Identification of male-biased gene: Parvalbumin in song control nuclei of the Bengalese finch

Neuroscience Research

Volumn 68, Issue 1, 2010, Pages 22-34

  Sun, LiNa ^a   Wang, Rui ^a   Zeng, ShaoJu ^a   Geng, ZhiTao ^a   Zhang, XinWen ^b   Zuo, MingXue ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

^b Hainan Normal College   (China)

Author keywords

Age groups; Calcium binding protein; Parvalbumin; Sex differentiation; Song control nuclei; Suppression subtraction hybridization

Indexed keywords

CALCIUM BINDING PROTEIN; COMPLEMENTARY DNA; MESSENGER RNA; PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CLONE; FEMALE; FINCH; GENE EXPRESSION; HIGH VOCAL CENTER; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVE CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEX DIFFERENCE; SONGBIRD; SUPPRESSION SUBTRACTION HYBRIDIZATION;

EID: 77955340714     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2010.05.003     Document Type: Article

References (68)

1. Agate R.J., Grisham W., Wade J., Mann S., Wingfield J., Schanen C., Palotie A., Arnold A.P. Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4873-4878.
2. Agate R.J., Choe M., Arnold A.P. Sex differences in structure and expression of the sex chromosome genes CHD1Z and CHD1W in zebra finches. Mol. Biol. Evol. 2004, 21:384-396.
3. Akutagawa E., Konishi M. Two separate areas of the brain differentially guide the development of a song control nucleus in the zebra finch. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:12413-12417.
4. Andressen C., Blümcke I., Celio M.R. Calcium-binding proteins, selective markers of nerve cells. Cell Tissue Res. 1993, 271:181-208.
5. Balmer T.S., Carels V.M., Frisch J.L., Nick T.A. Modulation of perineuronal nets and parvalbumin with developmental song learning. J. Neurosci. 2009, 29:12878-12885.
6. Balthazart J., Absil P., Fiasse V., Ball G.F. Effects of the aromatase inhibitor R76713 on sexual differentiation of brain and behavior in zebra finches. Behaviour 1995, 120:225-260.
7. Barnea A., Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl. Acad. Sci. 1994, 91:11217-11221.
8. Bottjer S.W., Halsema K.A., Brown S.A., Miesner E.A. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. Comp. Neurol. 1989, 279:312-326.
9. Brager D.H., Sickel M.J., McCarthy M.M. Developmental sex differences in calbindin-D28K and calretinin immunoreactivity in the neonatal rat hypothalamus. J. Neurobiol. 1999, 42:315-322.
10. Braun K., Scheich H., Heizmann C.W., Hunziker W. Parvalbumin and calbindin-D28K immunoreactivity as developmental markers of auditory and vocal motor nuclei of the zebra finch. Neuroscience 1991, 40:853-869.
11. Braunewell K.H., Gundelfinger E.D. Intracellular neuronal calcium sensor proteins, a family of EF-hand calcium-binding proteins in search of a function. Cell Tissue Res. 1999, 295:1-12.
12. Burek M.J., Nordeen K.W., Nordeen E.J. Estrogen promotes neuron addition to an avian song-control nucleus by regulating postmitotic events. Dev. Brain Res. 1995, 85:220-224.
13. 2+ and secretory vesicle dynamics. Trends Neurosci. 1995, 18:191-196.
14. 2+-binding proteins. Biochem. J. 2001, 353:1-12.
15. Caillard O., Moreno H., Schwaller B., Llano I., Celio M.R., et al. Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc. Natl. Acad. Sci. 2000, 97:13372-13377.
16. Clayton D.F. Role of gene regulation in song circuit development and song learning. J. Neurobiol. 1997, 33:549-571.
17. de Lecea L., del Río J.A., Soriano E. Developmental expression of parvalbumin mRNA in the cerebral cortex and hippocampus of the rat. Brain Res. Mol. Brain Res. 1995, 32:1-13.
18. Fierro L., Llano I. High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J. Physiol. 1996, 496:617-625.
19. Grisham W., Arnold A.P. A direct comparison of the masculinizing effects of testosterone, androstenedione, estrogen, and progesterone on the development of the zebra finch song system. J. Neurobiol. 1995, 26:163-170.
