Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord

Development

Volumn 131, Issue 21, 2004, Pages 5393-5403

  Wine Lee, Lara ^a,b   Ahn, Kyung J ^a   Richardson, Rory D ^a   Mishina, Yuji ^c   Lyons, Karen M ^d   Crenshaw III, E Bryan ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bmpr1b mutant; Bone morphogenetic protein receptor type I; Cre mediated conditional Bmpr1a knockout; Dorsal interneuron development; Mouse; Neural tube patterning

Indexed keywords

BINDING PROTEIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; RECEPTOR SUBTYPE; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LOSS; CELL MATURATION; CELL POPULATION; CELL TYPE; CONTROLLED STUDY; DORSAL ROOT; EMBRYO; GENE EXPRESSION; GENETIC ANALYSIS; INTERNEURON; KNOCKOUT MOUSE; MOUSE; MULTIGENE FAMILY; NERVE CELL DIFFERENTIATION; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPINAL CORD; STEM CELL; VENTRAL ROOT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; DOWN-REGULATION; EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERNEURONS; MICE; MICE, KNOCKOUT; MUTATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RECEPTORS, GROWTH FACTOR; SIGNAL TRANSDUCTION; SPINAL CORD; TRANSCRIPTION FACTORS; WNT PROTEINS;

ANIMALIA;

EID: 9444264776     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01379     Document Type: Article

References (51)

