Molecular characterization of the injury-induced aromatase transcript in the adult zebra finch brain

Journal of Neurochemistry

Volumn 105, Issue 5, 2008, Pages 1613-1624

  Wynne, Ryan D ^a   Maas, Stefan ^a   Saldanha, Colin J ^a  

^a LEHIGH UNIVERSITY   (United States)

Author keywords

Apoptosis; Estrogen; Glia; Neuron; Neuroprotection; Stroke

Indexed keywords

AROMATASE;

ANIMAL TISSUE; ARTICLE; BRAIN INJURY; FINCH; GENE AMPLIFICATION; GENE SEQUENCE; GENE SILENCING; GENETIC TRANSCRIPTION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

AGE FACTORS; ANIMALS; AROMATASE; BASE SEQUENCE; BRAIN INJURIES; FEMALE; FINCHES; MALE; MOLECULAR SEQUENCE DATA; OVARY; SONGBIRDS; TRANSCRIPTION, GENETIC; UP-REGULATION;

TAENIOPYGIA GUTTATA; VERTEBRATA;

EID: 43549096157     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05256.x     Document Type: Article

References (80)

1. Arnold A. P. Gorski R. A. (1984) Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 7, 413 442.
2. Azcoitia I., Sierra A., Veiga S., Honda S., Harada N. Garcia-Segura L. M. (2001) Brain aromatase is neuroprotective. J. Neurobiol. 47, 318 329.
3. Azcoitia I., Sierra A., Veiga S. Garcia-Segura L. M. (2003) Aromatase expression by reactive astroglia is neuroprotective. Ann N Y Acad Sci 1007, 298 305.
4. Balthazart J., Foidart A. Harada N. (1990) Immunocytochemical localization of aromatase in the brain. Brain Res. 514, 327 333.
5. Balthazart J., De Clerck A. Foidart A. (1992) Behavioral demasculinization of female quail is induced by estrogens: studies with the new aromatase inhibitor, R76713. Horm. Behav. 26, 179 203.
6. Balthazart J., Foidart A., Absil P. Harada N. (1996) Effects of testosterone and its metabolites on aromatase-immunoreactive cells in the quail brain: relationship with the activation of male reproductive behavior. J. Steroid Biochem. Mol. Biol. 56, 185 200.
7. Bouraima H., Hanoux V., Mittre H., Feral C., Benhaim A. Leymarie P. (2001) Expression of the rabbit cytochrome P450 aromatase encoding gene uses alternative tissue-specific promoters. Eur. J. Biochem. 268, 4506 4512.
8. Carreau S., Bourguiba S., Lambard S., Silandre D. Delalande C. (2004) The promoter(s) of the aromatase gene in male testicular cells. Reprod. Biol. 4, 23 34.
9. Cho J. J., Iannucci F. A., Fraile M., Franco J., Alesius T. N. Stefano G. B. (2003) The role of the estrogen in neuroprotection: implications for neurodegenerative diseases. Neuro Endocrinol Lett 24, 141 147.
10. DeVoogd T. J. (1986) Steroid interactions with structure and function of avian song control regions. J. Neurobiol. 17, 177 201.
11. DeVoogd T. Nottebohm F. (1981) Gonadal hormones induce dendritic growth in the adult avian brain. Science 214, 202 204.
12. Dohler K. D., Coquelin A., Davis F., Hines M., Shryne J. E. Gorski R. A. (1982) Differentiation of the sexually dimorphic nucleus in the preoptic area of the rat brain is determined by the perinatal hormone environment. Neurosci. Lett. 33, 295 298.
13. Dominguez R., Jalali C. de Lacalle S. (2004) Morphological effects of estrogen on cholinergic neurons in vitro involves activation of extracellular signal-regulated kinases. J. Neurosci. 24, 982 990.
14. Foidart A., Silverin B., Baillien M., Harada N. Balthazart J. (1998) Neuroanatomical distribution and variations across the reproductive cycle of aromatase activity and aromatase-immunoreactive cells in the pied flycatcher (Ficedula hypoleuca). Horm. Behav. 33, 180 196.
15. Furbass R., Kalbe C. Vanselow J. (1997) Tissue-specific expression of the bovine aromatase-encoding gene uses multiple transcriptional start sites and alternative first exons. Endocrinology 138, 2813 2819.
