Analysis of early ventral telencephalic defects in mice lacking functional Gli3 protein

Journal of Comparative Neurology

Volumn 512, Issue 5, 2009, Pages 613-627

  Yu, Tian ^a,b   Fotaki, Vassiliki ^a   Mason, John O ^a   Price, David J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Development; Diencephalon; Forebrain; Gli3; Mutant; Ventral telencephalon

Indexed keywords

TRANSCRIPTION FACTOR GLI3; BIOLOGICAL MARKER; GLI3 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; NERVE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN GROWTH; BRAIN NERVE CELL; BRAIN SIZE; CELL CYCLE; CELL FATE; CONTROLLED STUDY; DIENCEPHALON; EMBRYO; FOREBRAIN; MOUSE; MUTANT; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN EXPRESSION; TELENCEPHALON; WILD TYPE; ANIMAL; ANIMAL EMBRYO; CBA MOUSE; CELL DEATH; CELL DIFFERENTIATION; CONGENITAL MALFORMATION; GENETICS; GESTATIONAL AGE; HISTOLOGY; HUMAN; METABOLISM; MUTATION; NICK END LABELING; PHYSIOLOGY; THREE DIMENSIONAL IMAGING;

ANIMALS; BIOLOGICAL MARKERS; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; EMBRYO, MAMMALIAN; GESTATIONAL AGE; HUMANS; IMAGING, THREE-DIMENSIONAL; IN SITU NICK-END LABELING; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED CBA; MUTATION; NERVE TISSUE PROTEINS; TELENCEPHALON;

EID: 59049088067     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21918     Document Type: Article

References (91)

