Sexual differentiation of the zebra finch song system: Potential roles for sex chromosome genes

BMC Neuroscience

Volumn 10, Issue , 2009, Pages

  Tomaszycki, Michelle L ^a,c   Peabody, Camilla ^a   Replogle, Kirstin ^b   Clayton, David F ^b   Tempelman, Robert J ^a   Wade, Juli ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COMPLEMENTARY DNA; MESSENGER RNA; METHYLCROTONOYL COENZYME A CARBOXYLASE; SORTING NEXIN 2; TESTOSTERONE 17BETA DEHYDROGENASE; TESTOSTERONE 17BETA DEHYDROGENASE TYPE IV; UNCLASSIFIED DRUG; HYDROXYSTEROID DEHYDROGENASE; LIGASE; METHYLCROTONOYL COA CARBOXYLASE; METHYLCROTONOYL-COA CARBOXYLASE; VESICULAR TRANSPORT PROTEIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; FINCH; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC ASSOCIATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; POEPHILA CASTANOTIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEX CHROMOSOME; SEX DIFFERENTIATION; SINGING; TELENCEPHALON; ANIMAL; DNA MICROARRAY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT; SOUTHERN BLOTTING; VOCALIZATION;

17-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; BLOTTING, SOUTHERN; CARBON-CARBON LIGASES; FEMALE; FINCHES; GENE EXPRESSION; IN SITU HYBRIDIZATION; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEX CHARACTERISTICS; SEX CHROMOSOMES; SEX DIFFERENTIATION; TELENCEPHALON; VESICULAR TRANSPORT PROTEINS; VOCALIZATION, ANIMAL;

EID: 63849289226     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-10-24     Document Type: Article

References (65)