1. Ahn, K., Mishina, Y., Hanks, M. C., Behringer, R. R. and Crenshaw, E. B., III (2001). BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development 128, 4449-4461.
2. Bermingham, N. A., Hassan, B. A., Wang, V. Y., Fernandez, M., Banfi, S., Bellen, H. J., Fritzsch, B. and Zoghbi, H. Y. (2001). Proprioceptor pathway development is dependent on Math1. Neuron 30, 411-422.
3. Chang, H., Brown, C. W. and Matzuk, M. M. (2002). Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr. Rev. 23, 787-823.
4. Chenn, A. and Walsh, C. A. (2002). Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365-369.
5. Derynck, R. and Zhang, Y. E. (2003). Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577-584.
6. Ebendal, T., Bengtsson, H. and Soderstrom, S. (1998). Bone morphogenetic proteins and their receptors, potential functions in the brain. J. Neurosci. Res. 51, 139-146.
7. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M. and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-1801
8. Goulding, M. (1998). Specifying motor neurons and their connections. Neuron 21, 943-946.
9. Gowan, K., Helms, A. W., Hunsaker, T. L., Collisson, T., Ebert, P. J., Odom, R. and Johnson, J. E. (2001). Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 31, 219-232.
10. Grinspan, J. B., Coulalaglou, M., Beesley, J. S., Carpio, D. F. and Scherer, S. S. (1998). Maturation-dependent apoptotic cell death of oligodendrocytes in myelin-deficient rats. J. Neurosci. Res. 54, 623-634.
11. Gross, M. K., Dottori, M. and Goulding, M. (2002). Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34, 535-549.
12. Helms, A. W. and Johnson, J. E. (1998). Progenitors of dorsal commisural interneurons are defined by Math1 expression. Development 125, 919-928.
13. Helms, A. W. and Johnson, J. E. (2003). Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 13 42-49.
14. Hendzel, M. J., Wei, Y., Mancini, M. A., van Hooser, A., Ranalli, T., Brinkley, B. R., Bazett-Jones, D. P. and Allis, C. D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosome 106, 348-360.
15. Heydemann, A., Nguyen, L. C. and Crenshaw, E. B., III (2001). A regulatory region of the Brn4/Pou3f4 promoter directs expression to developing forebrain and neural tube. Dev. Brain Res. 128, 83-90.
16. Hogan, B. L. (1996). Bone morphogenetic proteins, multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
17. Hollnagel, A., Oehlmann, V., Heymer, J., Ruther, U. and Nordheim, A. (1999). Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J. Biol. Chem. 274 19838-19845.
18. Hollyday, M., McMahon, J. A. and McMahon, A. P. (1995). Wnt expression patterns in chick embryo nervous system. Mech. Dev. 52, 9-25.
19. Jessell, T. M. (2000). Neuronal specification in the spinal cord, inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
20. Lee, K. J. and Jessell, T. M. (1999). The specification of dorsal cell fates in the vertebrate central nervous system. Annu. Rev. Neurosci. 22, 261-294.
21. Lee, K. J., Mendelsohn, M. and Jessell, T. M. (1998). Neuronal patterning by BMPs, a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes Dev. 12, 3394-3407.
22. Lee, K. J., Dietrich, P. and Jessell, T. M. (2000). Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403, 734-740.
23. Lee, S. K. and Pfaff, S. L. (2001). Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat. Neurosci. 4, 1183-1191.
24. Liem, K. F., Jr, Tremml, G., Roelink, H. and Jessell, T. M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969-979.
25. Liem, K. F., Jr, Tremml, G. and Jessell, T. M. (1997). A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91, 127-138.
26. Lyden, D., Young, A. Z., Zagzag, D., Yen, W., Gerald, W., O'Reilly, R., Bader, B. L., Hynes, R. O., Zhuang, Y., Manova, K. et al. (1999). Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401, 670-677.
27. Massague, J. (1996). TGFbeta signaling, receptors, transducers, and Mad proteins. Cell 85, 947-950.
28. Massague, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791.
29. Megason, S. G. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
30. Mehler, M. F., Mabie, P. C., Zhang, D. and Kessler, J. A. (1997). Bone morphogenetic proteins in the nervous system. Trends Neurosci. 20, 309-317.
31. Millonig, J. H., Millen, K. J. and Hatten, M. E. (2000). The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 403, 764-769.
32. Mishina, Y., Suzuki, A., Ueno, N. and Behringer, R. R. (1995). Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9, 3027-3037.
33. Mishina, Y., Hanks, M. C., Miura, S., Tallquist, M. D. and Behringer, R. R. (2002). Generation of Bmpr/Alk3 conditional knockout mice. Genesis 32, 69-72.
34. Muller, T., Brohmann, H., Pierani, A., Heppenstall, P. A., Lewin, G. R., Jessell, T. M. and Birchmeier, C. (2002). The homeodomain factor lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34, 551-562.
35. Muroyama, Y., Fujihara, M., Ikeya, M., Kondoh, H. and Takada, S. (2002). Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 16, 548-553.
36. Nguyen, V. H., Trout, J., Connors, S. A., Andermann, P., Weinberg, E. and Mullins, M. C. (2000). Dorsal and intermediate neuronal cell types of the spinal cord are established by a BMP signaling pathway. Development 127, 1209-1220.
37. Norton, J. D. (2000). ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J. Cell Sci. 113 3897-3905.
38. Nowak, S. J. and Corces, V. G. (2000). Phosphorylation of histone H3 correlates with transcriptionally active loci. Genes Dev. 14, 3003-3013.
39. Panchision, D. M., Pickel, J. M., Studer, L., Lee, S. H., Turner, P. A., Hazel, T. G. and McKay, R. D. (2001). Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev. 15, 2094-2110.
40. Parr, B. A. and McMahon, A. P. (1994). Wnt genes and vertebrate development. Curr. Opin. Genet. Dev. 4, 523-528.
41. Phippard, D., Lu, L., Lee, D., Saunders, J. C. and Crenshaw, E. B., III (1999). Targeted mutagenesis of the POU-domain gene, Brn4/Pou3f4, causes development defects in the inner ear. J. Neurosci. 19, 5980-5989.
42. Pizette, S. and Niswander, L. (1999). BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126, 883-894.
43. Rockman, S. P., Currie, S. A., Ciavarella, M., Vincan, E., Dow, C., Thomas, R. J. and Phillips, W. A. (2001). Id2 is a target of the beta-catenin/T cell factor pathway in colon carcinoma. J. Biol. Chem. 276, 45113-45119.
44. Roelink, H. (1996). Tripartite signaling of pattern, interactions between Hedgehogs, BMPs and Wnts in the control of vertebrate development. Curr. Opin. Neurobiol. 6, 33-40.
45. Ross, S. E., Greenberg, M. E. and Stiles, C. D. (2003). Basic helix-loop-helix factors in cortical development. Neuron 39, 13-25.
46. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
47. Soshnikova, N., Zechner, D., Huelsken, J., Mishina, Y., Behringer, R. R., Taketo, M. M., Crenshaw, E. B., III and Birchmeier, W. (2003). Genetic interaction between Wnt/beta-catenin and BMP receptor signaling during formation of the AER and the dorsal-ventral axis in the limb. Genes Dev. 17, 1963-1968.
48. Thor, S., Andersson, S. G., Tomlinson, A. and Thomas, J. B. (1999). A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature 397, 76-80.
49. Timmer, J. R., Wang, C. and Niswander, L. (2002). BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loop-helix transcription factors. Development 129, 2459-2472.
50. Yi, S. E., Daluiski, A., Pederson, R., Rosen, V. and Lyons, K. M. (2000). The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127, 621-630.
51. Zechner, D., Fujita, Y., Hulsken, J., Muller, T., Walther, I., Taketo, M. M., Crenshaw, E. B., III, Birchmeier, W. and Birchmeier, C. (2003). beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol. 258, 406-418.