Expression of reelin, its receptors and its intracellular signaling protein, Disabled1 in the canary brain: Relationships with the song control system

Neuroscience

Volumn 153, Issue 4, 2008, Pages 944-962

  Balthazart, J ^a   Voigt, C ^a   Boseret, G ^a   Ball, G F ^b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Dab1; immunocytochemistry; in situ hybridization; neuroplasticity; reelin; songbirds

Indexed keywords

LIPOPROTEIN RECEPTOR; MESSENGER RNA; PROTEIN APOER2; PROTEIN DISABLED1; REELIN; SIGNAL PEPTIDE; TESTOSTERONE; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANARY; CONTROLLED STUDY; FEMALE; MALE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

ANIMALS; BRAIN; BRAIN MAPPING; CANARIES; CELL ADHESION MOLECULES, NEURONAL; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NERVE TISSUE PROTEINS; RECEPTORS, CELL SURFACE; SERINE ENDOPEPTIDASES;

EID: 44149088054     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.02.020     Document Type: Article

References (98)

1. Aamodt S.M., Kozlowski M.R., Nordeen E.J., and Nordeen K.W. Distribution and developmental change in [3H]MK-801 binding within zebra finch song nuclei. J Neurobiol 23 (1992) 997-1005
2. Absil P., Pinxten R., Balthazart J., and Eens M. Effects of testosterone on Reelin expression in the brain of male European starlings. Cell Tissue Res 312 (2003) 81-93
3. Alcantara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., Sotelo C., and Soriano E. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18 (1998) 7779-7799
4. Alvarez-Buylla A., and Kirn J.R. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33 (1997) 585-601
5. Alvarez-Buylla A., and Nottebohm F. Migration of young neurons in adult avian brain. Nature 335 (1988) 353-354
6. Alvarez-Buylla A., Theelen M., and Nottebohm F. Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. Proc Natl Acad Sci U S A 85 (1988) 8722-8726
7. Appeltants D., Ball G.F., and Balthazart J. The distribution of tyrosine hydroxylase in the canary brain: demonstration of a specific and sexually dimorphic catecholaminergic innervation of the telencephalic song control nuclei. Cell Tissue Res 304 (2001) 237-259
8. Appeltants D., Ball G.F., and Balthazart J. Song activation by testosterone is associated with an increased catecholaminergic innervation of the song control system in female canaries. Neuroscience 121 (2003) 801-814
9. Bading H. Nuclear calcium-activated gene expression: possible roles in neuronal plasticity and epileptogenesis. Epilepsy Res 36 (1999) 225-231
10. Ball G.F. Chemical neuroanatomical studies of the steroid-sensitive songbird vocal control system: a comparative approach. In: Balthazart J. (Ed). Hormones, brain and behaviour in vertebrates. 1. Sexual differentiation, neuroanatomical aspects, neurotransmitters and neuropeptides. Comp. Physiol Vol. 8 (1990), Karger, Basel 148-167
11. Ball G.F. Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behav Evol 44 (1994) 234-246
12. Ball G.F. Neuroendocrine basis of seasonal changes in vocal behavior among songbirds. In: Hauser M., and Konishi M. (Eds). The design of animal communication (1999), MIT Press, Cambridge, MA 213-253
13. Ball G.F., and Balthazart J. The neuroendocrinology and neurochemistry of birdsong. In: Lajtha A., and Blaustein J.D. (Eds). Handbook of neurochemistry and molecular neurobiology. 3rd edition (2007), Springer, New York 419-457
14. Balthazart J., Absil P., Foidart A., Houbart M., Harada N., and Ball G.F. Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): Implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J Neurobiol 31 (1996) 129-148
