Bmps as mediators of roof plate repulsion of commissural neurons

Neuron

Volumn 24, Issue 1, 1999, Pages 127-141

  Augsburger, Adela ^a   Schuchardt, Anita ^a   Hoskins, Sally ^a   Dodd, Jane ^a,b   Butler, Samantha ^a  

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

^b CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; OSTEOGENIC PROTEIN 1;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GROWTH CONE; NERVE FIBER GROWTH; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; SYNAPTOGENESIS;

EID: 0033199552     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80827-2     Document Type: Article

References (93)

1. Altman, J., and Bayer, S.A. (1984). The development of the rat spinal cord. Adv. Anat. Embryol. Cell Biol. 85, 1-164.
2. Basler, K., Edlund, T., Jessell, T.M., and Yamada, T. (1993). Control of cell pattern in the neural tube: regulation of cell differentiation by dorsalin-1, a novel TGFB family member. Cell 73, 687-702.
3. Bergemann, A.D., Zhang, L., Chiang, M., Brambilla, R., Klein, R., and Flanagan, J.G. (1998). Ephrin-B3, a ligand for the receptor EphB3, expressed at the midline of the developing neural tube. Oncogene 16, 471-480.
4. Birgbauer, E., Dinsmore, J.H., Winckler, B., Lander, A.D., and Solomon, F. (1991). Association of ezrin isoforms with the neuronal cytoskeleton. J. Neurosci. Res. 30, 232-241.
5. Bovolenta, P., and Dodd, J. (1990). Guidance of commissural growth cones at the floor plate in embryonic rat spinal cord. Development 109, 435-477.
6. Bovolenta, P., and Dodd, J. (1991). Perturbation of neuronal differentiation and axon guidance in the spinal cord of mouse embryos lacking a floor plate: analysis of Danforth's short-tail mutation. Development 113, 625-639.
7. Brose, K., Bland, K.S., Wang, K.H., Arnott, D., Henzel, W., Goodman, C.S., Tessier-Lavigne, M., and Kidd, T. (1999). Slit proteins bind robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795-806.
8. Celeste, A.J., Iannazzi, J.A., Taylor, R.C., Hewick, R.M., Rosen, V., Wang, E.A., and Wozney, J.M. (1990). Identification of transforming growth factor-β family members present in bone-inductive protein purified from bovine bone. Proc. Natl. Acad. Sci. USA 87, 9843-9847.
9. 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.
10. Choi, S.E., Choi, E.Y., Kim, P.H., and Kim, J.H. (1999). Involvement of protein kinase C and rho GTPase in the nuclear signaling pathway by transforming growth factor-beta1 in rat-2 fibroblast cells. Cell Signal 11, 71-76.
11. Colamarino, S., and Tessier-Lavigne, M. (1995). The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629.
12. Colavita, A., Krishna, S., Zheng, H., Padgett R.W., and Culotti, J.G. (1998). Pioneer axon guidance by UNC-129, a C. elegans TGF-beta. Science 281, 706-709.
13. Cunningham, N.S., Paralkar, V., and Reddi, A.H. (1992). Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor beta 1 mRNA expression. Proc. Natl. Acad. Sci. USA 89, 11740-11744.
14. Dale, K., Vesque, C., Sattar, N., Lints, T., Sampath, K., Furley, A., Dodd, J., and Placek, M. (1997). Cooperation of BMP7 and SHH in the induction of forebrain ventral midline cells by prechordal mesoderm. Cell 90, 257-269.
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. Dudley, A.T., Lyons, K.M., and Robertson, E.J. (1995). A requirement for bone morpohogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9, 2795-2807.
17. Dudley, A.T., and Robertson, E.J. (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.
18. Ebens, A., Brose, K., Leonardo, E.D., Hanson, M.G. Jr., Bladt, F., Birchmeier, C., Barres, B.A., and Tessier-Lavigne, M. (1996). Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17, 1157-1172.
19. Eichmann, A., Grapin-Botton, A., Kelly, L., Graf, T., Le Douarin, N.M., and Sieweke, M. (1997). The expression pattern of the mafB/kr gene in birds and mice reveals that the kreisler phenotype does not represent a null mutant. Mech. Dev. 65, 111-122.
