Neural expression and post-transcriptional dosage compensation of the steroid metabolic enzyme 17β-HSD type 4
详细信息    查看全文
  • 作者:Sarah E London (1) (2) (3) (5)
    Yuichiro Itoh (2) (3)
    Valentin A Lance (2)
    Petra M Wise (2)
    Preethika S Ekanayake (2)
    Randi K Oyama (2)
    Arthur P Arnold (1) (2) (3)
    Barney A Schlinger (1) (2) (3) (4)
  • 刊名:BMC Neuroscience
  • 出版年:2010
  • 出版时间:December 2010
  • 年:2010
  • 卷:11
  • 期:1
  • 全文大小:2254KB
  • 参考文献:1. Nottebohm F, Arnold AP: Sexual dimorphism in vocal control areas of the songbird brain. / Science 1976, 194:211-13. CrossRef
    2. Peterson RS, Yarram L, Schlinger BA, Saldanha CJ: Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. / Proc Royal Society B: Biol Sci 2005, 272:2089-096. CrossRef
    3. Remage-Healey L, Maidment NT, Schlinger BA: Forebrain steroid levels fluctuate rapidly during social interactions. / Nat Neurosci 2008, 11:1327-334. CrossRef
    4. Remage-Healey L, Oyama RK, Schlinger BA: Elevated aromatase activity in forebrain synaptic terminals during song. / J Neuroendocrinol 2009, 21:191-99. CrossRef
    5. Rohmann KN, Schlinger BA, Saldanha CJ: Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. / Dev Neurobiol 2007, 67:1-. CrossRef
    6. London SE, Boulter J, Schlinger BA: Cloning of the zebra finch androgen synthetic enzyme CYP17: a study of its neural expression throughout posthatch development. / J Comp Neurol 2003, 467:496-08. CrossRef
    7. London SE, Monks DA, Wade J, Schlinger BA: Widespread capacity for steroid synthesis in the avian brain and song system. / Endocrinol 2006, 147:5975-987. CrossRef
    8. Holloway CC, Clayton DF: Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. / Nat Neurosci 2001, 4:170-75. CrossRef
    9. Grisham W, Mathews GA, Arnold AP: Local intracerebral implants of estrogen masculinize some aspects of the zebra finch song system. / J Neurobiol 1994, 25:185-96. CrossRef
    10. Jacobs EC, Arnold AP, Campagnoni AT: Developmental regulation of the distribution of aromatase- and estrogen-receptor-mRNA-expressing cells in the zebra finch brain. / Dev Neurosci 2000, 21:453-72. CrossRef
    11. London SE, Schlinger BA: Steroidogenic enzymes along the ventricular proliferative zone in the developing songbird brain. / J Comp Neurol 2007, 502:507-21. CrossRef
    12. London SE, Remage-Healey L, Schlinger BA: Neurosteroid production in the songbird brain: A re-evaluation of core principles. / Front Neuroendocrinol 2009, 30:302-14. CrossRef
    13. Remage-Healey L, London SE, Schlinger BA: Birdsong and the neural production of steroids. / J Chem Neuroanatomy 2010, 39:72-1. CrossRef
    14. Saldanha CJ, Tuerk MJ, Kim YH, Fernandes AO, Arnold AP, Schlinger BA: Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. / J Comp Neurol 2000, 423:619-30. CrossRef
    15. Schlinger BA, Arnold AP: Brain is the major site of estrogen synthesis in a male songbird. / Proc Natl Acad Sci USA 1991, 88:4191-194. CrossRef
    16. Schlinger BA, Arnold AP: Circulating estrogens in a male songbird originate in the brain. / Proc Natl Acad Sci USA 1992, 89:7650-653. CrossRef
    17. Schlinger BA, Soma KK, London SE: Neurosteroids and brain sexual differentiation. / Trends Neurosci 2001, 24:429-31. CrossRef
    18. Shen P, Campagnoni CW, Kampf K, Schlinger BA, Arnold AP, Campagnoni AT: Isolation and characterization of a zebra finch aromatase cDNA: In situ hybridization reveals high aromatase expression in brain. / Mol Brain Res 1994, 24:227-37. CrossRef