16. Garcia-Segura L. M., Wozniak A., Azcoitia I., Rodriguez J. R., Hutchison R. E. Hutchison J. B. (1999) Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair. Neuroscience 89, 567 578.
17. Garcia-Segura L. M., Azcoitia I. DonCarlos L. L. (2001) Neuroprotection by estradiol. Prog. Neurobiol. 63, 29 60.
18. Garcia-Segura L. M., Veiga S., Sierra A., Melcangi R. C. Azcoitia I. (2003) Aromatase: A neuroprotective enzyme. Prog. Neurobiol. 71, 31 41.
19. Golovine K., Schwerin M. Vanselow J. (2003) Three different promoters control expression of the aromatase cytochrome p450 gene (cyp19) in mouse gonads and brain. Biol. Reprod. 68, 978 984.
20. Goodson J. L., Saldanha C. J., Hahn T. P. Soma K. K. (2005) Recent advances in behavioral neuroendocrinology: insights from studies on birds. Horm. Behav. 48, 461 473.
21. Gould E., Allan M. D. McEwen B. S. (1990) Dendritic spine density of adult hippocampal pyramidal cells is sensitive to thyroid hormone. Brain Res. 525, 327 329.
22. Graddy L. G., Kowalski A. A., Simmen F. A., Davis S. L., Baumgartner W. W. Simmen R. C. (2000) Multiple isoforms of porcine aromatase are encoded by three distinct genes. J. Steroid Biochem. Mol. Biol. 73, 49 57.
23. Gurney M. E. Konishi M. (1980) Hormone-Induced Sexual Differentiation of Brain and Behavior in Zebra Finches. Science 208, 1380 1383.
24. Harada N. (1993) [Estrogen synthetase (P-450. aromatase) as a regulatory factor concerning sexual differentiation of brain and sexual behavior - physiological functions and regulation of gene expression of aromatase]. Seikagaku 65, 67 85.
25. Harding C. F. (1986) The importance of androgen metabolism in the regulation of reproductive behavior in the avian male. Poult. Sci. 65, 2344 2351.
26. Harding C. F., Walters M. J., Collado D. Sheridan K. (1988) Hormonal specificity and activation of social behavior in male red-winged blackbirds. Horm. Behav. 22, 402 418.
27. Honda S., Harada N. Takagi Y. (1996) The alternative exons 1 of the mouse aromatase cytochrome P-450 gene. Biochim. Biophys. Acta 1305, 145 150.
28. Hutchison J. B. Schumacher M. (1986) Development of testosterone- metabolizing pathways in the avian brain: enzyme localization and characteristics. Brain Res. 390, 33 42.
29. Jacobs E. C., Arnold A. P. Campagnoni A. T. (1999) Developmental regulation of the distribution of aromatase- and estrogen-receptor- mRNA-expressing cells in the zebra finch brain. Dev. Neurosci. 21, 453 472.
30. Jin T., Zhang X., Li H. Goss P. E. (2000) Characterization of a novel silencer element in the human aromatase gene PII promoter. Breast Cancer Res. Treat. 62, 151 159.
31. Kamat A., Hinshelwood M. M., Murry B. A. Mendelson C. R. (2002) Mechanisms in tissue-specific regulation of estrogen biosynthesis in humans. Trends Endocrinol Metab 13, 122 128.
32. Kishida M. Callard G. V. (2001) Distinct cytochrome P450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinology 142, 740 750.
33. Leranth C., Shanabrough M. Horvath T. L. (2000) Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience 101, 349 356.
34. Leranth C., Shanabrough M. Redmond DE. Jr. (2002) Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J. Comp. Neurol. 447, 34 42.
35. MacLusky N. J. Naftolin F. (1981) Sexual differentiation of the central nervous system. Science 211, 1294 1302.
36. Maggi A., Ciana P., Belcredito S. Vegeto E. (2004) Estrogens in the nervous system: mechanisms and nonreproductive functions. Annu. Rev. Physiol. 66, 291 313.
37. McEwen B. S. (2001) Invited review: Estrogens effects on the brain: multiple sites and molecular mechanisms. J. Appl. Physiol. 91, 2785 2801.
38. Merchenthaler I., Dellovade T. L. Shughrue P. J. (2003) Neuroprotection by estrogen in animal models of global and focal ischemia. Ann N Y Acad Sci 1007, 89 100.
