Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning

Development

Volumn 130, Issue 20, 2003, Pages 4895-4906

  Corbin, Joshua G ^a   Rutlin, Michael ^a   Gaiano, Nicholas ^b   Fishell, Gord ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gsh2; Mouse; Nkx2.1; Patterning; Pax6; Telencephalon

Indexed keywords

HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GSH2; TRANSCRIPTION FACTOR NKX2; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; GENE EXPRESSION; GENE REPRESSION; MAMMAL; MEDIAN EMINENCE; MOUSE; MOUSE MUTANT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; TELENCEPHALON;

ANIMALS; EYE PROTEINS; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; MICE; PAIRED BOX TRANSCRIPTION FACTORS; PHENOTYPE; REPRESSOR PROTEINS; TELENCEPHALON; TRANS-ACTIVATORS;

ANIMALIA; MAMMALIA;

EID: 0142149995     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00717     Document Type: Article

References (62)

1. Alberta, J. A., Park, S. K., Mora, J., Yuk, D., Pawlitzky, I., Iannarelli, P., Vartanian, T., Stiles, C. D. and Rowitch, D. H. (2001). Sonic hedgehog is required during an early phase of oligodendrocyte development in mammalian brain. Mol. Cell. Neurosci. 18, 434-441.
2. Anderson, S. A., Marin, O., Horn, C., Jennings, K. and Rubenstein, J. L. (2001). Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353-363.
3. Behar, T., Ma, W., Hudson, L. and Barker, J. L. (1994). Analysis of the anatomical distribution of GAD67 mRNA encoding truncated glutamic acid decarboxylase proteins in the embryonic rat brain. Dev. Brain Res. 77, 77-87.
4. Bell, E., Ensini, M., Gulisano, M. and Lumsden, A. (2001). Dynamic domains of gene expression in the early avian forebrain. Dev. Biol. 236, 76-88.
5. Bertrand, N., Castro, D. S. and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.
6. Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T., Rubenstein, J. L. R. and Ericson, J. (1999). The Nkx2.2 homeobox gene mediates graded Sonic Hedgehog signaling and controls ventral neuronal subtype identity. Nature 398, 622-627.
7. Briscoe, J., Pierani, A., Jessell, T. M. and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 12, 435-445.
8. Campbell, K. (2003). Dorsal-ventral patterning in the mammalian telencephalon. Curr. Opin. Neurobiol. 13, 50-56.
9. Caric, D., Gooday, D., Hill, R. E., McConnell, S. K. and Price, D. J. (1997). Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax-6. Development 124, 5087-5096.
10. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic Hedgehog gene function. Nature 383, 407-413.
11. Chu, H., Parras, C., White, K. and Jiménez, F. (1998). Formation and specification of ventral neuroblasts is controlled by vnd in Drosophila neurogenesis. Genes Dev. 12, 3613-3624.
12. Corbin, J. G., Gaiano, N., Machold, R. P., Langston, A. and Fishell G. (2000). The Gsh2 homeodomain gene controls multiple aspects of telencephalic development. Development 127, 5007-5020.
13. Corbin, J. G., Nery, S. and Fishell, G. (2001). Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat. Neurosci. Suppl. 4, 1177-1182.
14. Cornell, R. A. and Ohlen, T. V. (2000). Vnd/nkx, ind/gsh, and msh/msx: conserved regulators of dorsoventral neural patterning? Curr. Opin. Neurobiol. 10, 63-71.
15. Garel, S., Marin, F., Mattei, M. G., Vesque, C., Vincent, A. and Charnay P. (1997). Family of Ebf/Olf-1-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev. Dyn. 3, 191-205.
16. Garel, S., Marin, F., Grosschedl, R. and Charnay, P. (1999). Ebf1 controls early cell differentiation in the embryonic striatum. Development 126, 5285-5294.