    19. Tam H, Schlinger BA: Activities of 3beta-HSD and aromatase in slices of developing and adult zebra finch brain. / Gen Comp Endocrinol 2007, 150:26-3. CrossRef
    20. Gong A, Freking FW, Wingfield J, Schlinger BA, Arnold AP: Effects of embryonic treatment with fadrozole on phenotype of gonads, syrinx, and neural song system in zebra finches. / Gen Comp Endocrinol 1999, 115:346-53. CrossRef
    21. Wade J, Springer ML, Wingfield JC, Arnold AP: Neither testicular androgens nor embryonic aromatase activity alters morphology of the neural song system in zebra finches. / Biol Reproduction 1996, 55:1126-132. CrossRef
    22. Wade J, Arnold AP: Functional testicular tissue does not masculinize development of the zebra finch song system. / Proc Natl Acad Sci USA 1996, 93:5264-268. CrossRef
    23. Wade J, Swender DA, McElhinny TL: Sexual differentiation of the zebra finch song system parallels genetic, not gonadal, sex. / Horm Behav 1999, 36:141-52. CrossRef
    24. Wade J, Arnold AP: Sexual differentiation of the zebra finch song system. / Ann N Y Aca Sci 2004, 1016:540-59. CrossRef
    25. Agate RJ, Grisham W, Wade J, Mann S, Wingfield J, Schanen C, Palotie A, Arnold AP: Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. / Proc Natl Acad Sci USA 2003, 100:4873-878. CrossRef
    26. Grisham W, Tam A, Greco CM, Schlinger BA, Arnold AP: A putative 5 alpha-reductase inhibitor demasculinizes portions of the zebra finch song system. / Brain Research 1997, 750:122-28. CrossRef
    27. Grisham W, Lee J, McCormick ME, Yang-Stayner K, Arnold AP: Antiandrogen blocks estrogen-induced masculinization of the song system in female zebra finches. / J Neurobiol 2002, 51:1-. CrossRef
    28. Mathews GA, Arnold AP: Antiestrogens fail to prevent the masculine ontogeny of the zebra finch song system. / Gen Comp Endocrinol 1990, 80:48-8. CrossRef
    29. Arnold AP: Sex chromosomes and brain gender. / Nat Rev Neurosci 2004, 5:701-08. CrossRef
    30. Chen X, Agate RJ, Itoh Y, Arnold AP: Sexually dimorphic expression of trkB, a Z-linked gene, in early posthatch zebra finch brain. / Proc Natl Acad Sci USA 2005, 102:7730-735. CrossRef
    31. Cam V, Schlinger BA: Activities of aromatase and 3beta-hydroxysteroid dehydrogenase/delta4-delta5 isomerase in whole organ cultures of tissues from developing zebra finches. / Horm Behav 1998, 33:31-9. CrossRef
    32. Jacobs EC, Arnold AP, Campagnoni AT: Zebra finch estrogen receptor cDNA: cloning and mRNA expression. / J Steroid Biochem and Mol Biol 1996, 59:135-45. CrossRef
    33. Kim YH, Perlman WR, Arnold AP: Expression of androgen receptor mRNA in zebra finch song system: developmental regulation by estrogen. / J Comp Neurol 2004, 469:535-47. CrossRef
    34. Perlman WR, Arnold AP: Expression of estrogen receptor and aromatase mRNAs in embryonic and posthatch zebra finch brain. / J Neurobiol 2003, 55:204-19. CrossRef
    35. Perlman WR, Ramachandran B, Arnold AP: Expression of androgen receptor mRNA in the late embryonic and early posthatch zebra finch brain. / J Comp Neurol 2003, 455:513-30. CrossRef
    36. Schlinger BA, Amur-Umarjee S, Campagnoni AT, Arnold AP: 5 beta-reductase and other androgen-metabolizing enzymes in primary cultures of developing zebra finch telencephalon. / J Neuroendocrinol 1995, 7:187-92. CrossRef
    37. Wade J, Schlinger BA, Arnold AP: Aromatase and 5 beta-reductase activity in cultures of developing zebra finch brain: an investigation of sex and regional differences. / J Neurobiol 1995, 27:240-51. CrossRef
    38. Adkins-Regan E, Mansukhani V, Seiwert C, Thompson R: Sexual differentiation of brain and behavior in the zebra finch: Critical periods for effects of early estrogen treatment. / J Neurobiol 1994, 25:865-77. CrossRef
