Zic1 and Zic3 regulate medial forebrain development through expansion of neuronal progenitors

Journal of Neuroscience

Volumn 27, Issue 20, 2007, Pages 5461-5473

  Inoue, Takashi ^a   Ota, Maya ^a   Ogawa, Miyuki ^a   Mikoshiba, Katsuhiko ^a   Aruga, Jun ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Forebrain development; Neuronal differentiation; Neuronal progenitors; Olfactory bulb; Septum; Zic

Indexed keywords

NEUROPEPTIDE; PROTEIN ZIC1; PROTEIN ZIC3; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CYCLE; CELL DIFFERENTIATION; CHOROID PLEXUS; FOREBRAIN; HIPPOCAMPUS; HYPOPLASIA; MOUSE; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPTUM PELLUCIDUM;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PREGNANCY; PROSENCEPHALON; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 34249106757     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4046-06.2007     Document Type: Article

References (69)

1. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997a) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
2. Anderson SA, Qiu M, Bulfore A, Eisenstat DD, Meneses, Pederson S, Rubenstein JL (1997b) Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19:27-37.
3. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
4. Aruga J (2004) The role of Zic genes in neural development. Mol Cell Neurosci 26:205-221.
5. Aruga J, Minowa O, Yaginuma H, Kuno J, Nagai T, Noda T, Mikoshiba K (1998) Mouse Zic1 is involved in cerebellar development. J Neurosci 18:284-293.
6. Aruga J, Inoue T, Hoshino J, Mikoshiba K (2002a) Zic2 controls cerebellar development in cooperation with Zic1. J Neurosci 22:218-225.
7. Aruga J, Tohmonda T, Homma S, Mikoshiba K (2002b) Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev Biol 244:329-341.
8. Aruga J, Ogura H, Shutoh F, Ogawa M, Franke B, Nagao S, Mikoshiba K (2004) Locomotor and oculomotor impairment associated with cerebellar dysgenesis in Zic3-deficient (Bent tail) mutant mice. Eur J Neurosci 20:2159-2167.
9. Aruga J, Kamiya A, Takahashi H, Fujimi TJ, Shimizu Y, Ohkawa K, Yazawa S, Umesono Y, Noguchi H, Shimizu T, Saitou N, Mikoshiba K., Sakaki Y, Agata K, Toyoda A (2006) A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity. Genomics 87:783-792.
10. Baker H, Liu N, Chun HS, Saino S, Berlin R, Volpe B, Son JH (2001) Phenotypic differentiation during migration of dopaminergic progenitor cells to the olfactory bulb. J Neurosci 21:8505-8513.
11. Bayer SA (1980) Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 190:87-114.
12. Bayer SA, Altman J (2004) Development of the telencephalon: neural stem cells, neurogenesis, and neuronal migration. In: The rat nervous system (Paxinos G, ed), pp 27-75. San Diego: Academic.
13. Behar T, Ma W, Hudson L, Barker JL (1994) Analysis of the anatomical distribution of GAD67 mRNA encoding truncated glutamic acid decarboxylase proteins in the embryonic rat brain. Brain Res Dev Brain Res 77:77-87.
14. Brown SA, Warburton D, Brown LY, Yu CY, Roeder ER, Stengel-Rutkowski S, Hennekam RC, Muenke M (1998) Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet 20:180-183.
15. Burgoyne RD, Cambray-Deakin MA, Lewis SA, Sarkar S, Cowan NJ (1988) Differential distribution of beta-tubulin isotypes in cerebellum. EMBO J 7:2311-2319.
16. Carrel T, Purandare SM, Harrison W, Elder F, Fox T, Casey B, Herman GE (2000) The X-linked mouse mutation Bent tail is associated with a deletion of the Zic3 locus. Hum Mol Genet 9:1937-1942.
17. Casarosa S, Fode C, Guillemot F (1999) Mash1 regulates neurogenesis in the ventral telencephalon. Development 126:525-534.
18. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369.
19. Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR, Ledent C, Vanderhaeghen P (2005) Ephrin signalling control brain size by regulating apoptosis of neural progenitors. Nature 435:1244-1250.
20. DiSalvo CV, Zhang D, Jacobberger JW (1995) Regulation of NIH-3T3 cell G1 phase transit by serum during exponential growth. Cell Prolif 28:511-524.
21. Dwyer ND, O'Leary DD (2001) Tbr1 conducts the orchestration of early cortical development. Neuron 29:309-311.
22. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas J, Puelles L, Rubenstein JL (1999) DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414:217-237.
23. Elms P, Scurry A, Davies J, Willoughby C, Hacker T, Bogani D, Arkell R (2004) Overlapping and distinct expression domains of Zic2 and Zic3 during mouse gastrulation. Gene Expr Patterns 4:505-511.
24. Faedo A, Ficara F, Ghiani M, Aiuti A, Rubenstein JL, Bulfore A (2002) Developmental expression of the T-box transcription factor T-bet/Tbx21 during mouse embryogenesis. Mech Dev 116:157-160.
25. Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67-80.
26. Franke B, Klootwijk R, Hekking JW, de Boer RT, ten Donkelaar HJ, Mariman EC, van Straaten HW (2003) Analysis of embryonic phenotype of Bent tail, a mouse model for X-linked neural tube defects. Anat Embryol 207:255-262.
27. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212.
28. Garber ED (1952) "Bent tail," a dominant, sex-linked mutation in the mouse. Proc Natl Acad Sci USA 38:876-879.
29. Grinberg I, Millen KJ (2005) The ZIC gene family in development and disease. Clin Genet 67:290-296.
30. 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.
31. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 124:2315-2325.
32. Guillemot F (2005) Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol 17:639-647.
33. Hinds JW (1968a) Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287-304.
34. Hinds JW (1968b) Autoradiographic study of histogenesis in the mouse olfactory bulb. II. Cell proliferation and migration. J Comp Neurol 134:305-322.
35. Hinds JW (1972a) Early neuron differentiation in the mouse olfactory bulb. I. Light microscopy. J Comp Neurol 146:233-252.
36. Hinds JW (1972b) Early neuron differentiation in the mouse olfactory bulb. I. Electron microscopy. J Comp Neurol 146:253-276.
37. Inoue T, Hatayama M, Tohmonda T, Itohara S, Aruga J, Mikoshiba K (2004) Mouse Zic5 deficiency results in neural tube defects and hypoplasia of cephalic neural crest derivatives. Dev Biol 270:146-162.
38. Inoue T, Ota M, Mikoshiba K, Aruga J (2007) Zic2 and Zic3 synergistically control neurulation and segmentation of paraxial mesoderm in mouse embryo. Dev Biol, in press.
39. Klootwijk R, Franke B, van der Zee CE, de Boer RT, Wilms W, Hol FA, Mariman EC (2000) A deletion encompassing Zic3 in bent tail, a mouse model for X-linked neural tube defects. Hum Mol Genet 9:1615-1622.
40. Kosaka K, Aika Y, Toida K, Heizmann CW, Hunziker W, Jacobowitz DM, Nagatsu I, Streit P, Visser TJ, Kosaka T (1995) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res 23:73-88.
41. Lee SM, Tole S, Grove E, McMahon AP (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127:457-467.
42. Long JE, Garel S, Depew MJ, Tobet S, Rubenstein JLR (2003) DLX5 regulates development of peripheral and central components of the olfactory system. J Neurosci 23:568-578.
43. Luskin MB (1998) Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J Neurobiol 36:221-233.
44. Marin O, Rubenstein JL (2001) A long remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790.
45. Mizugishi K, Aruga J, Nakata K, Mikoshiba K (2001) Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J Biol Chem 276:2180-2188.
