BMP receptor-activated Smads confer diverse functions during the development of the dorsal spinal cord

Developmental Biology

Volumn 367, Issue 2, 2012, Pages 216-227

  Hazen, V M ^a   Andrews, M G ^a   Umans, L ^b   Crenshaw, E B ^c,d   Zwijsen, A ^b   Butler, S J ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Axon guidance; Axon outgrowth; BMP signaling; BMPs; Bone morphogenetic proteins; Cell fate; Commissural axons; Dorsal spinal cord; Interneurons; Neural progenitors; Neurons; Receptor activated Smads; Smad1; Smad5; Smads; Spinal cord

Indexed keywords

BONE MORPHOGENETIC PROTEIN; RECEPTOR REGULATED SMAD PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL MATURATION; COMPARTMENT MODEL; CONTROLLED STUDY; EMBRYO; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPINAL CORD; SPINAL CORD NERVE CELL; TISSUE DISTRIBUTION;

EID: 84862133987     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.05.014     Document Type: Article

References (71)

1. Arnold S.J., Maretto S., Islam A., Bikoff E.K., Robertson E.J. Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo. Dev. Biol. 2006, 296:104-118.
2. Aubin J., Davy A., Soriano P. In vivo convergence of BMP and MAPK signaling pathways: impact of differential Smad1 phosphorylation on development and homeostasis. Genes Dev. 2004, 18:1482-1494.
3. Augsburger A., Schuchardt A., Hoskins S., Dodd J., Butler S. BMPs as mediators of roof plate repulsion of commissural neurons. Neuron 1999, 24:127-141.
4. Ball R.W., Warren-Paquin M., Tsurudome K., Liao E.H., Elazzouzi F., Cavanagh C., An B.S., Wang T.T., White J.H., Haghighi A.P. Retrograde BMP signaling controls synaptic growth at the NMJ by regulating trio expression in motor neurons. Neuron 2010, 66:536-549.
5. Birgbauer E., Dinsmore J.H., Winckler B., Lander A.D., Solomon F. Association of ezrin isoforms with the neuronal cytoskeleton. J. Neurosci. Res. 1991, 30:232-241.
6. Birgbauer E., Solomon F. A marginal band-associated protein has properties of both microtubule- and microfilament-associated proteins. J. Cell Biol. 1989, 109:1609-1620.
7. Bovolenta P., Dodd J. Guidance of commissural growth cones at the floor plate in embryonic rat spinal cord. Development 1990, 109:435-447.
8. Briscoe J., Pierani A., Jessell T.M., Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 2000, 101:435-445.
9. Burrill J.D., Moran L., Goulding M.D., Saueressig H. PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1+ interneurons that require PAX6 for their development. Development 1997, 124:4493-4503.
10. Butler S.J., Dodd J. A role for BMP heterodimers in roof plate-mediated repulsion of commissural axons. Neuron 2003, 38:389-401.
11. Chang H., Huylebroeck D., Verschueren K., Guo Q., Matzuk M.M., Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development (Cambridge, England) 1999, 126:1631-1642.
12. Charron F., Stein E., Jeong J., McMahon A.P., Tessier-Lavigne M. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 2003, 113:11-23.
13. Chesnutt C., Burrus L.W., Brown A.M., Niswander L. Coordinate regulation of neural tube patterning and proliferation by TGFbeta and WNT activity. Dev. Biol. 2004, 274:334-347.
14. Chizhikov V.V., Millen K.J. Roof plate-dependent patterning of the vertebrate dorsal central nervous system. Dev. Biol. 2005, 277:287-295.
15. Das R.M., Van Hateren N.J., Howell G.R., Farrell E.R., Bangs F.K., Porteous V.C., Manning E.M., McGrew M.J., Ohyama K., Sacco M.A., Halley P.A., Sang H.M., Storey K.G., Placzek M., Tickle C., Nair V.K., Wilson S.A. A robust system for RNA interference in the chicken using a modified microRNA operon. Dev. Biol. 2006, 294:554-563.
16. Dick A., Meier A., Hammerschmidt M. Smad1 and Smad5 have distinct roles during dorsoventral patterning of the zebrafish embryo. Dev. Dyn. 1999, 216:285-298.
17. Dodd J., Morton S.B., Karagogeos D., Yamamoto M., Jessell T.M. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1988, 1:105-116.
18. Ericson J., Briscoe J., Rashbass P., van Heyningen V., Jessell T.M. Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb. Symp. Quant. Biol. 1997, 62:451-466.
19. 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.
