BMP type I receptor complexes have distinct activities mediating cell fate and axon guidance decisions

Development

Volumn 135, Issue 6, 2008, Pages 1119-1128

  Yamauchi, Ken ^a   Phan, Keith D ^a   Butler, Samantha J ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Axon guidance; Bone morphogenetic proteins; Commissural neurons; Morphogen; Spinal cord

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; MORPHOGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYO; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPINAL CORD;

ANIMALS; AXONS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL DIFFERENTIATION; CHICK EMBRYO; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; MULTIPROTEIN COMPLEXES; PREGNANCY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 42549136934     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.012989     Document Type: Article

References (57)

1. Akiyama, S., Katagiri, T., Namiki, M., Yamaji, N., Yamamoto, N., Miyama, K., Shibuya, H., Ueno, N., Wozney, J. M. and Suda, T. (1997). Constitutively active BMP type I receptors transduce BMP-2 signals without the ligand in C2C12 myoblasts. Exp. Cell Res. 235, 362-369.
2. Aubin, J., Davy; A. and Soriano, P. (2004). In vivo convergence of BMP and MAPK signaling pathways: impact of differential Smad1 phosphorylation on development and homeostasis. Genes Dev. 18, 1482-1494.
3. Augsburger, A., Schuchardt A., Hoskins, S., Dodd, J. and Butler, S. (1999). BMPs as mediators of roof plate repulsion of commissural neurons. Neuron 24, 127-141.
4. Bourikas, D., Pekarik, V., Baeriswyl, T., Grunditz, A., Sadhu, R., Nardo, M. and Stoeckli, E. T. (2005). Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat. Neurosci. 8, 297-304.
5. Bovolenta, P., Rodriguez, J. and Esteve, P. (2006). Frizzled/RYK mediated signalling in axon guidance. Development 133, 4399-4408.
6. 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 101, 435-445.
7. Brittis, P. A., Silver, J., Walsh, F. S. and Doherty, P. (1996). Fibroblast growth factor receptor function is required for the orderly projection of ganglion cell axons in the developing mammalian retina. Mol. Cell. Neurosci. 8, 120-128.
8. Butler, S. J. and Dodd, J. (2003). A role for BMP heterodimers in roof platemediated repulsion of commissural axons. Neuron 38, 389-401.
9. Campbell, D. S. and Holt, C. E. (2001). Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026.
10. Charron, F. and Tessier-Lavigne, M. (2005). Novel brain wiring functions for classical morphogens: a role as graded positional cues in axon guidance. Development 132, 2251-2262.
11. Charron, F., Stein, E., Jeong, J., McMahon, A. R and Tessier-Lavigne, M. (2003). The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113, 11-23.
12. Dewulf, N., Verschueren, K., Lonnoy, O., Moren, A., Grimsby, S., Vande Spiegle, K., Miyazono, K., Huylebroeck, D. and Ten Dijke, P. (1995). Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 136, 2652-2663.
13. Dickson, B. J. (2002). Molecular mechanisms of axon guidance. Science 298, 1959-1964.
14. Dodd, J. and Jessell, T. M. (1988). Axon guidance and the patterning of neuronal projections in vertebrates. Science 242, 692-699.
15. Dodd, J., Morton, S. B., Karagogeos, D., Yamamoto, M. and Jessell, T. M. (1988). Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1, 105-116.
16. 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.
17. Foletta, V. C., Lim, M. A., Soosairajah, J., Kelly, A. P., Stanley, E. G., Shannon, M., He, W., Das, S., Massague, J. and Bernard, O. (2003). Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J. Cell Biol. 162, 1089-1098.
18. Hamburger, V. and Hamilton, H. L. (1992). A series of normal stages in the development of the chick embryo. 1951. Dev Dyn. 195, 231-272.
19. Heldin, C. H., Miyazono, K. and ten Dijke, P. (1997). TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
20. Helms, A. W. and Johnson, J. E. (1998). Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development 125, 919-928.
21. Helms, A. W., Abney, A. L, Ben-Arie, N., Zoghbi, H. Y. and Johnson, J. E. (2000). Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. Development 127, 1185-1196.
22. Holley, J. A. (1982). Early development of the circumferential axonal pathway in mouse and chick spinal cord. J. Comp. Neurol. 205, 371-382.
23. Irving, C., Malhas, A., Guthrie, S. and Mason, I. (2002). Establishing the trochlear motor axon trajectory: role of the isthmic organiser and Fgf8. Development 129, 5389-5398.
24. Kretzschmar, M. and Massague, J. (1998). SMADs: mediators and regulators of TGF-beta signaling. Curr Opin. Genet. Dev. 8, 103-111.
25. 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.