39. Negri Cesi P., Melcangi R. C., Celotti F. Martini L. (1992) Aromatase activity in cultured brain cells: difference between neurons and glia. Brain Res. 589, 327 332.
40. Ottinger M. A., Adkins-Regan E., Buntin J., Cheng M. F., DeVoogd T., Harding C. Opel H. (1984) Hormonal mediation of reproductive behavior. J. Exp. Zool. 232, 605 616.
41. Perlman W. R. Arnold A. P. (2003) Expression of estrogen receptor and aromatase mRNAs in embryonic and posthatch zebra finch brain. J. Neurobiol. 55, 204 219.
42. Peterson R. S., Saldanha C. J. Schlinger B. A. (2001) Rapid upregulation of aromatase mRNA and protein following neural injury in the zebra finch (Taeniopygia guttata). J. Neuroendocrinol. 13, 317 323.
43. Peterson R. S., Lee D. W., Fernando G. Schlinger B. A. (2004) Radial glia express aromatase in the injured zebra finch brain. J. Comp. Neurol. 475, 261 269.
44. Ramachandran B., Schlinger B. A., Arnold A. P. Campagnoni A. T. (1999) Zebra finch aromatase gene expression is regulated in the brain through an alternate promoter. Gene 240, 209 216.
45. Rau S. W., Dubal D. B., Bottner M., Gerhold L. M. Wise P. M. (2003a) Estradiol attenuates programmed cell death after stroke-like injury. J. Neurosci. 23, 11420 11426.
46. Rau S. W., Dubal D. B., Bottner M. Wise P. M. (2003b) Estradiol differentially regulates c-Fos after focal cerebral ischemia. J. Neurosci. 23, 10487 10494.
47. Riters L. V., Eens M., Pinxten R., Duffy D. L., Balthazart J. Ball G. F. (2000) Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm. Behav. 38, 250 261.
48. Riters L. V., Baillien M., Eens M., Pinxten R., Foidart A., Ball G. F. Balthazart J. (2001) Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J. Neuroendocrinol. 13, 985 997.
49. Saldanha C. J., Tuerk M. J., Kim Y. H., Fernandes A. O., Arnold A. P. Schlinger B. A. (2000) Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J. Comp. Neurol. 423, 619 630.
50. Saldanha C. J., Schlinger B. A., Micevych P. E. Horvath T. L. (2004) Presynaptic N-methyl-D-aspartate receptor expression is increased by estrogen in an aromatase-rich area of the songbird hippocampus. J. Comp. Neurol. 469, 522 534.
51. Saldanha C. J., Rohmann K. N., Coomaralingam L. Wynne R. D. (2005) Estrogen provision by reactive glia decreases apoptosis in the zebra finch (Taeniopygia guttata). J. Neurobiol. 64, 192 201.
52. Schlinger B. A. (1997) The activity and expression of aromatase in songbirds. Brain Res. Bull. 44, 359 364.
53. Schlinger B. A. Arnold A. P. (1991) Brain is the major site of estrogen synthesis in a male songbird. Proc. Natl Acad. Sci. USA 88, 4191 4194.
54. Schlinger B. A. Arnold A. P. (1992) Circulating estrogens in a male songbird originate in the brain. Proc. Natl Acad. Sci. USA 89, 7650 7653.
55. Schlinger B. A., Amur-Umarjee S., Shen P., Campagnoni A. T. Arnold A. P. (1994) Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon. J. Neurosci. 14, 7541 7552.
56. Sharp P. J., Armstrong D. G. Moss R. (1986) Changes in aromatase activity in the neuroendocrine tissues of red grouse (Lagopus lagopus scoticus) in relation to the development of long-day refractoriness. J. Endocrinol. 108, 129 135.
57. Shen P., Campagnoni C. W., Kampf K., Schlinger B. A., Arnold A. P. Campagnoni A. T. (1994) Isolation and characterization of a zebra finch aromatase cDNA: in situ hybridization reveals high aromatase expression in brain. Brain Res. Mol. Brain Res. 24, 227 237.
58. Shen P., Schlinger B. A., Campagnoni A. T. Arnold A. P. (1995) An atlas of aromatase mRNA expression in the zebra finch brain. J. Comp. Neurol. 360, 172 184.
59. Shinoda K. (1994) Brain aromatization and its associated structures. Endocr. J. 41, 115 138.