20. Feng X.H., Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 2005, 21:659-693.
21. Goold C.P., Davis G.W. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron 2007, 56:109-123.
22. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 1992, 195:231-272.
23. Hata A., Lagna G., Massague J., Hemmati-Brivanlou A. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev. 1998, 12:186-197.
24. Hazen V.M., Phan K.D., Hudiburgh S., Butler S.J. Inhibitory Smads differentially regulate cell fate specification and axon dynamics in the dorsal spinal cord. Dev. Biol. 2011, 356:566-575.
25. Heldin C.H., Miyazono K., ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997, 390:465-471.
26. Helms A.W., Abney A.L., Ben-Arie N., Zoghbi H.Y., Johnson J.E. Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. Development (Cambridge, England) 2000, 127:1185-1196.
27. Helms A.W., Johnson J.E. Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development (Cambridge, England) 1998, 125:919-928.
28. Heydemann A., Nguyen L.C., Crenshaw E.B. Regulatory regions from the Brn4 promoter direct LACZ expression to the developing forebrain and neural tube. Brain Res. Dev. Brain Res. 2001, 128:83-90.
29. Huang S., Tang B., Usoskin D., Lechleider R.J., Jamin S.P., Li C., Anzano M.A., Ebendal T., Deng C., Roberts A.B. Conditional knockout of the Smad1 gene. Genesis 2002, 32:76-79.
30. Imamura T., Takase M., Nishihara A., Oeda E., Hanai J., Kawabata M., Miyazono K. Smad6 inhibits signalling by the TGF-beta superfamily. Nature 1997, 389:622-626.
31. Imondi R., Jevince A.R., Helms A.W., Johnson J.E., Kaprielian Z. Mis-expression of L1 on pre-crossing spinal commissural axons disrupts pathfinding at the ventral midline. Mol. Cell Neurosci. 2007, 36:462-471.
32. Irving C., Malhas A., Guthrie S., Mason I. Establishing the trochlear motor axon trajectory: role of the isthmic organiser and Fgf8. Development (Cambridge, England) 2002, 129:5389-5398.
33. Kretzschmar M., Doody J., Massague J. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 1997, 389:618-622.
34. Kretzschmar M., Doody J., Timokhina I., Massague J. A mechanism of repression of TGFbeta/ Smad signaling by oncogenic Ras. Genes Dev. 1999, 13:804-816.
35. Kretzschmar M., Liu F., Hata A., Doody J., Massague J. The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 1997, 11:984-995.
36. Le Dreau G., Garcia-Campmany L., Rabadan M.A., Ferronha T., Tozer S., Briscoe J., Marti E. Canonical BMP7 activity is required for the generation of discrete neuronal populations in the dorsal spinal cord. Development (Cambridge, England) 2012, 139:259-268.
37. Lee K.J., Dietrich P., Jessell T.M. Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 2000, 403:734-740.
38. Lee K.J., Jessell T.M. The specification of dorsal cell fates in the vertebrate central nervous system. Annu. Rev. Neurosci. 1999, 22:261-294.
39. Lee K.J., Mendelsohn M., Jessell T.M. 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. 1998, 12:3394-3407.
40. Li W., Chen F., Nagarajan R.P., Liu X., Chen Y. Characterization of the DNA-binding property of Smad5. Biochem. Biophys. Res. Commun. 2001, 286:1163-1169.
41. Liem K.F., Jessell T.M., Briscoe J. Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development (Cambridge, England) 2000, 127:4855-4866.
42. 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.
43. Lyuksyutova A.I., Lu C.C., Milanesio N., King L.A., Guo N., Wang Y., Nathans J., Tessier-Lavigne M., Zou Y. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science (New York, N.Y) 2003, 302:1984-1988.
44. Macias-Silva M., Abdollah S., Hoodless P.A., Pirone R., Attisano L., Wrana J.L. MADR2 is a substrate of the TGFbeta receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 1996, 87:1215-1224.
45. Matei V., Pauley S., Kaing S., Rowitch D., Beisel K.W., Morris K., Feng F., Jones K., Lee J., Fritzsch B. Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev. Dyn. 2005, 234:633-650.
46. McCabe B.D., Marques G., Haghighi A.P., Fetter R.D., Crotty M.L., Haerry T.E., Goodman C.S., O'Connor M.B. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 2003, 39:241-254.