26. Lee-Hoeflich, S. T., Causing, C. G., Podkowa, M., Zhao, X., Wrana, J. L. and Attisano, L. (2004). Activation of LlMK1 by binding to the BMP receptor, BMPRI1, regulates BMP-dependent dendritogenesis. EMBO J. 23, 4792-4801.
27. 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.
28. Liem, K. F., Jr, Jessell, T. M. and Briscoe, J. (2000). Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127, 4855-4866.
29. Liu, J., Wilson, S. and Reh, T. (2003). BMP receptor 1b is required for axon guidance and cell survival in the developing retina. Dev. Biol. 256, 34-48.
30. Lumpkin, E. A., Collisson, T., Parab, P., Omer-Abdalla, A., Haeberle, H., Chen, P., Doetzlhofer, A., White, P., Groves, A., Segil, N. et al. (2003). Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expr. Patterns 3, 389-395.
31. Lyuksyutova, A. I., Lu, C. C., Milanesio, N., King, L. A., Guo, N., Wang, Y., Nathans, J., Tessier-Lavigne, M. and Zou, Y. (2003). Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 302, 1984-1988.
32. Massague, J., Seoane, J. and Wotton, D. (2005). Smad transcription factors. Genes Dev. 19, 2783-2810.
33. Matei, V., Pauley, S., Kaing, S., Rowitch, D., Beisell, K. W., Morris, K., Feng, F., Jones, K., Lee, J. and Fritzsch, B. (2005). Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev. Dyn. 234, 633-650.
34. McFarlane, S., Cornell, E., Amaya, E. and Holt, C. E. (1996). Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition. Neuron 17, 245-254.
35. 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.
36. 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.
37. Murali, D., Yoshikawa, S., Corrigan, R. R., Plas, D. J., Crain, M. C., Oliver G., Lyons, K. M., Mishina, Y. and Furuta, Y. (2005). Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 132, 913-923.
38. Nybakken, K. and Perrimon, N. (2002). Hedgehog signal transduction: recent findings. Curr. Opin. Genet. Dev. 12, 503-511.
39. Okada, A., Charron, F., Morin, S., Shin, D. S., Wong, K., Fabre, P. J., Tessier-Lavigne, M. and McConnell, S. K. (2006). Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444, 369-373.
40. Oppenheim, R. W., Shnelderman, A., Shimizu, I. and Yaginuma, H. (1988). Onset and development of intersegmental projections in the chick embryo spinal cord. J. Comp. Neurol. 275, 159-180.
41. Roelen, B. A., Goumans, M. J., van Rooijen, M. A. and Mummery, C. L. (1997). Differential expression of BMP receptors in early mouse development. Int. J. Dev. Biol. 41, 541-549.
42. Ruegg, M. A., Stoeckil, E. T., Kuhn, T. B., Heller, M., Zuellig, R. and Sonderegger, P. (1989). Purification of axonin-1, a protein that is secreted from axons during neurogenesis. EMBO J. 8, 55-63.
43. Salie, R., Niederkofler, V. and Arber, S. (2005). Patterning molecules; multitasking in the nervous system. Neuron 45, 189-192.
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. Serafini, T., Colamarino, S. A., Leonardo, E. D., Wang, H., Becklington, R., Skarnes, W. C. and Tessier-Lavigne, M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
46. Swartz, M., Eberhart, J., Mastick. G. S. and Krull, C. E. (2001). Sparking new frontiers: using in vivo electroporation for genetic manipulations. Dev Biol. 233, 13-21.
47. Tabata, T. and Takell, Y. (2004). Morphogens, their identification and regulation. Development 131, 703-712.
48. ten Dijke, P., Yamashita, H., Sampath, T. K., Reddi, A. H., Estevez, M., Riddle, D. L, Ichijo, H., Heldin, C. H. and Miyazono, K. (1994). Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J. Biol. Chem. 269, 16985-16988.
49. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
50. 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.
51. Tsuchicla, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
52. Wen, Z., Han, L, Bamburg, J. R., Shim, S., Ming, G. L. and Zheng, J. Q. (2007). BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J. Cell Biol. 178, 107-119.
53. Wieser, R., Wrana, J. L. and Massague, J. (1995). GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGF-beta receptor complex. EMBO J. 14, 2199-2208.
54. Wine-Lee, L, Ahn, K. J., Richardson, R. D., Mishina, Y., Lyons, K. M. and Crenshaw, E. B., 3rd (2004). Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord. Development 131, 5393-5403.
55. 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.
56. Yi, S. E., LaPolt P. S., Yoon, B. S., Chen, J. Y., Lu, J. K. and Lyons, K. M. (2001). The type I BMP receptor BmprIB is essential for female reproductive function. Proc. Natl. Acad. Sci. USA 98, 7994-7999.
57. Yoon, B. S., Ovchinnikov, D. A., Yoshii, I., Mishina, Y., Behringer, R. R. and Lyons, K. M. (2005). Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc. Natl. Acad. Sci. USA 102, 5062-5067.