1. Aoto K, Nishimura T, Eto K, Motoyama J. 2002. Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev Biol 251:320-332.
2. Aza-Blanc P, Lin HY, Ruiz i Altaba A, Kornberg TB. 2000. Expression of the vertebrate Gli proteins in Drosophila reveals a distribution of activator and repressor activities. Development 127:4293-4301.
3. Bai CB, Stephen D, Joyner AL. 2004. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev Cell 6:103-115.
4. Banerjee A, Roach MC, Trcka P, Luduena RF. 1990. Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of betatubulin. J Biol Chem 265:1794-1799.
5. Bulfone A, Kim HJ, Puelles L, Porteus MH, Grippo JF, Rubenstein JL. 1993. The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mech Dev 40:129-140.
6. Buscher D, Bosse B, Heymer J, Ruther U. 1997. Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Mech Dev 62:175-182.
7. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383:407-413.
8. Crossley PH, Martinez S, Ohkubo Y, Rubenstein JL. 2001. Coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience 108:183-206.
9. Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP. 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417-1430.
10. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, 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.
11. Ericson J, Thor S, Edlund T, Jessell TM, Yamada T. 1992. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256:1555-1560.
12. Ericson J, Muhr J, Placzek M, Lints T, Jessell TM, Edlund T. 1995. Sonic hedgehog induces the differentiation of ventral forebrain neurons: a common signal for ventral patterning within the neural tube. Cell 81: 747-756.
13. Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, van Heyningen V, Jessell TM, Briscoe J. 1997. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90:169-180.
14. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O. 2007. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 27:9682-9695.
15. Fotaki V, Yu T, Zaki PA, Mason JO, Price DJ. 2006. Abnormal positioning of diencephalic cell types in neocortical tissue in the dorsal telencephalon of mice lacking functional Gli3. J Neurosci 26:9282-9292.
16. Fuccillo M, Rutlin M, Fishell G. 2006. Removal of Pax6 partially rescues the loss of ventral structures in Shh null mice. Cereb Cortex 16(Suppl 1):i96-102.
17. Furuta Y, Piston DW, Hogan BL. 1997. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212.
18. Garcia-Lopez M, Abellan A, Legaz I, Rubenstein JL, Puelles L, Medina L. 2008. Histogenic compartments of the mouse centromedial and extended amygdala based on gene expression patterns during development. J Comp Neurol 506:46-74.
19. Gokhan S, Marin-Husstege M, Yung SY, Fontanez D, Casaccia-Bonnefil P, Mehler MF. 2005. Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression. J Neurosci 25:8311-8321.
20. Gratzner HG. 1982. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science 218: 474-475.
21. 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 125: 2315-2325.
22. Guan W, Wang G, Scott SA, Condic ML. 2008. Shh influences cell number and the distribution of neuronal subtypes in dorsal root ganglia. Dev Biol 314:317-328.
23. Guillemot F, Joyner AL. 1993. Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech Dev 42:171-185.
24. Gulacsi A, Anderson SA. 2006. Shh maintains Nkx2.1 in the MGE by a Gli3-independent mechanism. Cereb Cortex 16(Suppl 1):i89-95.
25. Gunhaga L, Jessell TM, Edlund T. 2000. Sonic hedgehog signaling at gastrula stages specifies ventral telencephalic cells in the chick embryo. Development 127:3283-3293.
26. Gutin G, Fernandes M, Palazzolo L, Paek H, Yu K, Ornitz DM, McConnell SK, Hebert JM. 2006. FGF signalling generates ventral telencephalic cells independently of SHH. Development 133:2937-2946.
27. Hanashima C, Shen L, Li SC, Lai E. 2002. Brain factor-1 controls the proliferation and differentiation of neocortical progenitor cells through independent mechanisms. J Neurosci 22:6526-6536.
28. Hui CC, Joyner AL. 1993. A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat Genet 3:241-246.
29. Hui CC, Slusarski D, Platt KA, Holmgren R, Joyner AL. 1994. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev Biol 162:402-413.
30. Hynes M, Stone DM, Dowd M, Pitts-Meek S, Goddard A, Gurney A, Rosenthal A. 1997. Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron 19:15-26.
31. Ingham PW, McMahon AP. 2001. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15:3059-3087.
32. Johnson DR. 1967. Extra-toes: a new mutant gene causing multiple abnormalities in the mouse. J Embryol Exp Morphol 17:543-581.
33. Kawakami A, Kimura-Kawakami M, Nomura T, Fujisawa H. 1997. Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech Dev 66:119-130.
34. Kerr JF, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257.
35. Kuschel S, Ruther U, Theil T. 2003. A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon. Dev Biol 260:484-495.
36. Lee MK, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A. 1990. The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton 17:118-132.
37. Lee J, Platt KA, Censullo P, Ruiz i Altaba A. 1997. Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124:2537-2552.
38. Litingtung Y, Chiang C. 2000. Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat Neurosci 3:979-985.
39. Lo LC, Johnson JE, Wuenschell CW, Saito T, Anderson DJ. 1991. Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 5:1524-1537.
40. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH. 2000. Sonic hedgehog - regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25:317-329.
41. Marigo V, Johnson RL, Vortkamp A, Tabin CJ. 1996. Sonic hedgehog differentially regulates expression of GLI and GLI3 during limb development. Dev Biol 180:273-283.
42. Marklund M, Sjodal M, Beehler BC, Jessell TM, Edlund T, Gunhaga L. 2004. Retinoic acid signalling specifies intermediate character in the developing telencephalon. Development 131:4323-4332.
43. Marti E, Takada R, Bumcrot DA, Sasaki H, McMahon AP. 1995. Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121:2537-2547.
44. Martynoga B, Morrison H, Price DJ, Mason JO. 2005. Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol 283:113-127.
45. Mastick GS, Andrews GL. 2001. Pax6 regulates the identity of embryonic diencephalic neurons. Mol Cell Neurosci 17:190-207.
46. Mastick GS, Davis NM, Andrew GL, Easter SS Jr. 1997. Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain. Development 124:1985-1997.