20. Ericson, J., Muhr, J., Placzek, M., Lints, T., Jessell, T.M., and 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.
21. Ericson, J., Morton, S., Kawakami, A., Roelink, H., and Jessell, T.M. (1996). Two critical periods of Sonic hedgehog signaling required for the specification of motor neuron identity. Cell 87, 661-673.
22. 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, 169-180.
23. Evan, G.I., Lewis, G.K, Ramsay, G., and Bishop, J.M. (1985). Isolation of monoclonal antibodies specific for human c-myc protooncogene product. Mol. Cell. Biol. 5, 3610-3616.
24. Fan, J., and Raper, J.A. (1995). Localized collapsing cues steer growth cones without inducing their full collapse. Neuron 14, 263-274.
25. Fazeli, A., Dickinson, S.L., Hermiston, M.L., Tighe, R.V., Steen, R.G., Small, C.G., Stoeckli, E.T., Keino-Masu, K., Masu, M., Rayburn, H., et al. (1997). Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804.
26. Furuta, Y., Piston, D.W., and Hogan, B.L. (1997). Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124, 2203-2212.
27. Gale, N.W., Flenniken, A., Compton, D.C., Jenkins, N., Copeland, N.G., Gilbert, D.J., Davis, S., Wilkinson, D.G., and Yancopoulos, G.D. (1996). Elk-L3, a novel transmembrane ligand for the Eph family of receptor tyrosine kinases, expressed in embryonic floor plate, roof plate and hindbrain segments. Oncogene 19, 1343-1352.
28. Gitelman, S.E., Kobrin, M., Lee, A., Fet, V., Lyons, K., Hogan, B.L.M., and Derynck, R. (1997). Structure and sequence of the mouse Bmp6 gene. Mamm. Genome 8, 212-214.
29. Goslin, K., Birgbauer, E., Banker, G., and Solomon, F. (1989). The role of cytoskeleton in organizing growth cones: a microfilament-associated growth cone component depends upon microtubules for its localization. J. Cell Biol. 109, 1621-1631.
30. Graham, A., Francis-West, P., Brickell, P., Lumsden, A. (1994). The signaling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature 372, 684-686.
31. Gross, R.E., Mehler, M.F., Mabie, P.C., Zang, Z., Santschi, L., and Kessler, J.A. (1996). Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17, 595-606.
32. Guo, X., Rueger, D., and Higgins, D. (1998). Osteogenic protein-1 and bone morphogenetic proteins regulate dendritic growth and the expression of microtubule-associated protein-2 in rat sympathetic neurons. Neurosci. Lett. 245, 131-134.
33. Guthrie, S., and Pini, A. (1995). Chemorepulsion of developing motor axons by the floor plate. Neuron 14, 1117-1130.
34. Hahn, G.V., Cohen, R.B., Wozney, J.M., Levitz, C.L., Shore, E.M., Zasloff, M.A., and Kaplan, F.S. (1992). A bone morphogenetic protein subfamily: chromosomal localization of human genes for BMP5, BMP6, and BMP7. Genomics 14, 759-762.
35. Halstead, J., Kemp, K., and Ignotz, R.A. (1995). Evidence for involvement of phosphatidylcholine-phospholipase C and protein kinase C in transforming growth factor-beta signaling. J. Biol. Chem. 270, 13600-13603.
36. Helms, A.W., and Johnson, J.E. (1998). Progenitors of C interneurons are defined by MATH1 expression. Development 125, 919-928.
37. Hogan, B.L. (1994). Sorting out the signals. Curr. Biol. 4, 1122-1124.
38. Hogan, B.L. (1996). Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6, 432-438.
39. Holley, J.A. (1982). Early development of the circumferential axonal pathway in mouse and chick spinal cord. J. Comp. Neurol. 205, 371-382.
40. Holley, J.A., Nornes, H.O., and Morita, M. (1982). Guidance of neuritic growth in the transverse plane of embryonic mouse spinal cord. J. Comp. Neurol. 205, 360-370.
41. Hume, C.R., and Dodd, J. (1993). Cwnt-8C: a novel Wnt gene with a potential role in primitive streak formation and hindbrain organization. Development 119, 1147-1160.
42. Israel, D.I., Nove, J., Kerns, K.M., Kaufman, R.J., Rosen, V., Cox, K.A., and Wozney, J.M. (1996). Heterodimeric bone morphogenetic proteins show enhanced activity in vitro and in vivo. Growth Factors 13, 291-300.