    39. Rohmann KN, Schlinger BA, Saldanha CJ: Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. / J Neurobiol 2006, 67:1-. CrossRef
    40. Simpson HB, Vicario DS: Early estrogen treatment alone causes female zebra finches to produce learned, male-like vocalizations. / J Neurobiol 1991, 22:755-76. CrossRef
    41. Simpson HB, Vicario DS: Early estrogen treatment of female zebra finches masculinizes the brain pathway for learned vocalizations. / J Neurobiol 1991, 22:777-93. CrossRef
    42. Wade J, Arnold AP: Post-hatching inhibition of aromatase activity does not alter sexual differentiation of the zebra finch song system. / Brain Res 1994, 639:347-50. CrossRef
    43. Grisham W, Park SH, Hsia JK, Kim C, Leung MC, Kim L, Arnold AP: Effects of long-term flutamide treatment during development in zebra finches. / Neurosci Letters 2007, 418:92-6. CrossRef
    44. Mathews GA, Brenowitz EA, Arnold AP: Paradoxical hypermasculinization of the zebra finch song system by an antiestrogen. / Horm Behav 1988, 22:540-51. CrossRef
    45. Schlinger BA, Arnold AP: Androgen effects on the development of the zebra finch song system. / Brain Res 1991, 561:99-05. CrossRef
    46. Wade J, Springer ML, Wingfield JC, Arnold AP: Neither testicular androgens nor embryonic aromatase activity alters morphology of the neural song system in zebra finches. / Biol Reprod 1996, 55:1126-132. CrossRef
    47. Agate RJ, Choe M, Arnold AP: Sex differences in structure and expression of the sex chromosome genes CHD1Z and CHD1W in zebra finches. / Mol Biol Evol 2004, 21:384-96. CrossRef
    48. Arnold AP, Itoh Y, Melamed E: A Birds-Eye View of Sex Chromosome Dosage Compensation. / Annu Rev Genomics Hum Genet 2008, 9:109-27. CrossRef
    49. Wade J, Tang YP, Peabody C, Tempelman RJ: Enhanced gene expression in the forebrain of hatchling and juvenile male zebra finches. / J Neurobiol 2005, 64:224-38. CrossRef
    50. Tomaszycki ML, Peabody C, Replogle K, Clayton DF, Tempelman RJ, Wade J: Sexual differentiation of the zebra finch song system: Potential roles for sex chromosome genes. / BMC Neurosci 2009, 10:24. CrossRef
    51. Ellegren H, Hultin-Rosenberg L, Brunstrom B, Dencker L, Kultima K, Scholz B: Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. / BMC Biol 2007, 5:40. CrossRef
    52. Itoh Y, Kampf K, Arnold AP: Comparison of the chicken and zebra finch Z chromosomes shows evolutionary rearrangements. / Chromosome Res 2006, 14:805-15. CrossRef
    53. Melamed E, Arnold AP: Regional differences in dosage compensation on the chicken Z chromosome. / Genome Biol 2007, 8:R202. CrossRef
    54. Forlano PM, Schlinger BA, Bass AH: Brain aromatase: new lessons from non-mammalian model systems. / Front Neuroendocrinol 2006, 27:247-74. CrossRef
    55. Hojo Y, Murakami G, Mukai H, Higo S, Hatanaka Y, Ogiue-Ikeda M, Ishii H, Kimoto T, Kawato S: Estrogen synthesis in the brain--role in synaptic plasticity and memory. / Mol Cell Endocrinol 2008, 290:31-3. CrossRef
    56. Woolley CS: Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. / Horm Behav 1998, 34:140-48. CrossRef
    57. Itoh Y, Kampf K, Arnold AP: Comparison of the chicken and zebra finch Z chromosomes shows evolutionary rearrangements. / Chrom Res 2006, 14:805-15. CrossRef
    58. Gahr M, Metzdorf R: The sexually dimorphic expression of androgen receptors in the song nucleus hyperstriatalis ventrale pars caudale of the zebra finch develops independently of gonadal steroids. / J Neurosci 1999, 19:2628-636.