15. Balthazart J., Foidart A., Wilson E.M., and Ball G.F. Immunocytochemical localization of androgen receptors in the male songbird and quail brain. J Comp Neurol 317 (1992) 407-420
16. Bar I., Lambert de Rouvroit C., and Goffinet A.M. The Reelin signaling pathway in mouse cortical development. Eur J Morphol 38 (2000) 321-325
17. Basham M.E., Sohrabji F., Singh T.D., Nordeen E.J., and Nordeen K.W. Developmental regulation of NMDA receptor 2B subunit mRNA and ifenprodil binding in the zebra finch anterior forebrain. J Neurobiol 39 (1999) 155-167
18. Bernard D.J., and Ball G.F. Two histological markers reveal a similar photoperiodic difference in the volume of the high vocal center in male European starlings. J Comp Neurol 360 (1995) 726-734
19. Bernard D.J., Casto J.M., and Ball G.F. Sexual dimorphism in the volume of song control nuclei in European starlings: Assessment by a Nissl stain and autoradiography for muscarinic cholinergic receptors. J Comp Neurol 334 (1993) 559-570
20. Bernier B., Bar I., D'Arcangelo G., Curran T., and Goffinet A.M. Reelin mRNA expression during embryonic brain development in the chick. J Comp Neurol 422 (2000) 448-463
21. Bernier B., Bar I., Pieau C., Lambert de Rouvroit C., and Goffinet A.M. Reelin mRNA expression during embryonic brain development in the turtle Emys orbicularis. J Comp Neurol 413 (1999) 463-479
22. Boseret G., Ball G.F., and Balthazart J. The microtubule-associated protein doublecortin is broadly expressed in the telencephalon of adult canaries. J Chem Neuroanat 33 (2007) 140-154
23. Boseret G., Carere C., Ball G.F., and Balthazart J. Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J Neurobiol 66 (2006) 1044-1060
24. Bottjer S.W., Brady J.D., and Cribbs B. Connections of a motor cortical region in zebra finches: relation to pathways for vocal learning. J Comp Neurol 420 (2000) 244-260
25. Bottjer S.W., Halsema K.A., Brown S.A., and Miesner E.A. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J Comp Neurol 279 (1989) 312-326
26. Bottjer S.W., and Johnson F. Circuits, hormones, and learning: Vocal behavior in songbirds. J Neurobiol 33 (1997) 602-618
27. Bottjer S.W., Miesner E.A., and Arnold A.P. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224 (1984) 901-903
28. Brainard M.S., and Doupe A.J. Auditory feedback in learning and maintenance of vocal behaviour. Nat Rev Neurosci 1 (2000) 31-40
29. Brenowitz E., Margoliash D., and Nordeen K.W. The neurobiology of birdsong. J Neurobiol 33 (1997) 495-709
30. Brenowitz E.A. Plasticity of the adult avian song control system. Ann N Y Acad Sci 1016 (2004) 560-585
31. Canady R.A., Burd G.D., DeVoogd T.J., and Nottebohm F. Effect of testosterone on input received by an identified neuron type of the canary song system: A Golgi/electron microscopy/degeneration study. J Neurosci 8 (1988) 3770-3784
32. Cao J., Wenberg K., and Cheng M.F. Lesion induced new neuron incorporation in the adult hypothalamus of the avian brain. Brain Res 943 (2002) 80-92
33. Chen G., Bonder E.M., and Cheng M.F. Lesion-induced neurogenesis in the hypothalamus is involved in behavioral recovery in adult ring doves. J Neurobiol 66 (2006) 537-551
34. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., and Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21 (2005) 1-14
35. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., and Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374 (1995) 719-723
36. de Bergeyck V., Naerhuyzen B., Goffinet A.M., and Lambert de Rouvroit C. A panel of monoclonal antibodies against reelin, the extracellular matric protein defective in reeler mutant mice. J Neurosci Methods 82 (1998) 17-24
