TGFβ ligands promote the initiation of retinal ganglion cell dendrites in vitro and in vivo

Molecular and Cellular Neuroscience

Volumn 37, Issue 2, 2008, Pages 247-260

  Hocking, Jennifer C ^a   Hehr, Carrie L ^a   Chang, Ruoh Yeng ^a   Johnston, Jillian ^a   McFarlane, Sarah ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

BMP; Dendrite development; GDF; TGF ; Xenopus

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; GENE PRODUCT; TRANSFORMING GROWTH FACTOR BETA; BONE MORPHOGENETIC PROTEIN; GDF11 PROTEIN, HUMAN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DENDRITE; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL STIMULATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA GANGLION CELL; XENOPUS; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; FEMALE; METABOLISM; OOCYTE; PHYSIOLOGY; PRENATAL DEVELOPMENT; RETINA; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; XENOPUS LAEVIS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITES; FEMALE; OOCYTES; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; XENOPUS LAEVIS;

EID: 38649103445     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.09.011     Document Type: Article

References (74)

1. Ai X., Cappuzzello J., and Hall A.K. Activin and bone morphogenetic proteins induce calcitonin gene-related peptide in embryonic sensory neurons in vitro. Mol. Cell. Neurosci. 14 (1999) 506-518
2. Andersson O., Reissmann E., and Ibanez C.F. Growth differentiation factor 11 signals through the transforming growth factor-beta receptor ALK5 to regionalize the anterior-posterior axis. EMBO Rep. 7 (2006) 831-837
3. Bauch H., Stier H., and Schlosshauer B. Axonal versus dendritic outgrowth is differentially affected by radial glia in discrete layers of the retina. J. Neurosci. 18 (1998) 1774-1785
4. Beck H.N., Drahushuk K., Jacoby D.B., Higgins D., and Lein P.J. Bone morphogenetic protein-5 (BMP-5) promotes dendritic growth in cultured sympathetic neurons. BMC Neurosci. 2 (2001) 12
5. Belecky-Adams T., and Adler R. Developmental expression patterns of bone morphogenetic proteins, receptors, and binding proteins in the chick retina. J. Comp. Neurol. 430 (2001) 562-572
6. Butler S.J., and Dodd J. A role for BMP heterodimers in roof plate-mediated repulsion of commissural axons. Neuron 38 (2003) 389-401
7. Carri N.G., Bengtsson H., Charette M.F., and Ebendal T. BMPR-II expression and OP-1 effects in developing chicken retinal explants. NeuroReport 9 (1998) 1097-1101
8. Chalazonitis A., D'Autreaux F., Guha U., Pham T.D., Faure C., Chen J.J., Roman D., Kan L., Rothman T.P., Kessler J.A., and Gershon M.D. Bone morphogenetic protein-2 and -4 limit the number of enteric neurons but promote development of a TrkC-expressing neurotrophin-3-dependent subset. J. Neurosci. 24 (2004) 4266-4282
9. Chen Y.Y., Hehr C.L., Atkinson-Leadbeater K., Hocking J.C., and McFarlane S. Targeting of retinal axons requires the metalloproteinase ADAM10. J. Neurosci. 27 (2007) 8448-8456
10. Cohen-Cory S., and Fraser S.E. BDNF in the development of the visual system of Xenopus. Neuron 12 (1994) 747-761
11. Cohen-Cory S., Escandon E., and Fraser S.E. The cellular patterns of BDNF and trkB expression suggest multiple roles for BDNF during Xenopus visual system development. Dev. Biol. 179 (1996) 102-115
12. de Caestecker M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev. 15 (2004) 1-11
13. Dotti C.G., Sullivan C.A., and Banker G.A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8 (1988) 1454-1468
14. Dudley A.T., Lyons K.M., and Robertson E.J. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9 (1995) 2795-2807
15. Fenstermaker V., Chen Y., Ghosh A., and Yuste R. Regulation of dendritic length and branching by semaphorin 3A. J. Neurobiol. 58 (2004) 403-412
16. Ferguson, S., 2000. GABA and retino-tectal development. Thesis/Dissertation, University of Calgary.
17. Franke A.G., Gubbe C., Beier M., and Duenker N. Transforming growth factor-beta and bone morphogenetic proteins: cooperative players in chick and murine programmed retinal cell death. J. Comp. Neurol. 495 (2006) 263-278
18. Frisch A., and Wright C.V. XBMPRII, a novel Xenopus type II receptor mediating BMP signaling in embryonic tissues. Development 125 (1998) 431-442
19. Fujisawa H., Takagi S., and Hirata T. Growth-associated expression of a membrane protein, neuropilin, in Xenopus optic nerve fibers. Dev. Neurosci. 17 (1995) 343-349
