Differential gene expression in the developing lateral geniculate nucleus and medial geniculate nucleus reveals novel roles for Zic4 and Foxp2 in visual and auditory pathway development

Journal of Neuroscience

Volumn 29, Issue 43, 2009, Pages 13672-13683

  Horng, Sam ^a   Kreiman, Gabriel ^b   Ellsworth, Charlene ^a   Page, Damon ^a   Blank, Marissa ^c   Millen, Kathleen ^c   Sur, Mriganka ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP2; TRANSCRIPTION FACTOR ZIC4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; BRAIN DEVELOPMENT; CONTROLLED STUDY; GENE EXPRESSION; GENICULATE NUCLEUS; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; MOUSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; THALAMUS; VISUAL SYSTEM;

ANIMALS; ANIMALS, NEWBORN; AUDITORY PATHWAYS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; GENICULATE BODIES; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRESSOR PROTEINS; RETINA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THALAMUS; TRANSCRIPTION FACTORS; VISUAL PATHWAYS;

EID: 70350532596     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2127-09.2009     Document Type: Article

References (70)

1. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45:207-221. (Pubitemid 40136579)
2. Aruga J (2004) The role of Zic genes in neural development. Mol Cell Neurosci 26:205-221.
3. Bengel D, Murphy DL, Andrews AM, Wichems CH, Feltner D, Heils A, Mössner R, Westphal H, Lesch KP (1998) Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine ("Ecstasy") in serotonin transporter-deficient mice. Mol Pharmacol 53:649-655.
4. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193. (Pubitemid 36181903)
5. Bonnin A, Torii M, Wang L, Rakic P, Levitt P (2007) Serotonin modulates the response of embryonic thalamocortical axons to netrin-1. Nat Neurosci 10:588-597. (Pubitemid 46652450)
6. Braissant O, Wahli W (1998) A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1:10-16.
7. Braun MM, Etheridge A, Bernard A, Robertson CP, Roelink H (2003) Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development 130:5579-5587. (Pubitemid 37540835)
8. Brunet I, Weinl C, Piper M, Trembleau A, Volovitch M, Harris W, Prochiantz A, Holt C (2005) The transcription factor Engrailed-2 guides retinal axons. Nature 438:94-98. (Pubitemid 41599826)
9. Dehay C, Giroud P, Berland M, Smart I, Kennedy H (1993) Modulation of the cell cycle contributes to the parcellation of the primate visual cortex. Nature 366:464-466. (Pubitemid 24013879)
10. Dehay C, Savatier P, Cortay V, Kennedy H (2001) Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons. J Neurosci 21:201-214. (Pubitemid 32098743)
11. Figdor MC, Stern CD (1993) Segmental organization of embryonic diencephalon. Nature 363:630-634.
12. Gaston-Massuet C, Henderson DJ, Greene ND, Copp AJ (2005) Zic4, a zinc-finger transcription factor, is expressed in the developing mouse nervous system. Dev Dyn 233:1110-1115.
13. Grinberg I, Northrup H, Ardinger H, Prasad C, Dobyns WB, Millen KJ (2004) Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation. Nat Genet 36:1053-1055. (Pubitemid 41184463)
14. Grove EA, Fukuchi-Shimogori T (2003) Generating the cerebral cortical area map. Annu Rev Neurosci 26:355-380.
15. Guido W (2008) Refinement of the retinogeniculate pathway. J Physiol 586:4357-4362.
16. Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T, Jarvis ED, Scharff C (2004) FoxP2 expression in avian vocal learners and non-learners. J Neurosci 24:3164-3175. (Pubitemid 38451883)
17. Haesler S, Rochefort C, Georgi B, Licznerski P, Osten P, Scharff C (2007) Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus area X. PLoS Biol 5:e321.
18. Harrington SC, Simari RD, Conover CA (2007) Genetic deletion of pregnancy-associated plasma protein-A is associated with resistance to atherosclerotic lesion development in apolipoprotein E-deficient mice challenged with a high-fat diet. Circ Res 100:1696-1702.
19. Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB, Ullian EM, Baccus SA, Barres BA (2008) Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59:425-438.
20. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15.
21. Jones EG (2007) The thalamus, Ed 2. New York: Plenum.