37. des Portes V., Francis F., Pinard J.M., Desguerre I., Moutard M.L., Snoeck I., Meiners L.C., Capron F., Cusmai R., Ricci S., Motte J., Echenne B., Ponsot G., Dulac O., Chelly J., and Beldjord C. doublecortin is the major gene causing X-linked subcortical laminar heterotopia (SCLH). Hum Mol Genet 7 (1998) 1063-1070
38. DeVoogd T.J., and Nottebohm F. Gonadal hormones induce dendritic growth in the adult brain. Science 214 (1981) 202-204
39. Doupe A.J., Solis M.M., Kimpo R., and Boettiger C.A. Cellular, circuit, and synaptic mechanisms in song learning. Ann N Y Acad Sci 1016 (2004) 495-523
40. Fatemi S.H. Reelin glycoprotein: structure, biology and roles in health and disease. Mol Psychiatry 10 (2005) 251-257
41. Fatemi S.H. Reelin glycoprotein in autism and schizophrenia. Int Rev Neurobiol 71 (2005) 179-187
42. Forster E., Jossin Y., Zhao S., Chai X., Frotscher M., and Goffinet A.M. Recent progress in understanding the role of Reelin in radial neuronal migration, with specific emphasis on the dentate gyrus. Eur J Neurosci 23 (2006) 901-909
43. Forster E., Tielsch A., Saum B., Weiss K.H., Johanssen C., Graus-Porta D., Muller U., and Frotscher M. Reelin, disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci U S A 99 (2002) 13178-13183
44. Frotscher M., Zhao S., and Forster E. Development of cell and fiber layers in the dentate gyrus. Prog Brain Res 163 (2007) 133-807
45. Fuentealba R.A., Barria M.I., Lee J., Cam J., Araya C., Escudero C.A., Inestrosa N.C., Bronfman F.C., Bu G., and Marzolo M.P. ApoER2 expression increases Abeta production while decreasing Amyloid Precursor Protein (APP) endocytosis: Possible role in the partitioning of APP into lipid rafts and in the regulation of gamma-secretase activity. Mol Neurodegener 2 (2007) 14
46. Goffinet A.M., Bar I., Bernier B., Trujillo C., Raynaud A., and Meyer G. Reelin expression during embryonic brain development in lacertilian lizards. J Comp Neurol 414 (1999) 533-550
47. Goldman S.A., and Nottebohm F. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci U S A 80 (1983) 2390-2394
48. Guidotti A., Auta J., Davis J.M., Di-Giorgi-Gerevini V., Dwivedi Y., Grayson D.R., Impagnatiello F., Pandey G., Pesold C., Sharma R., Uzunov D., and Costa E. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 57 (2000) 1061-1069
49. Heng J.I., Moonen G., and Nguyen L. Neurotransmitters regulate cell migration in the telencephalon. Eur J Neurosci 26 (2007) 537-546
50. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., and Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 26 (2000) 93-96
51. Ikeda Y., and Terashima T. Expression of reelin, the gene responsible for the reeler mutation, in embryonic development and adulthood in the mouse. Dev Dyn 210 (1997) 157-172
52. Jarvis E.D., Gunturkun O., Bruce L., Csillag A., Karten H., Kuenzel W., Medina L., Paxinos G., Perkel D.J., Shimizu T., Striedter G., Wild J.M., Ball G.F., Dugas-Ford J., Durand S.E., Hough G.E., Husband S., Kubikova L., Lee D.W., Mello C.V., Powers A., Siang C., Smulders T.V., Wada K., White S.A., Yamamoto K., Yu J., Reiner A., and Butler A.B. Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6 (2005) 151-159
53. Johnson F., Sablan M.M., and Bottjer S.W. Topographic organization of a forebrain pathway involved with vocal learning in zebra finches. J Comp Neurol 358 (1995) 260-278
54. Kirn J., O'Loughlin B., Kasparian S., and Nottebohm F. Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc Natl Acad Sci U S A 91 (1994) 7844-7848
55. Kirn J.R., and Nottebohm F. Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci 13 (1993) 1654-1663
56. Li X., Wang X.J., Tannenhauser J., Podell S., Mukherjee P., Hertel M., Biane J., Masuda S., Nottebohm F., and Gaasterland T. Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc Natl Acad Sci U S A 104 (2007) 6834-6839