43. Jones, C.M., Lyons, K.M., and Hogan, B.L. (1991). Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111, 531-542.
44. Kennedy, T.E., Serafini, T., de la Torre, J., and Tessier-Lavigne, M. (1994). Netrins are chemotropic factors for C axons in the embryonic spinal cord. Cell 78, 425-435.
45. Kretzschmar, M., and Massague, J. (1998). SMADs: mediators and regulators of TGFβ signaling. Curr. Opin. Genet. Dev. 8, 103-111.
46. Lee, Y.S., and Chuong, C.M. (1997). Activation of protein kinase A is a pivotal step involved in both BMP-2-and cyclic AMP-induced chondrogenesis. J. Cell Physiol. 170, 153-165.
47. 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.
48. 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.
49. Li, H., Chen, J., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z., Nash, W., Gick, C., et al. (1999). Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96, 807-818.
50. Liem, K.F., Jr., Tremml, G., Roelink, H., and Jessel, T.M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderms. Cell 82, 969-979.
51. Liem, K.F., Jr., Tremml, G., and Jessell, T.M. (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.
52. Loschinger, J., Bandtlow, C.E., Jung, J., Klostermann, S., Schwab, M.E., Bonhoeffer, F., and Kater, S.B. (1997). Retinal axon growth cone responses to different environmental cues are mediated by different second messenger systems. J. Neurobiol. 33, 825-834.
53. Lumsden, A., and Davies, A. (1986). Chemotropic effect of specific target epithelium in development of the mammalian nervous system. Nature 323, 538-539.
54. Luo, Y., Raible, D., and Raper, J.A. (1993). Collapsin: a protein in the brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227.
55. Luo, Y., Shepherd, I., Li, J., Renzi, M.J., Chang, S., and Raper, J.A. (1995). A family of molecules related to collapsin in the embryonic chick nervous system. Neuron 14, 1131-1140.
56. Lyons, K.M., Hogan, B.L.M., and Robertson, E.J. (1995). Colocalization of BMP7 and BMP2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev. 50, 71-83.
57. Marti, E., Takada, R., Bumcrot, D.A., Sasaki, H., and McMahon, A.P. (1995). Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121, 2537-2547.
58. McFarlane, S., Cornel, 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.
59. McFarlane, S., Zuber, M.E., and Holt, C.E. (1998). A role for the fibroblast growth factor receptor in cell fate decisions in the developing vertebrate retina. Development 125, 3967-3975.
60. Mueller, B.K. (1999). Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 22, 351-388.
61. Nornes, H.O., and Das, G.D. (1974). Temporal pattern of neurogenesis in the spinal cord of rat. I. Time and sites of origin and migration and settling patterns of neuroblasts. Brain Res. 73, 121-138.
62. Oppenheim, R.W., Schneiderman, 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.
63. Parr, B.A., Shea, M.J., Vassileva, G., and McMahon, A.P. (1993). Mouse Wnt genes exhibit discrete domains of expression in the early CNS and limb buds. Development 119, 247-261.
64. Perides, G., Hu, G., Rueger, D.C., and Charness, M.E. (1993). Osteogenic protein-1 regulates L1 and neural cell adhesion molecule gene expression in neural cells. J. Biol. Chem. 268, 25179-25205.
65. Placzek, M., Tessier-Lavigne, M., Jessell, T.M., and Dodd, J. (1990). Orientation of commissural axons in vitro in response to a floor plate-derived chemoattractant. Development 110, 19-30.
66. Placzek, M., Yamada, T., Tessier-Lavigne, M., Jessell, T.M., and Dodd, J. (1991). Control of dorsoventral pattern in vertebrate neural development: induction and polarizing properties of the floor plate. Dev. Suppl. 2, 105-122.
67. Postlethwaite, A., Raghow, R., Stricklin, G., Ballow, L., and Sampath, T. (1994). Osteogenic protein-1 a bone morphogenetic protein member of the TGFβ superfamily shares chemotactic properties but not fibrogenic properties with TGFβ. J. Cell Phys. 161, 562-570.