17. Gaiano, N., Kohtz, J. D., Turnbull, D. H. and Fishell, G. (1999). A method for rapid gain-of-function studies in the mouse embryonic nervous system. Nature Neurosci. 2, 812-819.
18. Götz, M., Stoykova, A. and Gruss, P. (1998). Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031-1044.
19. Gradwohl, G., Fode, C. and Guillemot, F. (1996). Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180, 227-241.
20. Grigoriou, M., Tucker, A. S., Sharpe, P. T. and Pachnis, V. (1998). Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. Development 125, 2063-2074.
21. Grindley, J. C., Davidson, D. R. and Hill, R. E. (1995). The role of Pax-6 in eye and nasal development. Development 121, 1433-1442.
22. Guillemot, F. and Joyner, A. L. (1993). Dynamic expression of the murine Achaete-Scute orthologue Mash-1 in the developing nervous system. Mech. Dev. 42, 171-185.
23. Heins, N., Malatesta, P., Cecconi, F., Nakafuku, M., Tucker, K. L., Hack, M. A., Chapouton, P., Barde, Y. A. and Gotz, M. (2002). Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5, 308-315.
24. Hill, R. E., Favor, J., Hogan, B. L., Ton, C. C., Saunders, G. F., Hanson, I. M., Prosser, J., Jordan, T., Hastie, N. D. and van Heyningen, V. (1991). Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522-525.
25. Ho, K. S. and Scott, M. P. (2002). Sonic hedgehog in the nervous system: functions, modifications and mechanisms. Curr. Opin. Neurobiol. 12, 57-63.
26. Inoue, T., Nakamura, S. and Osumi, N. (2000). Fate mapping of the mouse prosencephalic neural plate. Dev. Biol. 219, 373-383.
27. Kessaris, N., Pringle, N. and Richardson, W. D. (2001). Ventral neurogenesis and the neuron-glial switch. Neuron 31, 677-680.
28. Lavdas, A. A., Grigoriou, M., Pachnis, V. and Parnavelas, J. G. (1999). The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881-7888.
29. Lu, Q. R., Yuk, D., Alberta, J. A., Zhu, Z., Pawlitzky, I., Chan, J., McMahon, A. P., Stiles, C. D. and Rowitch, D. H. (2000). Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317-329.
30. Marin, O. and Rubenstein, J. L. (2001). A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2, 780-790.
31. Marquardt, T. and Pfaff, S. L. (2001). Cracking the transcriptional code for cell specification in the neural tube. Cell 106, 651-654.
32. Mercola, M., Wang, C. Y., Kelly, J., Brownlee, C., Jackson-Grusby, L., Stiles, C. and Bowen-Pope, D. (1990). Selective expression of PDGF A and its receptor during early mouse embryogenesis. Dev. Biol. 138, 114-122.
33. McDonald, J. A., Holbrook, S., Isshiki, T., Weiss, J., Doe, C. Q. and Mellerick, D. M. (1998). Dorsoventral patterning in the Drosophila central nervous system: the vnd homeobox gene specifies ventral column identity. Genes Dev. 12, 3603-3612.
34. Nery, S., Wichterle, H. and Fishell, G. (2001). Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527-540.
35. Nery, S., Fishell, G. and Corbin, J. G. (2002). The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5, 1279-1287.
36. Nery, S., Corbin, J. G. and Fishell, G. (2003). Dlx2 progenitor migration in wild type and Nkx2.1 mutant telencephalon. Cerebral Cortex 13, 895-903.
37. Pabst, O., Herbrand, H., Takuma, N. and Hans-Henning, A. (2000). NKX2 gene expression in neuroectoderm but not in mesendodermally derived structures depends on sonic hedgehog in mouse embryos Dev. Genes Evol. 210, 47-50.
38. Perez-Villegas, E. M., Olivier, C., Spassky, N., Poncet, C., Cochard, P., Zalc, B., Thomas, J. L. and Martinez, S. (1999). Early specification of oligodendrocytes in the chick embryonic brain. Dev. Biol. 216, 98-113.
39. Pierani, A., Brenner-Morton, S., Chiang, C. and Jessell, T. M. (1999). A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97, 903-915.