47. Maynard TM, Jain MD, Balmer CW, LaMantia AS. 2002. High-resolution mapping of the Gli3 mutation extra-toes reveals a 51.5-kb deletion. Mamm Genome 13:58-61.
48. Oppenheim RW. 1991. Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
49. Parras CM, Hunt C, Sugimori M, Nakafuku M, Rowitch D, Guillemot F. 2007. The proneural gene Mash1 specifies an early population of telencephalic oligodendrocytes. J Neurosci 27:4233-4242.
50. Porteus MH, Bulfone A, Ciaranello RD, Rubenstein JL. 1991. Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron 7:221-229.
51. Porteus MH, Bulfone A, Liu JK, Puelles L, Lo LC, Rubenstein JL. 1994. DLX-2, MASH-1, and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J Neurosci 14(11 Pt 1):6370-6383.
52. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL. 2000. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424: 409-438.
53. Puelles E, Acampora D, Lacroix E, Signore M, Annino A, Tuorto F, Filosa S, Corte G, Wurst W, Ang SL, Simeone A. 2003. Otx dose-dependent integrated control of antero-posterior and dorso-ventral patterning of midbrain. Nat Neurosci 6:453-460.
54. Rallu M, Machold R, Gaiano N, Corbin JG, McMahon AP, Fishell G. 2002. Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and hedgehog signaling. Development 129:4963-4974.
55. Rash BG, Grove EA. 2007. Patterning the dorsal telencephalon: a role for sonic hedgehog? J Neurosci 27:11595-11603.
56. Ruiz i Altaba A. 1998. Combinatorial Gli gene function in floor plate and neuronal inductions by sonic hedgehog. Development 125:2203-2212.
57. Ruiz i Altaba A. 1999. Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 126:3205-3216.
58. Ruiz i Altaba A, Palma V, Dahmane N. 2002. Hedgehog-Gli signalling and the growth of the brain. Nat Rev Neurosci 3:24-33.
59. Ruppert JM, Vogelstein B, Arheden K, Kinzler KW. 1990. GLI3 encodes a 190-kilodalton protein with multiple regions of GLI similarity. Mol Cell Biol 10:5408-5415.
60. Schweitzer R, Vogan KJ, Tabin CJ. 2000. Similar expression and regulation of Gli2 and Gli3 in the chick limb bud. Mech Dev 98:171-174.
61. Sharpe J. 2003. Optical projection tomography as a new tool for studying embryo anatomy. J Anat 202:175-181.
62. Sharpe J, Ahlgren U, Perry P, Hill B, Ross A, Hecksher-Sorensen J, Baldock R, Davidson D. 2002. Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296:541-545.
63. Sheng HZ, Bertuzzi S, Chiang C, Shawlot W, Taira M, Dawid I, Westphal H. 1997. Expression of murine Lhx5 suggests a role in specifying the forebrain. Dev Dyn 208:266-277.
64. Shibui S, Hoshino T, Vanderlaan M, Gray JW. 1989. Double labeling with iodo-and bromodeoxyuridine for cell kinetics studies. J Histochem Cytochem 37:1007-1011.
65. Shimamura K, Hartigan DJ, Martinez S, Puelles L, Rubenstein JL. 1995. Longitudinal organization of the anterior neural plate and neural tube. Development 121:3923-3933.
66. Simeone A, Acampora D, Gulisano M, Stornaiuolo A, Boncinelli E. 1992. Nested expression domains of four homeobox genes in developing rostral brain. Nature 358:687-690.
67. Simeone A, Acampora D, Mallamaci A, Stornaiuolo A, D'Apice MR, Nigro V, Boncinelli E. 1993. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. Embo J 12:2735-2747.
68. Smith SM, Cartwright MM. 1997. Spatial visualization of apoptosis using a whole-mount in situ DNA end-labeling technique. Biotechniques 22: 832-834.
69. Stoykova A, Gruss P. 1994. Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J Neurosci 14(3 Pt 2): 1395-1412.
70. Stoykova A, Fritsch R, Walther C, Gruss P. 1996. Forebrain patterning defects in Small eye mutant mice. Development 122:3453-3465.
71. Stoykova A, Gotz M, Gruss P, Price J. 1997. Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124:3765-3777.
72. 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 pallidum into the striatum. Development 126:3359-3370.
73. Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, Nabeshima Y. 2000. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 99:143-148.
74. Tao W, Lai E. 1992. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 8:957-966.
75. te Welscher P, Zuniga A, Kuijper S, Drenth T, Goedemans HJ, Meijlink F, Zeller R. 2002. Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298:827-830.
76. Theil T. 2005. Gli3 is required for the specification and differentiation of preplate neurons. Dev Biol 286:559-571.
77. Theil T, Alvarez-Bolado G, Walter A, Ruther U. 1999. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development 126:3561-3571.
78. Tole S, Ragsdale CW, Grove EA. 2000. Dorsoventral patterning of the telencephalon is disrupted in the mouse mutant extra-toes(J). Dev Biol 217:254-265.
79. Tole S, Remedios R, Saha B, Stoykova A. 2005. Selective requirement of Pax6, but not Emx2, in the specification and development of several nuclei of the amygdaloid complex. J Neurosci 25:2753-2760.
80. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79:957-970.
81. Vaux DL, Korsmeyer SJ. 1999. Cell death in development. Cell 96:245-254.
82. von Mering C, Basler K. 1999. Distinct and regulated activities of human Gli proteins in Drosophila. Curr Biol 9:1319-1322.
83. Walther C, Gruss P. 1991. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113:1435-1449.
84. Wang HF, Liu FC. 2001. Developmental restriction of the LIM homeodomain transcription factor Islet-1 expression to cholinergic neurons in the rat striatum. Neuroscience 103:999-1016.
85. Wang B, Fallon JF, Beachy PA. 2000. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100:423-434.
86. Wang C, Ruther U, Wang B. 2007. The Shh-independent activator function of the full-length Gli3 protein and its role in vertebrate limb digit patterning. Dev Biol 305:460-469.
87. Wijgerde M, McMahon JA, Rule M, McMahon AP. 2002. A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev 16:2849-2864.
88. Xuan S, Baptista CA, Balas G, Tao W, Soares VC, Lai E. 1995. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14:1141-1152.
89. Yamamoto Y, Stock DW, Jeffery WR. 2004. Hedgehog signalling controls eye degeneration in blind cavefish. Nature 431:844-847.
90. Zaki PA, Martynoga B, Delafield-Butt JT, Fotaki V, Yu T, Price DJ. 2005. Loss of Gli3 enhances the viability of embryonic telencephalic cells in vitro. Eur J Neurosci 22:1547-1551.
91. Zhou Q, Wang S, Anderson DJ. 2000. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25:331-343.