEALING; WOUNDS, PENETRATING;

EID: 0033103571     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00340-6     Document Type: Article

References (87)

1. 1. Abe-Dohmae S., Tanaka R. and Harada N. (1994) Cell type-and region-specific expression of aromatase mRNA in cultured brain cells. Molec. Brain Res. 24, 153-158.
2. 2. Akwa Y., Sananes N., Gouezou M., Robel P., Baulieu E. E. and Le-Goascogne C. (1993) Astrocytes and neurosteroids: metabolism of pregnenolone and dehydroepiandrosterone. Regulation by cell density. J. Cell Biol. 121, 135-143.
3. 3. Balthazart J., Foidart A., Surlemont C. and Harada N. (1991) Distribution of aromatase-immunoreactive cells in the mouse forebrain. Cell Tiss. Res. 263, 71-79.
4. 4. Baulieu E. E. (1997) Neurosteroids: of the nervous system, by the nervous system, for the nervous system. Rec. Prog. Horm. Res. 52, 1-32.
5. 5. Baulieu E. E., Schumacher M., Koenig H., Jung-Testas I. and Akwa Y. (1996) Progesterone as a neurosteroid: actions within the nervous system. Cell. molec. Neurobiol. 16, 143-154.
6. 6. Behl C., Skutella T., Lezoualc'h F., Post A., Widmann M., Newton C. J. and Holsboer F. (1997) Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Molec. Pharmac. 51, 535-541.
7. 7. Behl C., Widmann M., Trapp T. and Holsboer F. (1997) 17β-estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem. biophys. Res. Commun. 216, 474-482.
8. 8. Ben-Ari Y. (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14, 375-403.
9. 9. Beyer C., Green S. J., Barker P. J., Huskisson N. S. and Hutchison J. B. (1994) Aromatase-immunoreactivity is localized specifically in neurons in the developing mouse hypothalamus and cortex. Brain Res. 638, 203-210.
10. 10. Beyer C., Green S. J. and Hutchison J. B. (1994) Androgens influence sexual differentiation of embryonic hypothalamic aromatase neurons in vitro. Endocrinology 135, 1220-1226.
11. 11. Beyer C. and Hutchison J. B. (1997) Androgens stimulate the morphological maturation of embryonic hypothalamic aromatase-immunoreactive neurons in the mouse. Devl Brain Res. 98, 74-81.
12. 12. Beyer C., Wozniak A. and Hutchison J. B. (1993) Sex-specific aromatization of testosterone in mouse hypothalamic neurons. Neuroendocrinology 58, 673-681.
13. 13. Block J. L., Block N. L. and Lokeshwar B. L. (1996) Modulation of aromatase activity by growth factors in an androgen sensitive human prostate cancer cell line, LNCaP. Cancer Lett. 102, 167-172.
14. 14. Brinton B. D., Proffitt P., Tran J. and Luu R. (1997) Equilin, a principal component of the estrogen replacement therapy premarin, increases the growth of cortical neurons via an NMDA receptor-dependent mechanism. Expl Neurol. 147, 211-220.
15. 15. Chowen J. A., Torres-Aleman I. and Garcia-Segura L. M. (1992) Trophic effects of estradiol on fetal rat hypothalamic neurons. Neuroendocrinology 56, 896-901.
16. 16. Day J. R., Laping N. J., McNeil T. H., Schreiber S. S., Pasinetti G. and Finch C. E. (1990) Castration enhances expression of glial fibrillary acidic protein and sulfated glycoprotein-2 in the intact and lesion-altered hippocampus of the adult male rat. Molec. Endocr. 4, 1995-2002.
17. 17. Del Cerro S., Garcia-Estrada J. and Garcia-Segura L. M. (1995) Neuroactive steroids regulate astroglia morphology in hippocampal cultures from adult rats. Glia 14. 65-71.
18. 18. Del Cerro S., Garcia-Estrada J. and Garcia-Segura L. M. (1996) Neurosteroids modulate the reaction of astroglia to high extracellular potassium levels. Glia 18, 293-305.
19. 19. Dueñas M., Torres-Aleman I., Naftolin F. and Garcia-Segura L. M. (1996) Interaction of insulin-like growth factor-I and estradiol signaling pathways on hypothalamic neuronal differentiation. Neuroscience 74, 531-539.
20. 20. Eddleston M. and Mucke L. (1993) Molecular profile of reactive astrocytes: implications for their role in neurologic disease. Neuroscience 54, 15-36.
21. 21. Eng L. F., Yu A. C. H. and Lee Y. L. (1992) Astrocytic response to injury. Prog. Brain Res. 94, 353-365.
