Role of BMPs in controlling the spatial and temporal origin of GFAP astrocytes in the embryonic spinal cord

Developmental Biology

Volumn 344, Issue 2, 2010, Pages 611-620

  Agius, Eric ^a   Decker, Yann ^b   Soukkarieh, Chadi ^c   Soula, Cathy ^a   Cochard, Philippe ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c DAMASCUS UNIVERSITY   (Syrian Arab Republic)

Author keywords

Astrocyte; BMP; Chick embryo; Development; Spinal cord; Wnt7b

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN REGION; CELL MIGRATION; CELL SPECIFICITY; CELLULAR DISTRIBUTION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEURAL TUBE; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPINAL CORD; TISSUE DISTRIBUTION; TISSUE SPECIFICITY;

VERTEBRATA;

EID: 77955272051     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.05.017     Document Type: Article

References (59)

1. Agius E., Soukkarieh C., Danesin C., Kan P., Takebayashi H., Soula C., Cochard P. Converse control of oligodendrocyte and astrocyte lineage development by Sonic hedgehog in the chick spinal cord. Dev. Biol. 2004, 270:308-321.
2. Agius, E., Soukkarieh, C., Decker, Y., Soula, C., Cochard, P., in preparation. Wnt7b a new astrocyte marker.
3. Battiste J., Helms A.W., Kim E.J., Savage T.K., Lagace D.C., Mandyam C.D., Eisch A.J., Miyoshi G., Johnson J.E. Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 2007, 134:285-293.
4. Braquart-Varnier C., Danesin C., Clouscard-Martinato C., Agius E., Escalas N., Benazeraf B., Ai X., Emerson C., Cochard P., Soula C. A subtractive approach to characterize genes with regionalized expression in the gliogenic ventral neuroepithelium: identification of chick sulfatase 1 as a new oligodendrocyte lineage gene. Mol. Cell. Neurosci. 2004, 25:612-628.
5. Chandran S., Kato H., Gerreli D., Compston A., Svendsen C.N., Allen N.D. FGF-dependent generation of oligodendrocytes by a hedgehog-independent pathway. Development 2003, 130:6599-6609.
6. Chen H.L., Panchision D.M. Concise review: bone morphogenetic protein pleiotropism in neural stem cells and their derivatives-alternative pathways, convergent signals. Stem Cells 2007, 25:63-68.
7. Cheng X., Wang Y., He Q., Qiu M., Whittemore S.R., Cao Q. Bone morphogenetic protein signaling and olig1/2 interact to regulate the differentiation and maturation of adult oligodendrocyte precursor cells. Stem Cells 2007, 25:3204-3214.
8. Chizhikov V.V., Millen K.J. Roof plate-dependent patterning of the vertebrate dorsal central nervous system. Dev. Biol. 2005, 277:287-295.
9. Colak D., Mori T., Brill M.S., Pfeifer A., Falk S., Deng C., Monteiro R., Mummery C., Sommer L., Gotz M. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J. Neurosci. 2008, 28:434-446.
10. Danesin C., Agius E., Escalas N., Ai X., Emerson C., Cochard P., Soula C. Ventral neural progenitors switch toward an oligodendroglial fate in response to increased Sonic hedgehog (Shh) activity: involvement of Sulfatase 1 in modulating Shh signaling in the ventral spinal cord. J. Neurosci. 2006, 26:5037-5048.
11. Davis S., Miura S., Hill C., Mishina Y., Klingensmith J. BMP receptor IA is required in the mammalian embryo for endodermal morphogenesis and ectodermal patterning. Dev. Biol. 2004, 270:47-63.
12. de Vitry F., Picart R., Jacque C., Tixier-Vidal A. Glial fibrillary acidic protein. A cellular marker of tanycytes in the mouse hypothalamus. Dev. Neurosci. 1981, 4:457-460.
13. Deneen B., Ho R., Lukaszewicz A., Hochstim C.J., Gronostajski R.M., Anderson D.J. The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 2006, 52:953-968.
14. Dessaud E., McMahon A.P., Briscoe J. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 2008, 135:2489-2503.
15. Ericson J., Morton S., Kawakami A., Roelink H., Jessell T.M. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 1996, 87:661-673.
16. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 1997, 90:169-180.
17. Faure S., Lee M.A., Keller T., ten Dijke P., Whitman M. Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development. Development 2000, 127:2917-2931.
18. Faure S., de Santa Barbara P., Roberts D.J., Whitman M. Endogenous patterns of BMP signaling during early chick development. Dev. Biol. 2002, 244:44-65.
19. Fu H., Cai J., Clevers H., Fast E., Gray S., Greenberg R., Jain M.K., Ma Q., Qiu M., Rowitch D.H., et al. A genome-wide screen for spatially restricted expression patterns identifies transcription factors that regulate glial development. J. Neurosci. 2009, 29:11399-11408.
20. Garcia-Dominguez M., Poquet C., Garel S., Charnay P. Ebf gene function is required for coupling neuronal differentiation and cell cycle exit. Development 2003, 130:6013-6025.
21. Garel S., Marin F., Mattei M.G., Vesque C., Vincent A., Charnay P. Family of Ebf/Olf-1-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev. Dyn. 1997, 210:191-205.
22. Gomes W.A., Mehler M.F., Kessler J.A. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev. Biol. 2003, 255:164-177.
23. Goulding M.D., Lumsden A., Gruss P. Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord. Development 1993, 117:1001-1016.
24. Gross R.E., Mehler M.F., Mabie P.C., Zang Z., Santschi L., Kessler J.A. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 1996, 17:595-606.
25. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. 1951 [classical article] [see comments]. Dev. Dyn. 1992, 195:231-272.
26. Hochstim C., Deneen B., Lukaszewicz A., Zhou Q., Anderson D.J. Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 2008, 133:510-522.
27. Itasaki N., Bel-Vialar S., Krumlauf R. Shocking' developments in chick embryology: electroporation and in ovo gene expression. Nat. Cell Biol. 1999, 1:E203-E207.
28. Ivanova A., Agochiya M., Amoyel M., Richardson W.D. Receptor tyrosine phosphatase zeta/beta in astrocyte progenitors in the developing chick spinal cord. Gene Expr. Patterns 2004, 4:161-166.
29. Kessaris N., Pringle N., Richardson W.D. Specification of CNS glia from neural stem cells in the embryonic neuroepithelium. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:71-85.
30. Kim C.H., Ueshima E., Muraoka O., Tanaka H., Yeo S.Y., Huh T.L., Miki N. Zebrafish elav/HuC homologue as a very early neuronal marker. Neurosci. Lett. 1996, 216:109-112.
31. Li W., Cogswell C.A., LoTurco J.J. Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J. Neurosci. 1998, 18:8853-8862.
32. Liem K.F., Tremml G., Jessell T.M. A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 1997, 91:127-138.
33. Liu A., Niswander L.A. Signalling in development: bone morphogenetic protein signalling and vertebrate nervous system development. Nat. Rev. Neurosci. 2005, 6:945-954.
34. Liu S.Y., Zhang Z.Y., Song Y.C., Qiu K.J., Zhang K.C., An N., Zhou Z., Cai W.Q., Yang H. SVZa neural stem cells differentiate into distinct lineages in response to BMP4. Exp. Neurol. 2004, 190:109-121.
35. Liu Y., Helms A.W., Johnson J.E. Distinct activities of Msx1 and Msx3 in dorsal neural tube development. Development 2004, 131:1017-1028.
36. Mabie P.C., Mehler M.F., Marmur R., Papavasiliou A., Song Q., Kessler J.A. Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J. Neurosci. 1997, 17:4112-4120.
37. Mabie P.C., Mehler M.F., Kessler J.A. Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J. Neurosci. 1999, 19:7077-7088.
38. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
39. Megason S.G., McMahon A.P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 2002, 129:2087-2098.
40. Melton K.R., Iulianella A., Trainor P.A. Gene expression and regulation of hindbrain and spinal cord development. Front. Biosci. 2004, 9:117-138.
41. Panchision D.M., Pickel J.M., Studer L., Lee S.H., Turner P.A., Hazel T.G., McKay R.D. Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev. 2001, 15:2094-2110.
42. Persson U., Izumi H., Souchelnytskyi S., Itoh S., Grimsby S., Engstrom U., Heldin C.H., Funa K., ten Dijke P. The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 1998, 434:83-87.
43. Pringle N.P., Yu W.P., Howell M., Colvin J.S., Ornitz D.M., Richardson W.D. Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 2003, 130:93-102.
44. Rowitch D.H. Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 2004, 5:409-419.
45. Sahni V., Mukhopadhyay A., Tysseling V., Hebert A., Birch D., McGuire T.L., Stupp S.I., Kessler J.A. BMPR1a and BMPR1b signaling exert opposing effects on gliosis after spinal cord injury. J. Neurosci. 2010, 30:1839-1855.
46. Sakurai K., Osumi N. The neurogenesis-controlling factor, Pax6, inhibits proliferation and promotes maturation in murine astrocytes. J. Neurosci. 2008, 28:4604-4612.
47. See J., Mamontov P., Ahn K., Wine-Lee L., Crenshaw E.B., Grinspan J.B. BMP signaling mutant mice exhibit glial cell maturation defects. Mol. Cell. Neurosci. 2007, 35:171-182.
48. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
49. Shibata T., Yamada K., Watanabe M., Ikenaka K., Wada K., Tanaka K., Inoue Y. Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J. Neurosci. 1997, 17:9212-9219.
50. Smith W.C., Knecht A.K., Wu M., Harland R.M. Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature 1993, 361:547-549.
51. Sommer L., Ma Q., Anderson D.J. Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 1996, 8:221-241.
52. Soula C., Danesin C., Kan P., Grob M., Poncet C., Cochard P. Distinct sites of origin of oligodendrocytes and somatic motoneurons in the chick spinal cord: oligodendrocytes arise from Nkx2.2-expressing progenitors by a Shh-dependent mechanism. Development 2001, 128:1369-1379.
53. Stolt C.C., Lommes P., Sock E., Chaboissier M.C., Schedl A., Wegner M. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev. 2003, 17:1677-1689.
54. Stolt C.C., Schmitt S., Lommes P., Sock E., Wegner M. Impact of transcription factor Sox8 on oligodendrocyte specification in the mouse embryonic spinal cord. Dev. Biol. 2005, 281:309-317.
55. Timmer J.R., Wang C., Niswander L. BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loop-helix transcription factors. Development 2002, 129:2459-2472.
56. Wilkinson D.G. In Situ Hybridization: A Practical Approach 1992, 75-82. IRL Press, Oxford.
57. Wilson L., Maden M. The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev. Biol. 2005, 282:1-13.
58. Wine-Lee L., Ahn K.J., Richardson R.D., Mishina Y., Lyons K.M., Crenshaw E.B. Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord. Development 2004, 131:5393-5403.
59. Yi S.E., Daluiski A., Pederson R., Rosen V., Lyons K.M. The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 2000, 127:621-630.