22. Kaneko M, Stellwagen D, Malenka RC, Stryker MP (2008) Tumor necrosis factor-alpha mediates one component of competitive, experiencedependent plasticity in developing visual cortex. Neuron 58:673-680. (Pubitemid 351778470)
23. Kataoka A, Shimogori T (2008) Fgf8 controls regional identity in the developing thalamus. Development 135:2873-2881.
24. Kawasaki H, Crowley JC, Livesey FJ, Katz LC (2004) Molecular organization of the ferret visual thalamus. J Neurosci 24:9962-9970. (Pubitemid 39463577)
25. Kiecker C, Lumsden A (2004) Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat Neurosci 7:1242-1249. (Pubitemid 39426244)
26. Kiecker C, Lumsden A (2005) Compartments and their boundaries in vertebrate brain development. Nat Rev Neurosci 6:553-564. (Pubitemid 40942822)
27. Kilic U, Kilic E, Järve A, Guo Z, Spudich A, Bieber K, Barzena U, Bassetti CL, Marti HH, Hermann DM (2006) Human vascular endothelial growth factor protects axotomized retinal ganglion cells in vivo by activating ERK-1/2 and Akt pathways. J Neurosci 26:12439-12446.
28. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR (2008) Molecular identification of a retinal cell type that responds to upward motion. Nature 452:478-482.
29. Kitamura K, Miura H, Yanazawa M, Miyashita T, Kato K. (1997) Expression patterns of Brx1 (Rieg gene), Sonic hedgehog, Nkx2.2, Dlx1 and Arx during zona limitans intrathalamica and embryonic ventral lateral geniculate nuclear formation. Mech Dev 67:83-96.
30. Leamey CA, Glendining KA, Kreiman G, Kang ND, Wang KH, Fassler R, Sawatari A, Tonegawa S, Sur M (2008) Differential gene expression between sensory neocortical areas: potential roles for Ten-m3 and Bcl6 in patterning visual and somatosensory pathways. Cereb Cortex 18:53-66. (Pubitemid 350233052)
31. Lim Y, Golden JA (2007) Patterning the developing diencephalon. Brain Res Rev 53:17-26.
32. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, Dehay C (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47:353-364. (Pubitemid 41073877)
33. Lyckman AW, Jhaveri S, Feldheim DA, Vanderhaeghen P, Flanagan JG, Sur M (2001) Enhanced plasticity of retinothalamic projections in an ephrin- A2/A5 double mutant. J Neurosci 21:7684-7690. (Pubitemid 32904967)
34. Lyckman AW, Horng S, Leamey CA, Tropea D, Watakabe A, Van Wart A, McCurry C, Yamamori T, Sur M (2008) Gene expression patterns in visual cortex during the critical period: synaptic stabilization and reversal by visual deprivation. Proc Natl Acad Sci U S A 105:9409-9414.
35. Miyashita-Lin EM, Hevner R, Wassarman KM, Martinez S, Rubenstein JL. (1999) Early neocortical regionalization in the absence of thalamic innervation. Science 285:906-909. (Pubitemid 29381994)
36. Murray KD, Choudary PV, Jones EG (2007) Nucleus-and cell-specific gene expression in monkey thalamus. Proc Natl Acad Sci U S A 104:1989-1994.
37. Murray KD, Rubin CM, Jones EG, Chalupa LM (2008) Molecular correlates of laminar differences in the macaque dorsal lateral geniculate nucleus. J Neurosci 28:12010-120122.
38. Nakagawa Y, O'Leary DD (2001) Combinatorial expression patterns of LIM-homeodomain and other regulatory genes parcellate developing thalamus. J Neurosci 21:2711-2725. (Pubitemid 32298213)
39. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, She H, Michaud N, Hafezi-Moghadam A, Miller JW, Benowitz LI (2006) Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci 26:12633-12641.
40. Newton JR, Ellsworth C, Miyakawa T, Tonegawa S, Sur M (2004) Acceleration of visually cued conditioned fear through the auditory pathway. Nat Neurosci 7:968-973. (Pubitemid 39129506)
41. Nishijima K, Ng YS, Zhong L, Bradley J, Schubert W, Jo N, Akita J, Samuelsson SJ, Robinson GS, Adamis AP, Shima DT (2007) Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neuroprotectant during the adaptive response to ischemic injury. Am J Pathol 171:53-67.
42. O'Leary DD, Nakagawa Y (2002) Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex. Curr Opin Neurobiol 12:14-25.
43. Pak W, Hindges R, Lim YS, Pfaff SL, O'Leary DD (2004) Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 119:567-578. (Pubitemid 39482355)
44. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, Xu B, Connolly L, Kramvis I, Sahin M, He Z (2008) Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322:963-966.