22. 22. Fillit H. (1994) Observations in a preliminary open trial of estradiol therapy for senile dementia - Alzheimer's type. Ann. N. Y. Acad. Sci. 743, 233-239.
23. 23. Foidart A., Harada N. and Balthazart J. (1995) Aromatase-immunoreactive cells are present in mouse brain areas that are known to express high levels of aromatase activity. Cell Tiss. Res. 280, 561-574.
24. 24. Garcia-Estrada J., del Rio J. A., Luquin S., Soriano E. and Garcia-Segura L. M. (1993) Gonadal hormones down-regulate reactive gliosis and astrocyte proliferation after a penetrating brain injury. Brain Res. 628, 271-278.
25. 25. Garcia-Segura L. M., Cardona-Gomez P., Naftolin F. and Chowen J. A. (1998) Estradiol upregulates Bcl-2 expression in adult brain neurons. NeuroReport 9, 593-597.
26. 26. Garcia-Segura L. M., Chowen J. A., Duenas M., Parducz A. and Naftolin F. (1996) Gonadal steroids and astroglial plasticity. Cell. molec. Neurobiol. 16, 225-237.
27. 27. Garcia-Segura L. M., Chowen J. A. and Naftolin F. (1996) Endocrine glia: roles of glial cells in the brain actions of steroid and thyroid hormones and in the regulation of hormone secretion. Front. Neuroendocr. 17, 180-211.
28. 28. Giulian D. (1993) Reactive glia as rivals in regulating neuronal survival. Glia 7, 102-110.
29. 29. Henderson V. W., Paganini-Hill A., Emanuel C. K., Dunn M. E. and Buckwalter G. (1994) Estrogen replacement therapy in older women. Archs Neurol. 51, 896-900.
30. 30. Honjo H., Ogino Y., Naitoh K., Urabe M., Kitawaki J., Yasuda J., Yamamoto T., Ishihara S., Okada H., Yonezawa T., Hayashi K. and Nambara T. (1989) In vivo effects by estrone sulfate on the central nervous system senile dementia (Alzheimer's type). J. Steroid Biochem. 34, 521-525.
31. 31. Hutchison J. B. (1991) Hormonal control of behaviour: steroid action in the brain. Curr. Opin. Neurobiol. 1, 562-570.
32. 32. Hutchison J. B., Beyer C., Hutchison R. E. and Wozniak A. (1995) Sexual dimorphism in the developmental regulation of brain aromatase. J. Steroid Biochem. molec. Biol. 53, 307-313.
33. 33. Hutchison J. B., Wozniak A., Beyer C. and Hutchison R. E. (1996) Regulation of sex specific formation of oestrogen in brain development: endogenous inhibitors of aromatase. J. Steroid Biochem. molec. Biol. 56, 201-207.
34. 34. Jakab R. L., Harada N. and Naftolin F. (1994) Aromatase-(estrogen synthetase) immunoreactive neurons in the rat septal area. A light and electron microscopic study. Brain Res. 664, 85-93.
35. 35. Jakab R. L., Horvath T. L., Leranth C., Harada N. and Naftolin F. (1993) Aromatase immunoreactivity in the rat brain: gonadectomy-sensitive hypothalamic neurons and an unresponsive "limbic ring" of the lateral septum-bed nucleus-amygdala complex. J. Steroid Biochem. molec. Biol. 44, 481-498.
36. 36. Jolkkonen J., Jolkkonen E. and Pitkänen A. (1997) Seizure-induced damage to somatostatin-immunoreactive neurons in the rat hippocampus is regulated by fimbria-fornix transection. Expl Neurol. 145, 141-153.
37. 37. Jones K. J. (1993) Gonadal steroids as promoting factors in axonal regeneration. Brain Res. Bull. 30, 491-498.
38. 38. Jones K. J. (1993) Gonadal steroids and neuronal regeneration. A therapeutic role. Adv. Neurol. 59, 227-240.
39. 39. Jones K. J. (1994) Androgenic enhancement of motor neuron regeneration. Ann. N. Y. Acad. Sci. 743, 141-161.
40. 40. Jones K. J., Durica T. E. and Jacob S. K. (1997) Gonadal steroid preservation of central synaptic input to hamster facial motoneurons following peripheral axotomy. J. Neurocytol. 26, 257-266.
41. +-ATPase activity, glucose transport, and glutamine transport induced by amyloid β-peptide and iron. J. Neurosci. Res. 50, 522-530.