1. Tchernichovski O Nottebohm F Social inhibition of song imitation among sibling male zebra finches Proc Natl Acad Sci USA 1998, 95(15):8951-8956. 21183 9671785 10.1073/pnas.95.15.8951
2. Bottjer SW Neural strategies for learning during sensitive periods of development J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2002, 188(11-12):917-928. 12471491
3. Nordeen KW Nordeen EJ Anatomical and synaptic substrates for avian song learning J Neurobiol 1997, 33(5):532-548. 10.1002/ (SICI)1097-4695(19971105)33:5<532::AID-NEU4>3.0.CO;2-5 9369458
4. Nowicki S Searcy WA Song function and the evolution of female preferences: Why birds sing, why brains matter Ann N Y Acad Sci 2004, 1016:704-723. 10.1196/annals.1298.012 15313801
5. Arnold AP Sexual differentiation of the zebra finch song system: positive evidence, negative evidence, null hypotheses, and a paradigm shift J Neurobiol 1997, 33(5):572-584. 10.1002/ (SICI)1097-4695(19971105)33:5<572::AID-NEU6>3.0.CO;2-1 9369460
6. Reiner A Perkel DJ Bruce LL Butler AB Csillag A Kuenzel W Medina L Paxinos G Shimizu T Striedter G, et al Revised nomenclature for avian telencephalon and some related brainstem nuclei J Comp Neurol 2004, 473(3):377-414. 2518311 15116397 10.1002/cne.20118
7. Doupe AJ Solis MM Song- and order-selective neurons develop in the songbird anterior forebrain during vocal learning J Neurobiol 1997, 33(5):694-709. 10.1002/ (SICI)1097-4695(19971105)33:5<694::AID-NEU13>3.0.CO;2-9 9369467
8. Nottebohm F Arnold AP Sexual dimorphism in vocal control areas of the songbird brain Science 1976, 194(4261):211-213. 10.1126/science.959852 959852
9. Nixdorf-Bergweiler BE Lateral magnocellular nucleus of the anterior neostriatum (LMAN) in the zebra finch: Neuronal connectivity and the emergence of sex differences in cell morphology Microsc Res Tech 2001, 54(6):335-353. 10.1002/jemt.1147 11668647
10. Wade J Zebra finch sexual differentiation: The aromatization hypothesis revisited Microsc Res Tech 2001, 54(6):354-363. 10.1002/jemt.1148 11668648
11. 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(7):2628-2636. 10087076
12. Adkins-Regan E Ascenzi M Sexual differentiation of behavior in the zebra finch: Effect of early gonadectomy or androgen treatment Horm Behav 1990, 24:114-127. 10.1016/0018-506X(90)90031-R 2328966
13. Arnold AP The effects of castration on song development in zebra finches (Poephila guttata) J Exp Zool 1975, 191(2):261-278. 10.1002/ jez.1401910212 1113072
14. Mathews GA Arnold AP Tamoxifen's effects on the zebra finch song system are estrogenic, not antiestrogenic J Neurobiol 1991, 22(9):957-969. 10.1002/neu.480220907 1724458
15. Mathews GA Arnold AP Antiestrogens fail to prevent the masculine ontogeny of the zebra finch song system Gen Comp Endocrinol 1990, 80(1):48-58. 10.1016/0016-6480(90)90147-E 2272479
16. Mathews GA Brenowitz EA Arnold AP Paradoxical hypermasculinization of the zebra finch song system by an antiestrogen Horm Behav 1988, 22(4):540-551. 10.1016/0018-506X(88)90057-8 3235068
17. Balthazart J Absil P Fiasse V Ball GF Effects of the aromatase inhibitor R76713 on sexual differentiation of brain and behavior in zebra finches Behav 1995, 120:225-260.
18. 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(2):347-350. 10.1016/0006-8993(94)91752-3 8205488
19. Hutchison JB Wingfield JC Hutchison RE Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch J Endocrinol 1984, 103(3):363-369. 10.1677/joe.0.1030363 6502063
20. Adkins-Regan E Abdelnabi M Mobarak M Ottinger MA Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata) Gen Comp Endocrinol 1990, 78(1):93-109. 10.1016/0016-6480(90)90051-M 2332151
21. Schlinger BA Sexual differentiation of avian brain and behavior: Current views on gonadal hormone-dependent and independent mechanisms Annu Rev Physiol 1998, 60:407-429. 10.1146/annurev.physiol.60.1.407 9558471
22. Itoh Y Melamed E Yang X Kampf K Wang S Yehya N Van Nas A Replogle K Band MR Clayton DF, et al Dosage compensation is less effective in birds than in mammals J Biol 2007, 6(1):2. 2373894 17352797 10.1186/jbiol53