45. Pfeiffenberger C, Cutforth T, Woods G, Yamada J, Rentería RC, Copenhagen DR, Flanagan JG, Feldheim DA (2005) Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping. Nat Neurosci 8:1022-1027. (Pubitemid 41061512)
46. Ragsdale CW, Grove EA (2001) Patterning the mammalian cerebral cortex. Curr Opin Neurobiol 11:50-58.
47. Rousso DL, Gaber ZB, Wellik D, Morrisey EE, Novitch BG (2008) Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 59:226-240. (Pubitemid 352033689)
48. Salichon N, Gaspar P, Upton AL, Picaud S, Hanoun N, Hamon M, De Maeyer E, Murphy DL, Mossner R, Lesch KP, Hen R, Seif I (2001) Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase a and 5-ht transporter knock-out mice. J Neurosci 21:884-896.
49. Schneider GE (1973) Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behav Evol 8:73-109.
50. Sharma J, Angelucci A, Sur M (2000) Induction of visual orientation modules in auditory cortex. Nature 404:841-847. (Pubitemid 30230329)
51. Shimogori T, Banuchi V, Ng HY, Strauss JB, Grove EA (2004) Embryonic signaling centers expressing BMP, WNT and FGF proteins interact to pattern the cerebral cortex. Development 131:5639-5647.
52. Shu W, Cho JY, Jiang Y, Zhang M, Weisz D, Elder GA, Schmeidler J, De Gasperi R, Sosa MA, Rabidou D, Santucci AC, Perl D, Morrisey E, Buxbaum JD (2005) Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc Natl Acad Sci U S A 102:9643-9648.
53. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131:1164-1178. (Pubitemid 350235022)
54. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545-15550. (Pubitemid 41528093)
55. Sun T, Patoine C, Abu-Khalil A, Visvader J, Sum E, Cherry TJ, Orkin SH, Geschwind DH, Walsh CA (2005) Early asymmetry of gene transcription in embryonic human left and right cerebral cortex. Science 308: 1794-1798. (Pubitemid 40848009)
56. Sur M, Rubenstein JL (2005) Patterning and plasticity of the cerebral cortex. Science 310:805-810.
57. Sur M, Garraghty PE, Roe AW (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science 242:1437-1441.
58. Szabó NE, Zhao T, Zhou X, Alvarez-Bolado G (2009) The role of Sonic hedgehog of neural origin in thalamic differentiation in the mouse. J Neurosci 29:2453-2466.
59. Teramitsu I, White SA (2006) FoxP2 regulation during undirected singing in adult songbirds. J Neurosci 26:7390-7394. (Pubitemid 44315207)
60. Tilford CA, Siemers NO (2009) Gene set enrichment analysis. Methods Mol Biol 563:99-121.
61. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98:5116-5121.
62. Tuttle R, Braisted JE, Richards LJ, O'Leary DD (1998) Retinal axon guidance by region-specific cues in diencephalons. Development 125:791-801. (Pubitemid 28142822)
63. Upton AL, Salichon N, Lebrand C, Ravary A, Blakely R, Seif I, Gaspar P (1999) Excess of serotonin (5-HT) alters the segregation of ispilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: possible role of 5-HT uptake in retinal ganglion cells during development. J Neurosci 19:7007-7024.
64. Upton AL, Ravary A, Salichon N, Moessner R, Lesch KP, Hen R, Seif I, Gaspar P (2002) Lack of 5-HT(1B) receptor and of serotonin transporter have different effects on the segregation of retinal axons in the lateral geniculate nucleus compared to the superior colliculus. Neuroscience 111:597-610. (Pubitemid 34521898)
65. Vargha-Khadem F, Gadian DG, Copp A, Mishkin M (2005) FOXP2 and the neuroanatomy of speech and language. Nat Rev Neurosci 6:131-138.
66. Vernes SC, Nicod J, Elahi FM, Coventry JA, Kenny N, Coupe AM, Bird LE, Davies KE, Fisher SE (2006) Functional genetic analysis of mutations implicated in a human speech and language disorder. Hum Mol Genet 15:3154-3167. (Pubitemid 44605496)
67. von Melchner L, Pallas SL, Sur M (2000) Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404:871-876.
68. Vue TY, Aaker J, Taniguchi A, Kazemzadeh C, Skidmore JM, Martin DM, Martin JF, Treier M, Nakagawa Y (2007) Characterization of progenitor domains in the developing mouse thalamus. J Comp Neurol 505:73-91. (Pubitemid 350068231)
69. Vue TY, Bluske K, Alishahi A, Yang LL, Koyano-Nakagawa N, Novitch B, Nakagawa Y (2009) Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice. J Neurosci 29:4484-4497.
70. Zhou CJ, Pinson KI, Pleasure SJ (2004) Severe defects in dorsal thalamic development in low-density lipoprotein receptor-related protein-6 mutants. J Neurosci 24:7632-7639.