Neuronal patterning by BMPs: A requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord

Genes and Development

Volumn 12, Issue 21, 1998, Pages 3394-3407

  Lee, Kevin J ^a   Mendelsohn, Monica ^a   Jessell, Thomas M ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

BMPs; Commissural neurons; Neural patterning; Spinal cord

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN COMMISSURE; CENTRAL NERVOUS SYSTEM; ECTODERM; EMBRYO DEVELOPMENT; GENE INDUCTION; INTERNEURON; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL CREST; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; STEM CELL; VERTEBRATE;

ANIMALIA; MAMMALIA; VERTEBRATA;

EID: 0032213969     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.21.3394     Document Type: Article

References (62)

1. Akazawa, C., M. Ishibashi, C. Shimizu, S. Nakanishi, and R. Kageyama. 1995. A mammalian helix-loop-helix factor structurally related to the product of the Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 270: 8730-8738.
2. Altman, J. and S.A. Bayer. 1984. The development of the rat spinal cord. Adv. Anat. Embryol. Cell Biol. 85: 1-164.
3. Aono, A., M. Hazama, K. Notoya, S. Taketomi, H. Yamasaki, R. Tsukuda, S. Sasaki, and Y. Fujisawa. 1995. Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer. Biochem. Biophys. Res. Commun. 210: 670-677.
4. Arkell, R. and R.S.P. Beddington. 1997. BMP7 influences pattern and growth of the developing hindbrain of mouse embryos. Development 124: 1-12.
5. Basler, K., T. Edlund, T.M. Jessell, and T. Yamada. 1993. Control of cell pattern in the neural tube: Regulation of cell differentiation by dorsalin-1, a novel TGF beta family member. Cell 73: 687-702.
6. Ben-Arie, N., A.E. McCall, S. Berkman, G. Eichele, H.J. Bellen, and H.Y. Zoghbi. 1996. Evolutionary conservation of sequence and expression of the bHLH protein Atonal suggests a conserved role in neurogenesis. Hum. Mol. Genet. 5: 1207-1216.
7. Chen, H., Y. Lun, D. Ovchinnikov, H. Kokubo, K.C. Oberg, C.V. Pepicelli, L. Gan, B. Lee, and R.L. Johnson. 1998. Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nature Genet. 19:51-55.
8. Chiang, C., Y. Litingtung, E. Lee, K.E. Young, J.L. Corden, H. Westphal, and P.A. Beachy. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
9. Crossley, P.H., S. Martinez, and G.R. Martin. 1996. Midbrain development induced by FGF8 in the chick embryo. Nature 380: 66-68.
10. Dickinson, M.E., M.A. Selleck, A.P. McMahon, and F.M. Bronner. 1995. Dorsalization of the neural tube by the non-neural ectoderm. Development 121: 2099-2106.
11. Dudley, A.T. and E.J. Robertson. 1997. Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev. Dyn. 208: 349-362.
12. Dudley, A.T., K.M. Lyons, and E.J. Robertson. 1995. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes & Dev. 9: 2795-2807.
13. Ericson, J., S. Morton, A. Kawakami, H. Roelink, and T.M. Jessell. 1996. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87: 661-673.
14. Ericson, J., P. Rashbass, A. Schedl, S. Brenner-Morton, A. Kawakami, V. van Heyningen, T.M. Jessell, and J. Briscoe. 1997. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90: 169-180.
15. Furuta, Y., D.W. Piston, and B.L.M. Hogan. 1997. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212.
16. Helms, A.W. and J.E. Johnson. 1998. Progenitors of dorsal commissural interneurons are defined by mATH1 expression. Development 125: 919-928.
17. Hogan, B.L. 1996. Bone morphogenetic proteins in development. Curr. Opin. Gen. Dev. 6: 432-438.