60. Simpson E. R., Mahendroo M. S., Means G. D., Kilgore M. W., Corbin C. J. Mendelson C. R. (1993) Tissue-specific promoters regulate aromatase cytochrome P450 expression. J. Steroid Biochem. Mol. Biol. 44, 321 330.
61. Simpson E. R., Mahendroo M. S., Means G. D. et al. (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr. Rev. 15, 342 355.
62. Soma K. K., Bindra R. K., Gee J., Wingfield J. C. Schlinger B. A. (1999) Androgen-metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild songbird. J. Neurobiol. 41, 176 188.
63. Soma K. K., Schlinger B. A., Wingfield J. C. Saldanha C. J. (2003) Brain aromatase, 5 alpha-reductase, and 5 beta-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior. J. Neurobiol. 56, 209 221.
64. Stokes T. M., Leonard C. M. Nottebohm F. (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol. 156, 337 374.
65. Suzuki S., Brown C. M. Wise P. M. (2006) Mechanisms of neuroprotection by estrogen. Endocrine 29, 209 215.
66. Tchoudakova A. Callard G. V. (1998) Identification of multiple CYP19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary. Endocrinology 139, 2179 2189.
67. Vanselow J., Zsolnai A., Fesus L., Furbass R. Schwerin M. (1999) Placenta-specific transcripts of the aromatase encoding gene include different untranslated first exons in sheep and cattle. Eur. J. Biochem. 265, 318 324.
68. Vanselow J., Furbass R., Zsolnai A., Kalbe C., Said H. M. Schwerin M. (2001) Expression of the aromatase cytochrome P450 encoding gene in cattle and sheep. J. Steroid Biochem. Mol. Biol. 79, 279 288.
69. Wang J. Chen S. (1992) Identification of a promoter and a silencer at the 3′-end of the first intron of the human aromatase gene. Mol. Endocrinol. 6, 1479 1488.
70. Wise P. M. (2002) Estrogens and neuroprotection. Trends Endocrinol Metab 13, 229 230.
71. Wise P. M., Dubal D. B., Rau S. W., Brown C. M. Suzuki S. (2005) Are estrogens protective or risk factors in brain injury and neurodegeneration? Reevaluation after the Women's health initiative Endocr. Rev. 26, 308 312.
72. Wynne R. D. Saldanha C. J. (2004) Glial aromatization decreases neural injury in the zebra finch (Taeniopygia guttata): influence on apoptosis. J. Neuroendocrinol. 16, 676 683.
73. Wynne R. D., Walters B. J., Bailey D. J. Saldanha C. J. (2008) Inhibition of injury-induced glial aromatase reveals a wave of secondary degeneration in the songbird brain. Glia 56, 97 105.
74. Yague J. G., Lavaque E., Carretero J., Azcoitia I. Garcia-Segura L. M. (2004) Aromatase, the enzyme responsible for estrogen biosynthesis, is expressed by human and rat glioblastomas. Neurosci. Lett. 368, 279 284.
75. Yague J. G., Munoz A., de Monasterio-Schrader P., Defelipe J., Garcia-Segura L. M. Azcoitia I. (2006) Aromatase expression in the human temporal cortex. Neuroscience 138, 389 401.
76. Yamada K., Harada N., Honda S. Takagi Y. (1995) Regulation of placenta-specific expression of the aromatase cytochrome P-450 gene. Involvement of the trophoblast-specific element binding protein. J. Biol. Chem. 270, 25064 25069.
77. Yamada-Mouri N., Hirata S. Kato J. (1996) Existence and expression of the untranslated first exon of aromatase mRNA in the rat brain. J. Steroid Biochem. Mol. Biol. 58, 163 166.
78. Zhao C., Fujinaga R., Tanaka M., Yanai A., Nakahama K. Shinoda K. (2007) Region-specific expression and sex-steroidal regulation on aromatase and its mRNA in the male rat brain: immunohistochemical and in situ hybridization analyses. J. Comp. Neurol. 500, 557 573.
79. Zhou D. Chen S. (1998) Characterization of a silencer element in the human aromatase gene. Arch. Biochem. Biophys. 353, 213 220.
80. Zwain I. H. Yen S. S. (1999) Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140, 3843 3852.