    59. Kim YH, Perlman WR, Arnold AP: Expression of Androgen Receptor mRNA in Zebra Finch Song System: Developmental Regulation by Estrogen. / J Comp Neurol 2004, 469:535-47. CrossRef
    60. Replogle K, Arnold AP, Ball GF, Band M, Bensch S, Brenowitz Dong S, Drnevich J, Ferris M, George JM, Gong G, Hasselquist D, Hernandez AG, Kim R, Lewin HA, Liu L, Lovell PV, Mello CV, Naurin S, Rodriguez-Zas S, Thimmapuram J, Wade J, Clayton DF: The Songbird Neurogenomics (SoNG) Initiative: Community-based tools and strategies for study of brain gene function and evolution. / BMC Genomics 2008, 9:134. CrossRef
    61. Adamski J, Leenders F, Carstensen JF, Kaufmann M, Markus MM, Husen B, Tesdorpf JG, Seedorf U, de Launoit Y, Jakob F: Steroids, fatty acyl-CoA, and sterols are substrates of 80-kDa multifunctional protein. / Steroids 1997, 62:159-63. CrossRef
    62. Normand T, Husen B, Leenders F, Pelczar H, Baert JL, Begue A, Flourens AC, Adamski J, de Launoit Y: Molecular characterization of mouse 17 beta-hydroxysteroid dehydrogenase IV. / J Steroid Biochem Mol Biol 1995, 55:541-48. CrossRef
    63. Lewis SE, Searle SM, Harris N, Gibson M, Lyer V, Richter J, Wiel C, Bayraktaroglir L, Birney E, Crosby MA, Kaminker JS, Matthews BB, Prochnik SE, Smithy CD, Tupy JL, Rubin GM, Misra S, Mungall CJ, Clamp ME: Apollo: a sequence annotation editor. / Genome Biol 2002, 3:RESEARCH0082. CrossRef
    64. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Kunstner A, Searle S, White S, Vilella AJ, Heger A, Kong L, Ponting CP, Jarvis E, Mello CV, Minx P, Yang S-P, Lovell P, Velho TAF, Ferris M, Balakrishnan CN, Sinha S, Blatti C, London SE, Li Y, Lin Y-C, George J, Sweedler J, Southey B, Gunaratne P, Watson M, Nam K, Backstrom N, Smeds L, Nabholz B, Itoh Y, Howard J, Pffenning A, Whitney O, V?lker M, Skinner BM, Griffin DK, Ye L, Flicek P, Quesada V, Velasco G, Lopez-Otin C, Puente XS, Oleander T, Lancet D, Villela A, Smit AFA, Hubley R, Konkel M, Walker JA, Batzer MA, Gu W, Pollock DD, Chen L, Cheng G, Eichler E, Stapley J, Slate J, Ekblom R, Burt D, Scharff C, Adam I, Richard H, Sultan M, Soldatov A, Graves T, Fulton L, Nelson J, Chinwalla A, Hou S, Mardis ER, Wilson RK: The genome of a songbird. / Nature, in press.
    65. Leenders F, Dolez V, Begue A, Moller G, Gloeckner JC, de Launoit , Adamski J: Structure of the gene for the human 17beta-hydroxysteroid dehydrogenase type IV. / Mamm Genome 1998, 9:1036-041. CrossRef
    66. Itoh Y, Melamed E, Yang X, Kampf K, Wang S, Yehya N, Van Nas A, Replogle K, Band MR, Clayton DF, Schadt EE, Lusis AJ, Arnold AP: Dosage compensation is less effective in birds than in mammals. / J Biol 2007, 6:2. CrossRef
    67. Itoh Y, Kampf K, Arnold AP: Molecular cloning of zebra finch W chromosome repetitive sequences: Evolution of the avian W chromosome. / Chromosoma 2008, 117:111-21. CrossRef
    68. Itoh Y, Kampf K, Arnold AP: Disruption of FEM1C-W gene in zebra finch: Evolutionary insights on avian ZW genes. / Chromosoma 2009, 118:323-34. CrossRef
    69. Remage-Healey L, Coleman MJ, Oyama RK, Schlinger BA: Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. / Proc Natl Acad Sci USA 107(8):3852-.