18. Holley, S.A., J.L. Neul, L. Attisano, J.L. Wrana, Y. Sasai, M.B. O'Connor, E.M. De Robertis, and E.L. Ferguson. 1996. The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell 86: 607-617.
19. Hooper, M., K. Hardy, A. Handyside, S. Hunter, and M. Monk. 1987. HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature 326: 292-295.
20. Ikeya, M., S.M.K. Lee, J.E. Johnson, A.P. McMahon, and S. Takada. 1997. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389: 966-970.
21. Jones, C.M., K.M. Lyons, and B.L. Hogan. 1991. Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111: 531-542.
22. King, J.A., P.C. Marker, K.J. Seung, and D.M. Kingsley. 1994. BMP5 and the molecular, skeletal and soft-tissue alterations in short ear mice. Dev. Biol. 166: 112-122.
23. Kingsley, D. 1994. The TGFβ superfamily: New members, new receptors, and new genetic tests of function in different organisms. Genes & Dev. 8: 133-146.
24. Leber, S.M. and J.R. Sanes. 1995. Migratory paths of neurons and glia in the embryonic chick spinal cord. J. Neurosci. 15: 1236-1248.
25. Lee, S.M.K., P.S. Danielian, B. Fritzsch, and A.P. McMahon. 1997. Evidence that FGF8 signaling from the midbrain-hindbrain junction regulates growth and polarity in the developing midbrain. Development 124: 959-969.
26. Liem, K.F., G. Tremml, H. Roelink, and T.M. Jessell. 1995. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82: 969-979.
27. Liem, K.F., G. Tremml, and T.M. Jessell. 1997. A role for the roof plate and its resident TGFβ-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91: 127-138.
28. Lumsden, A. and R. Krumlauf. 1996. Patterning the vertebrate neuraxis. Science 274: 1109-1115.
29. Luo, G., C. Hofmann, A.L.J. Bronckers, M. Sohocki, A. Bradley, and G. Karsenty. 1995. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes & Dev. 9: 2808-2820.
30. Lyons, K.M., R.W. Pelton, and B.L.M. Hogan. 1989. Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that transforming growth factor-β-like genes coordinately regulate aspects of embryonic development. Genes & Dev. 3: 1657-1668.
31. Lyons, K.M., B.L. Hogan, and E.J. Robertson. 1995. Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50: 71-83.
32. Ma, Q., C. Kintner, and D.J. Anderson. 1996. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87: 43-52.
33. MacKenzie, A., M.W.J. Ferguson, and P.T. Sharpe. 1991. Hox-7 expression during murine craniofacial development. Development 113: 601-611.
34. Marti, E., D.A. Bumcrot, R. Takada, and A.P. McMahon. 1995. Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types. Nature 375: 322-325.
35. McMahon, A.P. and A. Bradley. 1990. The Wnt-1 (int-1) protooncogene is required for development of a large region of the mouse brain. Cell 62: 1073-1085.
36. McMahon, J.A., S. Takada, L.B. Zimmerman, C.M. Fan, R.M. Harland, and A.P. McMahon. 1998. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes & Dev. 12: 1438-1452.
37. Meyers, E.N., M. Lewandoski, and G.R. Martin. 1998. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nature Genet. 18: 136-141.
38. Monaghan, A.P., D.R. Davidson, C. Sime, E. Graham, R. Baldock, S.S. Bhattacharya, and R.E. Hill. 1991. The Msh-like homeobox genes define domains in the developing vertebrate eye. Development 112: 1053-1061.
39. Moury, J.D. and A.G. Jacobson. 1989. Neural fold formation at newly created boundaries between neural plate and epidermis in the axolotl. Dev. Biol. 133: 44-57.
40. Nakamura, T., K. Takio, Y. Eto, H. Shibai, K. Titani, and H. Sugino. 1990. Activin-binding protein from rat ovary is follistatin. Science 247: 836-838.