20. Gurney M.E. Hormonal control of cell form and number in the zebra finch song system. J. Neurosci. 1981, 1:658-673.
21. Heizmann C.W. Calcium-binding proteins, basic concepts and clinical implications. Gen. Physiol. Biophys. 1992, 11:411-425.
22. Holloway C.C., Clayton D.F. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci. 2001, 4:170-175.
23. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
24. Itoh Y., Melamed E., Yang X., Kampf K., Wang S., Yehya N., Van Nas A., Replogle K., Band M.R., Clayton D.F., Schadt E.E., Lusis A.J., Arnold A.P. Dosage compensation is less effective in birds than in mammals. J. Biol. 2007, 6:2.
25. Jacobs E.C., Grisham W., Arnold A.P. Lack of a synergistic effect between estradiol and dihydrotestosterone in the masculinization of the zebra finch song system. J. Neurobiol. 1995, 27:513-519.
26. Jacobs E.C., Arnold A.P., Campagnoni A.T. Developmental regulation of the distribution of aromatase- and estrogen-receptor mRNA-expressing cells in the zebra finch brain. Dev. Neurosci. 1999, 21:453-472.
27. Jones E.G. Viewpoint, the core and matrix of thalamic organization. Neuroscience 1998, 85:331-345.
28. 2+-binding parvalbumin in rat testis, characterization, localization and expression during development. J. Biol. Chem. 1987, 262:7314-7320.
29. Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci. 1993, 13:4908-4923.
30. Kawaguchi Y., Kubota Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 1993, 70:387-396.
31. 2+/calmodulin-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:945-949.
32. Konishi M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 1965, 22:770-783.
33. Krebs J.R., Sherry D.F., Healy S.D., Perry V.H., Vaccarino L. Hippocampal specialization of food-storing birds. Proc. Natl. Acad. Sci. 1989, 86:1388-1392.
34. Li X., Wang X.J., Tannenhauser J., Podell S., Mukherjee P., Hertel M., Biane J., Masuda S., Nottebohm F., Gaasterland T. Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:6834-6839.
35. Mathews G.A., Arnold A.P. Antiestrogens fail to prevent the masculine ontogeny of the zebra finch song system. Gen. Comp. Endocrinol. 1990, 80:48-58.
36. McMahon A., Wong B.S., Iacopino A.M., Ng M.C., Chi S., German D.C. Calbindin-D28k buffers intracellular calcium and promotes resistance to degeneration in PC12 cells. Brain Res. Mol. Brain Res. 1998, 54:56-63.
37. Münkle M.C., Waldvogel H.J., Faull R.L. The distribution of calbindin, calretinin and parvalbumin immunoreactivity in the human thalamus. J. Chem. Neuroanat. 2000, 19:155-173.
38. Nixdorf-Bergweiler B.E. Divergent and parallel development in volume sizes of telencephalic song nuclei in male and female zebra finches. J. Comp. Neurol. 1996, 375:445-456.
39. Nordeen E.J., Nordeen K.W., Arnold A.P. Sexual differentiation of androgen accumulation within the zebra finch brain through selective cell loss and addition. J. Comp. Neurol. 1987, 259:393-399.
40. Nottebohm F., Arnold A.P. Sexual dimorphism in vocal control areas of the songbird brain. Science 1976, 194:211-213.
41. Nottebohm F., Kelley D.B., Paton J.A. Connections of vocal control nuclei in the canary telencephalon. Comp. Neurol. 1982, 207:344-357.
42. Persechini A., Moncrief N.D., Kretsinger R.H. The EF-hand family of calcium-modulated proteins. Trends Neurosci. 1989, 12:462-467.
43. Pohl V., Pattyn G., Berchtold M. Parvalbumin expression during developmental differentiation of the rat ovary. Differentiation 1995, 59:235-242.
44. Saldanha C.J., Tuerk M.J., Kim Y.H., Fernandes A.O., Arnold A.P., Schlinger B.A. Distribution and regulation of telencephalic aromataseexpression in the zebra finch revealed with a specific antibody. J. Comp. Neurol. 2000, 423:619-630.
45. Schlinger B.A., Arnold A.P. Androgen effects on the development of the zebra finch song system. Brain Res. 1991, 561:99-105.
46. Schlinger B.A., Arnold A.P. Plasma sex steroids and tissue aromatization in hatchling zebra finches, Implications for the sexual differentiation of singing behavior. Endocrinology 1992, 130:289-299.