46. Nagai T, Aruga J, Takada S, Gunther T, Sporle R, Schughart K, Mikoshiba K (1997) The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev Biol 182:299-313.
47. Nagai T, Aruga J, Minowa O, Sugimoto T, Ohno Y, Noda T, Mikoshiba K (2000) Zic2 regulates the kinetics of neurulation. Proc Natl Acad Sci USA 97:1618-1623.
48. Nakahira E, Kagawa T, Shimizu T, Goulding MD, Ikenaka K (2006) Direct evidence that ventral forebrain cells migrate to the cortex and contribute to the generation of cortical myelinating oligodendrocytes. Dev Biol 291:123-131.
49. Nguyen Ba-Charvet KT, Brose K, Marillat V, Kidd T, Goodman CS, Tessier-Lavigne M, Sotelo C, Chedotal A (1999) Slit2-mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22:463-473.
50. Nieto M, Schuurmans C, Britz O, Guillemot F (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29:401-413.
51. Niwa H, Ymamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants. Gene 108:193-199.
52. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R (1999) Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J 18:2196-2207.
53. Ohtsuka T, Sakamoto M, Guillemot F, Kageyama R (2001) Roles of basic helix-loop-helix genes Hes1 and Hes5 in expression of neural stem cells of the developing brain. J Biol Chem 276:30467-30474.
54. Purandare SM, Ware SM, Kwan KM, Gebbia M, Bassi MT, Deng JM, Vogel H, Behringer RR, Belmont JW, Casey B (2002) A complex syndrome of left-right axis, central nervous system and axial skeleton defects in Zic3 mutant mice. Development 129:2293-2302.
55. Qiu M, Bulfone A, Martinez S, Meneses JJ, Shimamura K, Pedersen RA, Rubenstein JL (1995) Null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes Dev 9:2523-2538.
56. Rubenstein JL, Shimamura K, Martinez S, Puelles L (1998) Regionalization of the prosencephalic neural plate. Annu Rev Neurosci 21:445-477.
57. Saito T, Nakatsuji N (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240:237-246.
58. Soria JM, Taglialatela P, Gil-Perotin S, Galli R, Gritti A, Verdugo JM, Bertuzzi S (2004) Defective postnatal neurogenesis and disorganization of the rostral migratory stream in absence of the Vax1 homeobox gene. J Neurosci 24:11171-11181.
59. Stanfield BB, CowanWM (1979) The development of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:423-460.
60. Stanfield BB, Cowan WM (1988) The development of the hippocampal region. Cereb Cortex 7:91-131.
61. Stenman J, Toresson H, Campbell K (2003) Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167-174.
62. St. John JA, Clarris HJ, McKeown S, Royal S, Key B (2003) Sorting and convergence of primary axons are independent of the olfactory bulb. J Comp Neurol 464:131-140.
63. Sussel L, Marin O, Kimura S, Rubenstein JL (1999) Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallium into the striatum. Development 126:3359-3370.
64. Taglialatela P, Soria JM, Caironi V, Moiana A, Bertuzzi S (2004) Compromised generation of GABAergic interneurons in the brains of Vax1-/- mice. Development 131:4239-4249.
65. Takada S, Stark KL, Shea MJ, Vassileva G, McMahon JA, McMahon AP (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8:174-189.
66. Toida K, Kosaka K, Aika Y, Kosaka T (2000) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb-IV. Intraglomerular synapses of tyrosine hydroxylase- immunoreactive neurons. Neuroscience 101:11-17.
67. Turner DL, Weintraub H (1994) Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to neural fate. Genes Dev 15:1434-1447.
68. Yoshihara S, Omichi K, Yanazawa K, Kitamura K, Yoshihara Y (2005) Arx homeobox gene is essential for development of mouse olfactory system. Development 132:751-762.
69. Zaki PA, Quinn JC, Price DJ (2003) Mouse models of telencephalic development. Curr Opin Genet Dev 13:423-437.