20. Fukata Y., Kimura T., and Kaibuchi K. Axon specification in hippocampal neurons. Neurosci. Res. 43 (2002) 305-315
21. Furuta Y., and Hogan B.L. BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12 (1998) 3764-3775
22. Gascon E., Dayer A.G., Sauvain M.O., Potter G., Jenny B., De Roo M., Zgraggen E., Demaurex N., Muller D., and Kiss J.Z. GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J. Neurosci. 26 (2006) 12956-12966
23. Goldberg J.L. Intrinsic neuronal regulation of axon and dendrite growth. Curr. Opin. Neurobiol. 14 (2004) 551-557
24. Goldberg J.L., Espinosa J.S., Xu Y., Davidson N., Kovacs G.T., and Barres B.A. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33 (2002) 689-702
25. Goldberg J.L., Klassen M.P., Hua Y., and Barres B.A. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 296 (2002) 1860-1864
26. Gratacos E., Checa N., and Alberch J. Bone morphogenetic protein-2, but not bone morphogenetic protein-7, promotes dendritic growth and calbindin phenotype in cultured rat striatal neurons. Neuroscience 104 (2001) 783-790
27. Guo X., Rueger D., and Higgins D. Osteogenic protein-1 and related bone morphogenetic proteins regulate dendritic growth and the expression of microtubule-associated protein-2 in rat sympathetic neurons. Neurosci. Lett. 245 (1998) 131-134
28. Hanel M.L., and Hensey C. Eye and neural defects associated with loss of GDF6. BMC Dev. Biol. 6 (2006) 43
29. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36 (1991) 685-695
30. Harris W.A., and Messersmith S.L. Two cellular inductions involved in photoreceptor determination in the Xenopus retina. Neuron 9 (1992) 357-372
31. Hemmati-Brivanlou A., and Melton D.A. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature 359 (1992) 609-614
32. Hocking J.C., and McFarlane S. Expression of Bmp ligands and receptors in the developing Xenopus retina. Int. J. Dev. Biol. 51 (2007) 161-165
33. Holt C.E. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. J. Neurosci. 9 (1989) 3123-3145
34. Holt C.E., Garlick N., and Cornel E. Lipofection of cDNAs in the embryonic vertebrate central nervous system. Neuron 4 (1990) 203-214
35. Hsu D.R., Economides A.N., Wang X., Eimon P.M., and Harland R.M. The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1 (1998) 673-683
36. Huillard E., Laugier D., and Marx M. Defects in chicken neuroretina misexpressing the BMP antagonist Drm/Gremlin. Dev. Biol. 283 (2005) 335-344
37. Jan Y.N., and Jan L.Y. The control of dendrite development. Neuron 40 (2003) 229-242
38. Kalyani A.J., Piper D., Mujtaba T., Lucero M.T., and Rao M.S. Spinal cord neuronal precursors generate multiple neuronal phenotypes in culture. J. Neurosci. 18 (1998) 7856-7868
39. Kerrison J.B., Lewis R.N., Otteson D.C., and Zack D.J. Bone morphogenetic proteins promote neurite outgrowth in retinal ganglion cells. Mol. Vis. 11 (2005) 208-215
40. Kim J., Wu H.H., Lander A.D., Lyons K.M., Matzuk M.M., and Calof A.L. GDF11 controls the timing of progenitor cell competence in developing retina. Science 308 (2005) 1927-1930
41. Le Roux P., Behar S., Higgins D., and Charette M. OP-1 enhances dendritic growth from cerebral cortical neurons in vitro. Exp. Neurol. 160 (1999) 151-163
42. Lein P., Johnson M., Guo X., Rueger D., and Higgins D. Osteogenic protein-1 induces dendritic growth in rat sympathetic neurons. Neuron 15 (1995) 597-605
43. Lilienbaum A., Reszka A.A., Horwitz A.F., and Holt C.E. Chimeric integrins expressed in retinal ganglion cells impair process outgrowth in vivo. Mol. Cell. Neurosci. 6 (1995) 139-152
44. Liu J., Wilson S., and Reh T. BMP receptor 1b is required for axon guidance and cell survival in the developing retina. Dev. Biol. 256 (2003) 34-48
45. Lom B., and Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J. Neurosci. 19 (1999) 9928-9938
46. Lom B., Cogen J., Sanchez A.L., Vu T., and Cohen-Cory S. Local and target-derived brain-derived neurotrophic factor exert opposing effects on the dendritic arborization of retinal ganglion cells in vivo. J. Neurosci. 22 (2002) 7639-7649
47. Luo G., Hofmann C., Bronckers A.L., Sohocki M., Bradley A., and Karsenty G. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev. 9 (1995) 2808-2820
48. Mabie P.C., Mehler M.F., and Kessler J.A. Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J. Neurosci. 19 (1999) 7077-7088