57. Ling C.Y., Zuo M.X., Alvarez-Buylla A., and Cheng M.F. Neurogenesis in juvenile and adult ring doves. J Comp Neurol 379 (1997) 300-312
58. Lipkind D., Nottebohm F., Rado R., and Barnea A. Social change affects the survival of new neurons in the forebrain of adult songbirds. Behav Brain Res 133 (2002) 31-43
59. Martìnez-Cerdeño V., and Clascà F. Reelin immunoreactivity in the adult neocortex: a comparative study in rodents, carnivores, and non-human primates. Brain Res Bull 57 (2002) 485-488
60. Matsuzaki H., Minabe Y., Nakamura K., Suzuki K., Iwata Y., Sekine Y., Tsuchiya K.J., Sugihara G., Suda S., Takei N., Nakahara D., Hashimoto K., Nairn A.C., Mori N., and Sato K. Disruption of reelin signaling attenuates methamphetamine-induced hyperlocomotion. Eur J Neurosci 25 (2007) 3376-3384
61. Mello C.V., Vates G.E., Okuhata S., and Nottebohm F. Descending auditory pathways in the adult male zebra finch (Taeniopygia guttata). J Comp Neurol 395 (1998) 137-160
62. Nicholls T.J., and Storey C.R. The effect of duration of the daily photoperiod on recovery of photosensitivity in photorefractory canaries (Serinus canarius). Gen Comp Endocrinol 31 (1977) 72-74
63. Niu S., Renfro A., Quattrocchi C.C., Sheldon M., and D'Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41 (2004) 71-84
64. Nixdorf-Bergweiler BE, Bischof H-J (2006) A stereotaxic atlas of the brain of the zebra finch, Taeniopygia guttata, with special emphasis on telencephalic visual and song system nuclei in transverse and sagittal sections. http://www.ncbi.nlm.gov/books/bv.fgci?rid=alas.
65. Nottebohm F. Brain pathways for vocal learning in birds: A review of the first 10 years. In: Sprague J.M., and Epstein A.N. (Eds). Progress in psychobiology and physiological psychology Vol. 9 (1980), Academic Press, New York 85-214
66. Nottebohm F. Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res 189 (1980) 429-436
67. Nottebohm F. A brain for all seasons: Cyclical anatomical changes in song-control nuclei of the canary brain. Science 214 (1981) 1368-1370
68. Nottebohm F. Neuronal replacement in adulthood. Ann N Y Acad Sci 457 (1985) 143-161
69. Nottebohm F., Kelley D.B., and Paton J.A. Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol 207 (1982) 344-357
70. Nottebohm F., Stokes T.M., and Leonard C.M. Central control of song in the canary, Serinus canarius. J Comp Neurol 165 (1976) 457-486
71. Nottebohm F. The neural basis of birdsong. PLoS Biol 3 (2005) e164
72. Oka K., Ishimura-Oka K., Chu M.J., Sullivan M., Krushkal J., Li W.H., and Chan L. Mouse very-low-density-lipoprotein receptor (VLDLR) cDNA cloning, tissue-specific expression and evolutionary relationship with the low-density-lipoprotein receptor. Eur J Biochem 224 (1994) 975-982
73. Okuhata S., and Saito N. Synaptic connections of thalamo-cerebelar vocal control nuclei of the canary. Brain Res Bull 18 (1987) 35-44
74. Pappas G.D., Kriho V., and Pesold C. Reelin in the extracellular matrix and dendritic spines of the cortex and hippocampus: a comparison between wild type and heterozygous reeler mice by immunoelectron microscopy. J Neurocytol 30 (2001) 413-425
75. Paton J.A., and Nottebohm F.N. Neurons generated in the adult brain are recruited into functional circuits. Science 225 (1984) 1046-1048
76. Pearlman A.L., and Sheppard A.M. Extracellular matrix in early cortical development. Prog Brain Res 108 (1996) 117-134
77. Perez-Garcia C.G., Gonzalez-Delgado F.J., Suarez-Sola M.L., Castro-Fuentes R., Martin-Trujillo J.M., Ferres-Torres R., and Meyer G. Reelin-immunoreactive neurons in the adult vertebrate pallium. J Chem Neuroanat 21 (2001) 41-51