23. 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(8):4873-4878. 153648 12672961 10.1073/pnas.0636925100
24. 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(21):7730-7735. 1140405 15894627 10.1073/pnas.0408350102
25. Tang YP Peabody C Tomaszycki ML Wade J Sexually dimorphic SCAMP1 expression in the forebrain motor pathway for song production of juvenile zebra finches Dev Neurobiol 2007, 67(4):474-482. 10.1002/ dneu.20354 17443802
26. Duncan KA Carruth LL The sexually dimorphic expression of L7/SPA, an estrogen receptor coactivator, in zebra finch telencephalon Dev Neurobiol 2007, 67(14):1852-1866. 10.1002/dneu.20539 17823931
27. Tang YP Wade J Sexually dimorphic expression of the genes encoding ribosomal proteins L17 and L37 in the song control nuclei of juvenile zebra finches Brain Res 2006, 1126(1):102-108. 10.1016/ j.brainres.2006.08.002 16938280
28. Wolfinger RD Gibson G Wolfinger ED Bennett L Hamadeh H Bushel P Afshari C Paules RS Assessing gene significance from cDNA microarray expression data via mixed models J Comput Biol 2001, 8(6):625-637. 10.1089/ 106652701753307520 11747616
29. Wade J Arnold AP Sexual differentiation of the zebra finch song system Ann N Y Acad Sci 2004, 1016:540-559. 10.1196/annals.1298.015 15313794
30. Bottjer SW Glaessner SL Arnold AP Ontogeny of brain nuclei controlling song learning and behavior in zebra finches J Neurosci 1985, 5(6):1556-1562. 4009245
31. Clayton NS Song discrimination learning in zebra finches Anim Behav 1988, 36:1016-1024. 10.1016/S0003-3472(88)80061-7
32. Replogle K Arnold AP Ball GF Band M Bensch S Brenowitz EA Dong S Drnevich J Ferris M George JM, et al The Songbird Neurogenomics (SoNG) Initiative: Community-based tools and strategies for study of brain gene function and evolution BMC Genomics 2008, 9:131. 2329646 18366674 10.1186/1471-2164-9-131
33. Allison DB Cui XQ Page GP Sabripour M Microarray data analysis: From disarray to consolidation and consensus Nature Reviews Genetics 2006, 7(1):55-65. 10.1038/nrg1749 16369572
34. Kerr KF Serikawa KA Wei CM Peters MA Bumgarner RE What is the best reference RNA? And other questions regarding the design and analysis of two-color microarray experiments Omics-a Journal of Integrative Biology 2007, 11(2):152. 165 10.1089/omi.2007.0012 17594235
35. Yang YH Dudoit S Luu P Lin DM Peng V Ngai J Speed TP Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation Nucleic Acids Res 2002, 30(4):e15. 100354 11842121 10.1093/nar/30.4.e15
36. Storey JD Tibshirani R Statistical significance for genomewide studies Proc Natl Acad Sci USA 2003, 100(16):9440-9445. 170937 12883005 10.1073/ pnas.1530509100
37. 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(2):224-238. 10.1002/neu.20141 15849735
38. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262 11846609
39. Dewing P Shi T Horvath S Vilain E Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation Brain Res Mol Brain Res 2003, 118(1-2):82-90. 10.1016/S0169-328X(03)00339-5 14559357
40. Clayton DF Role of gene regulation in song circuit development and song learning J Neurobiol 1997, 33(5):549-571. 10.1002/ (SICI)1097-4695(19971105)33:5<549::AID-NEU5>3.0.CO;2-4 9369459
41. 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. 2099419 17883843 10.1186/ 1741-7007-5-40
42. Melamed E Arnold AP Regional differences in dosage compensation on the chicken Z chromosome Genome Biol 2007, 8(9):R202. 2375040 17900367 10.1186/gb-2007-8-9-r202
43. Mank JE Ellegren H All dosage compensation is local: Gene-by-gene regulation of sex-biased expression on the chicken Z chromosome Heredity 2009, 102(3):312-320. 10.1038/hdy.2008.116 18985062
44. Scharff C Nottebohm F A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning J Neurosci 1991, 11(9):2896-2913. 1880555
45. Bottjer SW Miesner EA Arnold AP Forebrain lesions disrupt development but not maintenance of song in passerine birds Science 1984, 224(4651):901-903. 10.1126/science.6719123 6719123