49. Matus A. Microtubule-associated proteins and the determination of neuronal form. J. Physiol. ( Paris ) 84 (1990) 134-137
50. McFarlane S. Attraction vs. repulsion: the growth cone decides. Biochem. Cell. Biol. 78 (2000) 563-568
51. McFarlane S. Dendritic morphogenesis: building an arbor. Mol. Neurobiol. 22 (2000) 1-9
52. Merino R., Rodriguez-Leon J., Macias D., Ganan Y., Economides A.N., and Hurle J.M. The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 126 (1999) 5515-5522
53. Miyazono K., Maeda S., and Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 16 (2005) 251-263
54. Montague P.R., and Friedlander M.J. Morphogenesis and territorial coverage by isolated mammalian retinal ganglion cells. J. Neurosci. 11 (1991) 1440-1457
55. Mu X., Beremand P.D., Zhao S., Pershad R., Sun H., Scarpa A., Liang S., Thomas T.L., and Klein W.H. Discrete gene sets depend on POU domain transcription factor Brn3b/Brn-3.2/POU4f2 for their expression in the mouse embryonic retina. Development 131 (2004) 1197-1210
56. Murali D., Yoshikawa S., Corrigan R.R., Plas D.J., Crair M.C., Oliver G., Lyons K.M., Mishina Y., and Furuta Y. Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 132 (2005) 913-923
57. Nakashima M., Toyono T., Akamine A., and Joyner A. Expression of growth/differentiation factor 11, a new member of the BMP/TGFbeta superfamily during mouse embryogenesis. Mech. Dev. 80 (1999) 185-189
58. Nieuwkoop P.D., and Faber J. Normal Table of Xenopus laevis (1994), Garland Publishing Inc., New York
59. Nishimatsu S., Suzuki A., Shoda A., Murakami K., and Ueno N. Genes for bone morphogenetic proteins are differentially transcribed in early amphibian embryos. Biochem. Biophys. Res. Commun. 186 (1992) 1487-1495
60. Ohta K., Takagi S., Asou H., and Fujisawa H. Involvement of neuronal cell surface molecule B2 in the formation of retinal plexiform layers. Neuron 9 (1992) 151-161
61. Riehl R., Johnson K., Bradley R., Grunwald G.B., Cornel E., Lilienbaum A., and Holt C.E. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17 (1996) 837-848
62. Sakaguchi D.S., Murphey R.K., Hunt R.K., and Tompkins R. The development of retinal ganglion cells in a tetrapolid strain of Xenopus laevis: a morphological study utilizing intracellular dye injection. J. Comp. Neurol. 224 (1984) 231-251
63. Sakuta H., Takahashi H., Shintani T., Etani K., Aoshima A., and Noda M. Role of bone morphogenic protein 2 in retinal patterning and retinotectal projection. J. Neurosci. 26 (2006) 10868-10878
64. Shi Y., Katsev S., Cai C., and Evans S. BMP signaling is required for heart formation in vertebrates. Dev. Biol. 224 (2000) 226-237
65. Sternberger L.A., and Sternberger N.H. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 6126-6130
66. Stull N.D., Jung J.W., and Iacovitti L. Induction of a dopaminergic phenotype in cultured striatal neurons by bone morphogenetic proteins. Brain Res. Dev. Brain Res. 130 (2001) 91-98
67. Tropea M., Johnson M.I., and Higgins D. Glial cells promote dendritic development in rat sympathetic neurons in vitro. Glia 1 (1988) 380-392
68. Varley J.E., and Maxwell G.D. BMP-2 and BMP-4, but not BMP-6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp. Neurol. 140 (1996) 84-94
69. Wawersik S., Purcell P., Rauchman M., Dudley A.T., Robertson E.J., and Maas R. BMP7 acts in murine lens placode development. Dev. Biol. 207 (1999) 176-188
70. Webber C.A., Chen Y.Y., Hehr C.L., Johnston J., and McFarlane S. Multiple signaling pathways regulate FGF-2-induced retinal ganglion cell neurite extension and growth cone guidance. Mol. Cell. Neurosci. 30 (2005) 37-47
71. Withers G.S., Higgins D., Charette M., and Banker G. Bone morphogenetic protein-7 enhances dendritic growth and receptivity to innervation in cultured hippocampal neurons. Eur. J. Neurosci. 12 (2000) 106-116
72. Wordinger R.J., and Clark A.F. Bone morphogenetic proteins and their receptors in the eye. Exp. Biol. Med. (Maywood) 232 (2007) 979-992
73. Xia Y., Yu P.B., Sidis Y., Beppu H., Bloch K.D., Schneyer A.L., and Lin H.Y. Repulsive guidance molecule RGMa alters utilization of bone morphogenetic protein (BMP) type II receptors by BMP2 and BMP4. J. Biol. Chem. 282 (2007) 18129-18140
74. Zolessi F.R., Poggi L., Wilkinson C.J., Chien C.B., and Harris W.A. Polarization and orientation of retinal ganglion cells in vivo. Neural Develop. 1 (2006) 2