42. 42. Koenig H. L., Schumacher M., Ferzaz B., Thi A. N., Ressouches A., Guennoun R., Jung-Testas I., Robel P., Akwa Y. and Baulieu E. E. (1995) Progesterone synthesis and myelin formation by Schwann cells. Science 268, 1500-1503.
43. A receptor function. Trends pharmac. Sci. 16, 295-303.
44. 44. Lephart E. D. (1996) A review of brain aromatase cytochrome P450. Brain Res. Rev. 22, 1-26.
45. 45. MacLusky N. J. and Naftolin F. (1981) Sexual differentiation of the central nervous system. Science 211, 1294-1302.
46. A receptor. Mechanism of action and physiological significance. Prog. Neurobiol. 38, 379-395.
47. 47. Martini L., Melcangi R. C. and Maggi R. (1993) Androgen and progesterone metabolism in the central and peripheral nervous system. J. Steroid Biochem. molec. Biol. 47, 195-205.
48. 48. McMillan P. J., Singer C. A. and Dorsa D. M. (1996) The effect of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat. J. Neurosci. 16, 1860-1865.
49. 49. Miller W. R. and Mullen P. (1993) Factors influencing aromatase activity in the breast. J. Steroid Biochem. molec. Biol. 44, 597-604.
50. 50. Mook-Jung I., Joo I., Sohn S., Kwon H. J., Huh K. and Jung M. W. (1997) Estrogen blocks neurotoxic effects of β-amyloid (1-42) and induces neurite extension on B103 cells. Neurosci. Lett. 235, 101-104.
51. 51. Naftolin F., Horvath T. L., Jakab R. L., Leranth C., Harada N. and Balthazart J. (1996) Aromatase immunoreactivity in axon terminals of the vertebrate brain. An immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology 63, 149-155.
52. 52. Naftolin F., Ryan K. J. and Petro Z. (1971) Aromatization of androstendione by the diencephalon. J. clin. Endocr. Metab. 33, 368-370.
53. 53. Naftolin F., Ryan K. J. and Petro Z. (1971) Aromatization of androstendione by limbic system tissue from human foetuses. J. Endocr. 51, 795-796.
54. 54. Negri-Cesi P., Melcangi R. C., Celotti F. and Martini L. (1992) Aromatase activity in cultured brain cells: differences between neurons and glia. Brain Res. 589, 327-332.
55. 55. Nestler J. E. (1993) Regulation of aromatase activity of human placental cytotrophoblasts by insulin, insulin-like growth factor-I and -II. J. Steroid Biochem. molec. Biol. 44, 449-457.
56. 56. Ohkura T., Isse K., Akazawa K., Hamamoto M., Yaoi Y. and Hagino N. (1994) Evaluation of estrogen treatment in female patients with dementia of the Alzheimer type. Endocr. J. 41, 361-371.
57. 57. Paganini-Hill A. and Henderson V. W. (1994) Estrogen deficiency and risk of AD in women. Am. J. Epidemiol. 140, 256-261.
58. 58. Poletti A., Negri-Cesi P., Melcangi R. C., Colciago A., Martini L. and Celotti F. (1997) Expression of androgen-activating enzymes in cultured cells of developing rat brain. J. Neurochem. 68, 1298-1303.
59. 59. Rabbani O., Panickar K. S., Rajakumar G., King M. A., Bodor N., Meyer E. M. and Simpkins J. W. (1997) 17α-estradiol attenuates fimbrial lesion-induced decline of ChAT-immunoreactive neurons in the rat medial septum. Expl Neurol. 146, 179-186.
60. 60. Reed M. J., Topping L., Coldham N. G., Purchit A., Ghilchik M. W. and James V. H. (1993) Control of aromatase activity in breast cancer cells: the role of cytokines and growth factors. J. Steroid Biochem. molec. Biol. 44, 589-596.
61. 61. Ridet J. L., Malhotra S. K., Privat A. and Gage F. H. (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20, 570-577.
62. 62. Robel P. and Baulieu E. E. (1995) Neurosteroids: biosynthesis and function. Crit. Rev. Neurobiol. 9, 383-394.
63. 63. Sanghera M. K., Simpson E. R., McPhaul M. J., Kozlowski G., Conley A. J. and Lephart E. D. (1991) Immunocytochemical distribution of aromatase cytochrome P450 in the rat brain using peptide-generated polyclonal antibodies. Endocrinology 129, 2834-2844.
64. 64. Schauwecker P. E. and Steward O. (1997) Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. natn. Acad. Sci. U.S.A. 94, 4103-4108.