46. Korsia S Bottjer SW Developmental changes in the cellular composition of a brain nucleus involved with song learning in zebra finches Neuron 1989, 3(4):451-460. 10.1016/0896-6273(89)90204-3 2561972
47. Mooney R Rao M Waiting periods versus early innervation: The development of axonal connections in the zebra finch song system J Neurosci 1994, 14(11 Pt 1):6532-6543. 7965057
48. George JM Jin H Woods WS Clayton DF Characterization of a novel protein regulated during the critical period for song learning in the zebra finch Neuron 1995, 15(2):361-372. 10.1016/0896-6273(95)90040-3 7646890
49. Jin H Clayton DF Synelfin regulation during the critical period for song learning in normal and isolated juvenile zebra finches Neurobiol Learn Mem 1997, 68:271-284. 10.1006/nlme.1997.3795 9398589
50. Murin R Verleysdonk S Rapp M Hamprecht B Immunocytochemical localization of 3-methylcrotonyl-CoA carboxylase in cultured ependymal, microglial and oligodendroglial cells J Neurochem 2006, 97(5):1393-1402. 10.1111/ j.1471-4159.2006.03819.x 16696850
51. Hershkowitz M Wilson JE Glassman E The incorporation of radioactive amino acids into brain subcellular proteins during training J Neurochem 1975, 25(5):687-694. 10.1111/j.1471-4159.1975.tb04389.x 1194925
52. Baumgartner MR Dantas MF Suormala T Almashanu S Giunta C Friebel D Gebhardt B Fowler B Hoffmann GF Baumgartner ER, et al Isolated 3-methylcrotonyl-CoA carboxylase deficiency: Evidence for an allele-specific dominant negative effect and responsiveness to biotin therapy Am J Hum Genet 2004, 75(5):790-800. 1182108 15359379 10.1086/ 425181
53. Darin N Andersen O Wiklund LM Holmgren D Holme E 3-methylcrotonyl-CoA carboxylase deficiency and severe multiple sclerosis Pediatr Neurol 2007, 36(2):132-134. 10.1016/j.pediatrneurol.2006.09.007 17275669
54. Aamodt SM Nordeen EJ Nordeen KW Blockade of NMDA receptors during song model exposure impairs song development in juvenile zebra finches Neurobiol Learn Mem 1996, 65(1):91-98. 10.1006/nlme.1996.0010 8673412
55. Doupe AJ Perkel DJ Reiner A Stern EA Birdbrains could teach basal ganglia research a new song Trends Neurosci 2005, 28(7):353-363. 10.1016/ j.tins.2005.05.005 15935486
56. Haesler S Rochefort C Georgi B Licznerski P Osten P Scharff C Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X PLoS Biol 2007, 5(12):e321. 2100148 18052609 10.1371/journal.pbio.0050321
57. Brainard MS Contributions of the anterior forebrain pathway to vocal plasticity Ann N Y Acad Sci 2004, 1016:377-394. 10.1196/annals.1298.042 15313786
58. Bonifacino JS Rojas R Retrograde transport from endosomes to the trans-Golgi network Nat Rev Mol Cell Biol 2006, 7(8):568-579. 10.1038/ nrm1985 16936697
59. Griffin CT Trejo J Magnuson T Genetic evidence for a mammalian retromer complex containing sorting nexins 1 and 2 Proc Natl Acad Sci USA 2005, 102(42):15173-15177. 1257690 16214895 10.1073/pnas.0409558102
60. Small SA Kent K Pierce A Leung C Kang MS Okada H Honig L Vonsattel JP Kim TW Model-guided microarray implicates the retromer complex in Alzheimer's disease Ann Neurol 2005, 58(6):909-919. 10.1002/ana.20667 16315276
61. Doupe AJ Solis MM Kimpo R Boettiger CA Cellular, circuit, and synaptic mechanisms in song learning Ann N Y Acad Sci 2004, 1016:495-523. 10.1196/ annals.1298.035 15313792
62. Schlinger BA Sex steroids and their actions on the birdsong system J Neurobiol 1997, 33(5):619-631. 10.1002/ (SICI)1097-4695(19971105)33:5<619::AID-NEU9>3.0.CO;2-7 9369463
63. de Launoit Y Adamski J Unique multifunctional HSD17B4 gene product: 17beta-hydroxysteroid dehydrogenase 4 and D-3-hydroxyacyl-coenzyme A dehydrogenase/hydratase involved in Zellweger syndrome J Mol Endocrinol 1999, 22(3):227-240. 10.1677/jme.0.0220227 10343282
64. Wild JM Functional neuroanatomy of the sensorimotor control of singing Ann N Y Acad Sci 2004, 1016:438-462. 10.1196/annals.1298.016 15313789
65. Kirn JR DeVoogd TJ Genesis and death of vocal control neurons during sexual differentiation in the zebra finch J Neurosci 1989, 9(9):3176-3187. 2795159