41. Nornes, H.O. and G.D. Das. 1974. Temporal pattern of neurogenesis in spinal cord of rat. I. An autoradiographic study-time and sites of origin and migration and settling patterns of neuroblasts. Brain Res. 73: 121-138.
42. Parr, B.A., M.J. Shea, and A.P. McMahon. 1993. Mouse Wnt genes exhibit discrete domains of expression in its early embryonic CNS and limb buds. Development 119: 247-261.
43. Pfaff, S.L., M. Mendelsohn, C.L. Stewart, T. Edlund, and T.M. Jessell. 1996. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84: 1-20.
44. Riddle, R.D., M. Ensini, C. Nelson, T. Tsuchida, T.M. Jessell, and C. Tabin. 1995. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83: 631-640.
45. Rissi, M., J. Wittbrodt, E. Delot, M. Naegeli, and F.M. Rosa. 1995. Zebrafish Radar: A new member of the TGF-beta superfamily defines dorsal regions of the neural plate and the embryonic retina. Mech. Dev. 49: 223-234.
46. Roelink, H., J.A. Porter, C. Chiang, Y. Tanabe, D.T. Chang, P.A. Beachy, and T.M. Jessell. 1995. Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81: 445-455.
47. Schaeren-Wiemers, N. and A. Gerfin-Moser. 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.
48. Shah, N.M., A.K. Groves, and D.J. Anderson. 1996. Alternative neural crest cell fates are instructively promoted by TGFβ superfamily members. Cell 85: 331-343.
49. Shimamura, K., D.J. Hartigan, S. Martinez, L. Puelles, and J.L. Rubenstein. 1995. Longitudinal organization of the anterior neural plate and neural tube. Development 121: 3923-3933.
50. Storm, E.E., T.V. Huynh, N.G. Copeland, N.A. Jenkins, D.M. Kingsley, and S.-J. Lee. 1994. Limb alterations in brachypodism mice due to mutations in a new member of the TGFβ-superfamily. Nature 368: 639-643.
51. Suzuki, A., E. Kaneko, J. Maeda, and N. Ueno. 1997. Mesoderm induction by BMP-4 and -7 heterodimers. Biochem. Biophys. Res. Commun. 232: 153-156.
52. Tanabe, Y. and T.M. Jessell. 1996. Diversity and pattern in the developing spinal cord. Science 274: 1115-1123.
53. Tanabe, Y., H. Roelink, and T. Jessell. 1995. Induction of motor neurons by Sonic hedgehog is independent of floor plate differentiation. Curr. Biol. 5: 651-658.
54. Thomas, K.R. and M.R. Capecchi. 1990. Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346: 847-850.
55. Tsuchida, T., M. Ensini, S.B. Morton, M. Baldassare, T. Edlund, T.M. Jessell, and S.L. Pfaff. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79: 957-970.
56. Winnier, G., M. Blessing, P.A. Labosky, and B.L. Hogan. 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes & Dev. 9: 2105-2116.
57. Xu, Y., M. Baldassare, P. Fisher, G. Rathbun, E.M. Oltz, G.D. Yancopoulos, T.M. Jessell, and F.W. Alt. 1993. LH-2: A LIM/ homeodomain gene expressed in developing lymphocytes and neural cells. Proc. Natl. Acad. Sci. 90: 227-231.
58. Yamada, T., S.L. Pfaff, T. Edlund, and T.M. Jessell. 1993. Control of cell pattern in the neural tube: Motor neuron induction by diffusible factors from notochord and floor plate. Cell 73: 673-686.
59. Yamashita, H., P. ten Dijke, D. Huylebroeck, T.K. Sampath, M. Andries, J.C. Smith, C.H. Heldin, and K. Miyazono. 1995. Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130: 217-226.
60. Ye, W., K. Shimamura, J.L.R. Rubenstein, M.A. Hynes, and A. Rosenthal. 1998. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93: 755-766.
61. Zhang, H. and A. Bradley. 1996. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122: 2977-2986.
62. Zimmerman, L.B., J.M. De Jesus-Escobar, and R.M. Harland. 1996. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86: 599-606.