    70. Lovell PV, Clayton DF, Replogle KL, Mello CV: Birdsong "transcriptomics": Neurochemical specializations of the oscine song system. / PLoS ONE 2008, 3:e3440. CrossRef
    71. Gilfillan GD, Straub T, de Wit E, Greil F, Lamm R, van Steensel B, / et al.: Chromosome-wide gene-specific targeting of the Drosophila dosage compensation complex. / Genes Dev 2006, 20:858-70. CrossRef
    72. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, Dudko OK, Malley JD, Eastman PS, Oliver B: Global analysis of X-chromosome dosage compensation. / J Biol 2006, 5:3. CrossRef
    73. Nguyen DK, Disteche CM: Dosage compensation of the active X chromosome in mammals. / Nat Genetics 2006, 38:47-3. CrossRef
    74. Kacser H, Burns JA: The molecular basis of dominance. / Genetics 1981, 97:639-66.
    75. Itoh Y, Arnold AP: Chromosomal polymorphism and comparative painting analysis in the zebra finch. / Chrom Res 2005, 13:47-6. CrossRef
    76. Cam V, Schlinger BA: Activities of aromatase and 3β-hydroxysteroid dehydrogenase/Δ4-Δ5 isomerase in whole organ cultures of tissues from developing zebra finches. / Horm Behav 1998, 33:31-9. CrossRef
    77. Freking F, Nazairians T, Schlinger BA: The expression of the sex steroid-synthesizing enzymes CYP11A1, 3beta-HSD, CYP17, and CYP19 in gonads and adrenals of adult and developing zebra finches. / Gen Comp Endocrinol 2000, 119:140-51. CrossRef
    78. Schlinger BA, Lane NI, Grisham W, Thompson L: Androgen synthesis in a songbird: a study of cyp17 (17alpha-hydroxylase/C17,20-lyase) activity in the zebra finch. / Gen Comp Endocrinol 1999, 113:46-8. CrossRef
  • 作者单位:Sarah E London (1) (2) (3) (5)
    Yuichiro Itoh (2) (3)
    Valentin A Lance (2)
    Petra M Wise (2)
    Preethika S Ekanayake (2)
    Randi K Oyama (2)
    Arthur P Arnold (1) (2) (3)
    Barney A Schlinger (1) (2) (3) (4)

    1. Interdepartmental Program in Neuroscience, University of California at Los Angeles, Los Angeles, CA, USA
    2. Department of Physiological Science, University of California at Los Angeles, Los Angeles, CA, USA
    3. Laboratory of Neuroendocrinology of the Brain Research Institute, University of California at Los Angeles, Los Angeles, CA, USA
    5. Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
    4. Department of Ecology and Evolutionary Biology, University of California at Los Angeles, Los Angeles, CA, USA
文摘
Background Steroids affect many tissues, including the brain. In the zebra finch, the estrogenic steroid estradiol (E2) is especially effective at promoting growth of the neural circuit specialized for song. In this species, only the males sing and they have a much larger and more interconnected song circuit than females. Thus, it was surprising that the gene for 17β-hydroxysteroid dehydrogenase type 4 (HSD17B4), an enzyme that converts E2 to a less potent estrogen, had been mapped to the Z sex chromosome. As a consequence, it was likely that HSD17B4 was differentially expressed in males (ZZ) and females (ZW) because dosage compensation of Z chromosome genes is incomplete in birds. If a higher abundance of HSD17B4 mRNA in males than females was translated into functional enzyme in the brain, then contrary to expectation, males could produce less E2 in their brains than females. Results Here, we used molecular and biochemical techniques to confirm the HSD17B4 Z chromosome location in the zebra finch and to determine that HSD17B4 mRNA and activity were detectable in the early developing and adult brain. As expected, HSD17B4 mRNA expression levels were higher in males compared to females. This provides further evidence of the incomplete Z chromosome inactivation mechanisms in birds. We detected HSD17B4 mRNA in regions that suggested a role for this enzyme in the early organization and adult function of song nuclei. We did not, however, detect significant sex differences in HSD17B4 activity levels in the adult brain. Conclusions Our results demonstrate that the HSD17B4 gene is expressed and active in the zebra finch brain as an E2 metabolizing enzyme, but that dosage compensation of this Z-linked gene may occur via post-transcriptional mechanisms.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700