65. 65. Schlinger B. A., Amur-Umarjee S., Campagnoni A. T. and Arnold A. P. (1995) 5 beta-reductase and other androgen-metabolizing enzymes in primary cultures of developing zebra finch telencephalon. J. Neuroendocr. 7, 187-192.
66. 66. Schlinger B. A., Amur-Umarjee S., Shen P., Campagnoni A. T. and Arnold A. P. (1994) Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon. J. Neurosci. 14, 7541-7552.
67. 67. Schneider L. S., Farlow M. R., Henderson V. W. and Pogoda J. M. (1996) Effects of estrogen replacement therapy on response to tacrine in patients with Alzheimer's disease. Neurology 46, 1580-1584.
68. 68. Schumacher M. and Baulieu E. E. (1995) Neurosteroids: synthesis and functions in the central and peripheral nervous systems. Ciba Found. Symp. 191, 90-106.
69. 69. Schwob J. E., Fuller T., Price J. L. and Olney J. W. (1980) Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience 5, 991-1014.
70. 70. Shinoda K., Nagano M. and Osawa Y. (1994) Neuronal aromatase expression in preoptic, strial, and amygdaloid regions during late prenatal and early postnatal development in the rat. J. comp. Neurol. 343, 113-129.
71. 2). J. comp. Neurol. 290, 502-515.
72. 72. Shinoda K., Yagi H., Fujita H., Osawa Y. and Shiotani Y. (1989) Involvement of specific placental antigen X-P2 in rat olfaction: an immunohistochemical study in the olfactory bulb. J. comp. Neurol. 294, 340-344.
73. 73. Simpson I. A. and Sonne O. (1982) A simple, rapid and sensitive method for measuring protein concentration in subcellular membrane fractions prepared by sucrose density gradient ultracentrifugation. Analyt. Biochem. 119, 424-427.
74. 74. Singh M., Meyer E. M. and Simpkins J. W. (1995) The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology 136, 2320-2324.
75. 75. Sohrabji F., Greene L. A., Miranda R. C. and Toran-Allerand C. D. (1994) Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. J. Neurobiol. 25, 974-988.
76. 76. Sohrabji F., Miranda R. C. and Toran-Allerand C. D. (1994) Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J. Neurosci. 14, 459-471.
77. 77. Sperk G. (1994) Kainic acid seizures in the rat. Prog. Neurobiol. 42, 1-32.
78. 78. Steimer T. H. and Hutchison J. B. (1989) Is the androgen-dependent increase in preoptic estradiol-17β formation due ro aromatase induction? Brain Res. 480, 335-339.
79. 79. Stone D. J., Rozovsky I., Morgan T. E., Anderson C. P., Hajian H. and Finch C. E. (1997) Astrocytes and microglia respond to estrogen with increased apoE mRNA in vivo and in vitro.. Expl Neurol. 143, 313-318.
80. 80. Tang M. X., Jacobs D., Stern Y., Marder K., Schofield P., Gurland B., Andrews H. and Mayeux R. (1996) Effect of estrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 348, 429-432.
81. 81. Tanzer L. and Jones K. J. (1997) Gonadal steroid regulation of hamster facial nerve regeneration: effects of dihydrotestosterone and estradiol. Expl Neurol. 146, 258-264.
82. 82. Toran-Allerand C. D. (1984) On the genesis of sexual differentiation of the central nervous system. Morphogenetic consequences of steroidal exposure and possible role of α-fetoprotein. Prog. Brain Res. 61, 63-98.
83. 83. Toran-Allerand C. D., Miranda R. C., Bentham W. D., Sohrabji F., Brown T. J., Hochberg R. B. and MacLusky N. J. (1992) Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of adult rat forebrain. Proc. natn. Acad. Sci. U.S.A. 89, 4668-4672.
84. 84. Tsuro Y., Ishimura K., Fujita H. and Osawa Y. (1994) Immunocytochemical localization of aromatase-containing neurons in the rat brain during pre- and postnatal development. Cell Tiss. Res. 278, 29-39.
85. 85. Weaver C. E., Park-Chung M., Gibbs T. T. and Farb D. H. (1997) 17β-Estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptor. Brain Res. 761, 338-341.
86. 86. Wozniak A., Hutchison R. E. and Hutchison J. B. (1992) Localization of aromatase activity in androgen target areas of the mouse brain. Neurosci. Lett. 146, 191-194.
87. 87. Zwain I. H., Yen S. S. C. and Cheng C. Y. (1997) Astrocytes cultured in vitro produce estradiol-17β and express aromatase cytochrome P-450 (P-450 AROM) mRNA. Biochim. biophys. Acta 1334, 338-348.