47. Schlinger B.A., Soma K.K., London S.E. Neurosteroids and brain sexual differentiation. Trends Neurosci. 2001, 24:429-431.
48. Sherry D.F., Vaccarino A.L., Buckenham K., Herz R.S. The hippocampal complex of food-storing birds. Brain Behav. Evol. 1989, 34:308-317.
49. Springer M.L., Wade J. The effects of testicular tissue and prehatching inhibition of estrogen synthesis on the development of courtship and copulatory behavior in zebra finches. Horm. Behav. 1997, 32:46-59.
50. Stark L.L., Perkel D.J. Two-stage, input-specific synaptic maturation in anucleus essential for vocal production in the zebra finch. J. Neurosci. 1999, 19:9107-9116.
51. Tomaszycki M.L., Peabody C., Replogle K., Clayton D.F., Tempelman R.J., Wade J. Sexual differentiation of the zebra finch song system, potential roles for sex chromosome genes. BMC Neurosci. 2009, 10:24.
52. Veney S.L., Peabody C., Smith G.W., Wade J. Sexually dimorphic neurocalcin expression in the developing zebra finch telencephalon. J. Neurobiol. 2003, 56:372-386.
53. Vockel A., Prove E., Balthazart J. Sex- and age-related differences in the activity of testosterone-metabolizing enzymes in microdissected nuclei of the zebra finch brain. Brain Res. 1990, 511:291-302.
54. Wade J., Arnold A.P. Post-hatching inhibition of aromatase activity does not alter sexual differentiation of the zebra finch song system. Brain Res. 1994, 639:347-350.
55. Wade J., Schlinger B.A., Arnold A.P. Aromatase and 5b-reductase activity in cultures of developing zebra finch brain, an investigation of sex and regional differences. J. Neurobiol. 1995, 27:240-251.
56. Wade J., Arnold A.P. Functional testicular tissue does not masculinize development of the zebra finch song system. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:5264-5268.
57. Wade J., Springer M.L., Wingfield J.C., Arnold A.P. Neither testicular androgens nor embryonic aromatase activity alters morphology of theneural song system in zebra finches. Biol. Reprod. 1996, 55:1126-1132.
58. Wade J., Swender D.A., McElhinny T.L. Sexual differentiation of the zebra finch song system parallels genetic, not gonadal, sex. Horm. Behav. 1999, 36:141-152.
59. Wade J. Zebra finch sexual differentiation, the aromatization hypothesis revisited. Microsc. Res. Tech. 2001, 54:354-363.
60. Wade J., Peabody C., Coussens P., Tempelman R.J., Clayton D.F., Liu L., Arnold A.P., Agate R. A cDNA microarray from the telencephalon of juvenile male and female zebra finches. J. Neurosci. Methods 2004, 138:199-206.
61. Wade J., Tang Y.P., Peabody C., Tempelman R.J. Enhanced gene expression in the forebrain of hatchling and juvenile male zebra finches. J. Neurobiol. 2005, 64:224-238.
62. Wild J.M., Williams M.N., Suthers R.A. Parvalbumin-positive projection neurons characterise the vocal premotor pathway in male, but not female, zebra finches. Brain Res. 2001, 917:235-252.
63. Wild J.M., Williams M.N., Howie G.J., Mooney R. Calcium-binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata). J. Comp. Neurol. 2005, 483:76-90.
64. Zeigler H.P., Marler P. Behavioral Neurobiology of Birdsong 2004, New York Academy of Sciences, New York, pp. 788.
65. Zeng S.J., Zhang X.W., Zuo M.X. The mechanism of sexual difference of vocalization in Lonchura striata swinhoei. Zool. Res. 2001, 22:51-57.
66. Zeng S.J., Zhang X.W., Zuo M.X. Change and its neural mechanism of volumes of song control nuclei during development in the striated manikin (Lonchura striata swinhoei). Zool. Res. 2002, 23:456-462.
67. Zeng S.J., Song K., Xu N., Zhang X.W., Zuo M.X. Sex difference in cellular proliferation within the telencephalic ventricle zone of Bengalese finch. Neurosci. Res. 2007, 58:207-214.
68. Zhu N., Sun Y., Zeng S., Zhang X., Zuo M. Collapsin response mediator protein-4 (CRMP-4) expression in posthatching development of song control nuclei in Bengalese finches. Brain Res. Bull. 2008, 76:551-558.