40. Porteus, M. H., Bulfone, A., Ciaranello, R. D. and Rubenstein, J. L. (1991). Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron 2, 221-229.
41. Rallu, M., Machold, R., Gaiano, N., Corbin, J. G., McMahon, A. P. and Fishell, G. (2002a). Dorso-ventral patterning is established in the telencephalon of mutants lacking both Gli3 and hedgehog signaling. Development 129, 4963-4974.
42. Rallu, M., Corbin, J. G. and Fishell, G. (2002b). Parsing the prosencephalon. Nat. Rev. Neurosci. 12, 943-951.
43. Sauvageot, C. M. and Stiles, C. D. (2002). Molecular mechanisms controlling cortical gliogenesis. Curr. Opin. Neurobiol. 12, 244-249.
44. Schaeren-Wiemers, N. and Gerfin-Moser, A. (1993). A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440.
45. Schuurmans, C. and Guillemot, F. (2002). Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12, 26-34.
46. Shimamura, K., Hartigan, D. J., Martinez, S., Puelles, L. and Rubenstein, J. L. (1995). Longitudinal organization of the anterior neural plate and neural tube. Development 121, 3923-3933.
47. Spassky, N., Goujet-Zalc, C., Parmantier, E., Olivier, C., Martinez, S., Ivanova, A., Ikenaka, K., Macklin, W., Cerruti, I., Zalc, B. et al. (1998). Multiple restricted origin of oligodendrocytes. J. Neurosci. 18, 8331-8343.
48. Stoykova, A., Fritsch, R., Walther, C. and Gruss, P. (1996). Forebrain patterning defects in Small eye mutant mice. Development 122, 3453-3465.
49. Stoykova, A., Treichel, D., Hallonet, M. and Gruss, P. (2000). Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci. 20, 8042-8050.
50. Sussel, L., Marin, O., Kimura, S. and Rubenstein, J. L. R. (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.
51. Szucsik, J. C., Witte, D. P., Li, H., Pixley, S. K., Small, K. M. and Potter S. S. (1997). Altered forebrain and hindbrain development in mice mutant for the Gsh-2 homeobox gene. Dev. Biol. 191, 230-242.
52. Tekki-Kessaris, N., Woodruff, R., Hall, A. C., Gaffield, W., Kimura, S., Stiles, C. D., Rowitch, D. H. and Richardson, W. D. (2001). Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 128, 2545-2554.
53. Timsit, S., Martinez, S., Allinquant, B., Peyron, F., Puelles, L. and Zalc, B. (1995). Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J. Neurosci. 15, 1012-1024.
54. Toresson, H. and Campbell, K. (2001). A role for Gsh1 in the developing striatum and olfactory bulb of Gsh2 mutant mice. Development 128, 4769-4780.
55. Toresson, H., Potter, S. S. and Campbell, K. (2000). Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127, 4361-4371.
56. Valerius, M. T., Li, H., Stock, J. L., Weinstein, M., Kaur, S., Singh, G. and Potter, S. S. (1995). Gsh-1: a novel murine homeobox gene expressed in the central nervous system. Dev. Dyn. 203, 337-351.
57. Weiss, J. B., Von Ohlen, T., Mellerick, D. M., Dressler, G., Doe, C. Q. and Scott, M. P. (1998). Dorsoventral patterning in the Drosophila central nervous system: the intermediate neuroblasts defective homeobox gene specifies intermediate column identity. Genes Dev. 12, 3591-3602.
58. Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G. and Alvarez-Buylla, A. (1999). Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2, 461-466.
59. Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G. and Alvarez-Buylla, A. (2001). In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128, 3759-3771.
60. Wilkinson, D. G. and Nieto, M. A. (1993). Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225, 361-373.
61. Wilson, S. W. and Rubenstein, J. L. (2000). Induction and dorsoventral patterning of the telencephalon. Neuron 28, 641-651.
62. Yun, K., Potter, S. and Rubenstein, J. L. (2001). Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128, 193-205.