78. Petit-Turcotte C., Aumont N., Beffert U., Dea D., Herz J., and Poirier J. The apoE receptor apoER2 is involved in the maintenance of efficient synaptic plasticity. Neurobiol Aging 26 (2005) 195-206
79. Pulido J.S., Sugaya I., Comstock J., and Sugaya K. Reelin expression is upregulated following ocular tissue injury. Graefes Arch Clin Exp Ophthalmol 245 (2007) 889-893
80. Qiu S., Zhao L.F., Korwek K.M., and Weeber E.J. Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus. J Neurosci 26 (2006) 12943-12955
81. Reiner A.D., Perkel J., Bruce L., Butler A., Csillag A., Kuenzel W., Medina L., Paxinos G., Shimizu T., Striedter G., Wild M., Ball G.F., Durand S., Güntürkün O., Lee D.W., Mello C.V., White S.A., Hough G., Kubikova L., Smulders T.V., Wada K., Dugas-Ford J., Husband S., Yamamoto K., Yu J., Siang C., and Jarvis E.D. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473 (2004) 377-414
82. Ryan S., and Arnold A.P. Evidence for cholinergic participation in the control of bird song: acetylcholinesterase distribution and muscarinic receptor autoradiography in the zebra finch brain. J Comp Neurol 202 (1981) 211-219
83. Sartor J.J., Balthazart J., and Ball G.F. Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria). Horm Behav 47 (2005) 467-476
84. Schiffmann S.N., Bernier B., and Goffinet A.M. Reelin mRNA expression during mouse brain development. Eur J Neurosci 9 (1997) 1055-1071
85. Sheng M., and Greenberg M.E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4 (1990) 477-485
86. Smalheiser N.R., Costa E., Guidotti A., Impagnatiello F., Auta J., Lacor P., Kriho V., and Pappas G.D. Expression of reelin in adult mammalian blood, liver, pituitary pars intermedia and adrenal chromaffin cells. Proc Natl Acad Sci U S A 97 (2000) 1281-1289
87. Stokes T.M., Leonard C.M., and Nottebohm F. The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J Comp Neurol 156 (1974) 337-374
88. Thompson C.K., and Brenowitz E.A. Seasonal change in neuron size and spacing but not neuronal recruitment in a basal ganglia nucleus in the avian song control system. J Comp Neurol 481 (2005) 276-283
89. Tissir F., and Goffinet A.M. Reelin and brain development. Nat Rev Neurosci 4 (2003) 496-505
90. Tramontin A.D., and Brenowitz E.A. Seasonal plasticity in the adult brain. Trends Neurosci 23 (2000) 251-258
91. Vates G.E., Broome B.M., Mello C.V., and Nottebohm F. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata). J Comp Neurol 366 (1996) 613-642
92. Voigt C., Ball G.F., and Balthazart J. Neuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain. J Chem Neuroanat 33 (2007) 75-86
93. Wada K., Sakaguchi H., Jarvis E.D., and Hagiwara M. Differential expression of glutamate receptors in avian neural pathways for learned vocalization. J Comp Neurol 476 (2004) 44-64
94. Weeber E.J., Beffert U., Jones C., Christian J.M., Forster E., Sweatt J.D., and Herz J. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277 (2002) 39944-39952
95. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., and Greenberg M.E. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A 98 (2001) 11024-11031
96. Whitfield Jr. H.J., Brady L.S., Smith M.A., Mamalaki E., Fox R.J., and Herkenham M. Optimization of cRNA probe in situ hybridization methodology for localization of glucocorticoid receptor mRNA in rat brain: a detailed protocol. Cell Mol Neurobiol 10 (1990) 145-157
97. Williams H., and Vicario D.S. Temporal patterning of song production: Participation of nucleus uvaeformis of the thalamus. J Neurobiol 24 (1993) 903-912
98. Yu A.C., and Margoliash D. Temporal hierarchical control of singing in birds. Science 273 (1996) 1871-1875