68. Ramon y Cajal, S. (1909). Histologie du Systeme Nerveux de l'Homme et des Vertebres. (Madrid: Consejo Superior de Investigaciones Cientificas).
69. Roelink, H., and Nusse, R. (1991). Expression of two members of the wnt family during mouse development - restricted temporal and spatial patterns in the developing neural tube. Genes Dev. 5, 381-388.
70. Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz, I., Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T.M., and Dodd, J. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
71. 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.
72. Serafini, T., Kennedy, T.E., Galko, M.J., Mirzyan, C.M., Jessell, T.M., and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
73. Serafini, T., Colamarino, S.A., Leonardo, E.D., Wang, H., Beddington, 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.
74. Shah, N.M., Groves, A.K., and Anderson, D.J. (1996). BMP2 and BMP4, but not BMP6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp. Neurol. 140, 331-343.
75. Shah, S., Skromne, I., Hume, C., Kessler, D., Lee, K.J., Stern, C., and Dodd, J. (1997). Misexpression of chick Vg1 in the marginal zone induces primitive streak formation. Development 124, 5127-5138.
76. Silos-Santiago, I., and Snider, W.D. (1992). Development of commissural neurons in the embryonic rat spinal cord. J. Comp. Neurol. 325, 514-526.
77. Snow, D.M., Lemmon, V., Carrino, D.A., Caplan, A.I., and Silver, J. (1990a). Sulphated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 109, 111-130.
78. Snow, D.M., Steindler, D.A., and Silver, J. (1990b). Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in the development of an axon barrier. Dev. Biol. 138, 359-376.
79. Spiegelman, B., Lopata, M.A., and Kirschner, M.W. (1979). Aggregation of micrtuble initiation sites preceding neurite outgrowth in mouse neuroblastoma cells. Cell 16, 253-263.
80. Stern, C.D., Ireland, G.W., Herrick, S.E., Gherardi, E., Gray, J., Perryman, M., and Stoker, M. (1990). Epithelial scatter factor and development of the chick embryonic axis. Development 110, 1271-1284.
81. Stoeckli, E.T., and Landmesser, L.T. (1995). Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14, 1165-1179.
82. Tanabe, Y., and Jessell, T.M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
83. Tanaka, E., and Sabry, J. (1995). Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83, 171-176.
84. 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 I and bone morphogenetic protein-4. J. Biol. Chem. 269, 16985-16988.
85. Tessier-Lavigne, M., and Goodman, C.S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
86. Tessier-Lavigne, M., Placzek, M., Lumsden, A., Dodd, J., and Jessell, T.M. (1988). Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336, 775-778.
87. Vukicevic, S., Latin, V., Chen, P., Batorsky, R., Reddi, A.M., and Sampath, T.K. (1994). Localization of osteogenic protein-1 (bone morphogenetic protein-7) during human embryonic development: high affinity binding to basement membranes. Biochem. Biophys. Res. Commun. 198, 693-700.
88. Wang, H.U., and Anderson, D.J. (1997). Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth. Neuron 18, 383-396.
89. Wentworth, L.E. (1984). The development of the cervical spinal cord of the mouse embryo. II. A Golgi analysis of sensory, commissural and association cell differentiation. J. Comp. Neurol. 222, 96-115.
90. Whitman, M. (1997). Signal transduction. Feedback from inhibitory SMADs. Nature 389, 549-551.
91. Yaginuma, H., Homma, S., Kunzi, R., and Oppenheim, R.W. (1991). Pathfinding by growth cones of C interneurons in the chick embryo spinal cord: a light and electron microscopic study. J. Comp. Neurol. 304, 78-102.
92. Yamashita, H., ten Dijke, P., Huylebroeck, D., Sampath, T.K., Andries, M., Smith, J.C., Heldin, C.H., and Miyazono, K. (1995). Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130, 217-226.
93. Zimmerman, L.B., De Jesus-Escobar, J.M., and Harland, R.M. (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606.