47. McReynolds L.J., Gupta S., Figueroa M.E., Mullins M.C., Evans T. Smad1 and Smad5 differentially regulate embryonic hematopoiesis. Blood 2007, 110:3881-3890.
48. Mori T., Kitano K., Terawaki S., Maesaki R., Fukami Y., Hakoshima T. Structural basis for CD44 recognition by ERM proteins. J. Biol. Chem. 2008, 283:29602-29612.
49. Moustakas A., Heldin C.H. The regulation of TGFbeta signal transduction. Development (Cambridge, England) 2009, 136:3699-3714.
50. Nakao A., Afrakhte M., Moren A., Nakayama T., Christian J.L., Heuchel R., Itoh S., Kawabata M., Heldin N.E., Heldin C.H., ten Dijke P. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 1997, 389:631-635.
51. Novitch B.G., Chen A.I., Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 2001, 31:773-789.
52. Orvis G.D., Jamin S.P., Kwan K.M., Mishina Y., Kaartinen V.M., Huang S., Roberts A.B., Umans L., Huylebroeck D., Zwijsen A., Wang D., Martin J.F., Behringer R.R. Functional redundancy of TGF-beta family type I receptors and receptor-Smads in mediating anti-Mullerian hormone-induced Mullerian duct regression in the mouse. Biol. Reprod. 2008, 78:994-1001.
53. Pangas S.A., Li X., Umans L., Zwijsen A., Huylebroeck D., Gutierrez C., Wang D., Martin J.F., Jamin S.P., Behringer R.R., Robertson E.J., Matzuk M.M. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol. Cell Biol. 2008, 28:248-257.
54. Parikh P., Hao Y., Hosseinkhani M., Patil S.B., Huntley G.W., Tessier-Lavigne M., Zou H. Regeneration of axons in injured spinal cord by activation of bone morphogenetic protein/Smad1 signaling pathway in adult neurons. Proc. Nat. Acad. Sci. USA 2011, 108:E99-E107.
55. Perron J.C., Dodd J. Inductive specification and axonal orientation of spinal neurons mediated by divergent bone morphogenetic protein signaling pathways. Neural Develop. 2011, 6:36.
56. Peterson R.S., Andhare R.A., Rousche K.T., Knudson W., Wang W., Grossfield J.B., Thomas R.O., Hollingsworth R.E., Knudson C.B. CD44 modulates Smad1 activation in the BMP-7 signaling pathway. J. Cell Biol. 2004, 166:1081-1091.
57. Phan K.D., Hazen V.M., Frendo M., Jia Z., Butler S.J. The bone morphogenetic protein roof plate chemorepellent regulates the rate of commissural axonal growth. J. Neurosci. 2010, 30:15430-15440.
58. Rousso D.L., Gaber Z.B., Wellik D., Morrisey E.E., Novitch B.G. Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 2008, 59:226-240.
59. Schaeren-Wiemers N., Gerfin-Moser A. 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 1993, 100:431-440.
60. Skaggs K., Martin D.M., Novitch B.G. Regulation of spinal interneuron development by the Olig-related protein Bhlhb5 and Notch signaling. Development (Cambridge, England) 2011, 138:3199-3211.
61. Tanabe Y., Jessell T.M. Diversity and pattern in the developing spinal cord. Science (New York, N.Y) 1996, 274:1115-1123.
62. Timmer J., Chesnutt C., Niswander L. The activin signaling pathway promotes differentiation of dI3 interneurons in the spinal neural tube. Dev. Biol. 2005, 285:1-10.
63. 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 (Cambridge, England) 2002, 129:2459-2472.
64. Tremblay K.D., Dunn N.R., Robertson E.J. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development (Cambridge, England) 2001, 128:3609-3621.
65. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., Pfaff S.L. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 1994, 79:957-970.
66. Umans L., Vermeire L., Francis A., Chang H., Huylebroeck D., Zwijsen A. Generation of a floxed allele of Smad5 for cre-mediated conditional knockout in the mouse. Genesis 2003, 37:5-11.
67. 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 (Cambridge, England) 2004, 131:5393-5403.
68. Yamauchi K., Phan K.D., Butler S.J. BMP type I receptor complexes have distinct activities mediating cell fate and axon guidance decisions. Development (Cambridge, England) 2008, 135:1119-1128.
69. Yamauchi, K., Varadarajan, S., Li, J.E., Butler, S.J. Type I BMP receptors moderate the rate of commissural axon extension through inhibition of cofilin activity. Submitted for publication.
70. Yanagisawa M., Nakashima K., Takeda K., Ochiai W., Takizawa T., Ueno M., Takizawa M., Shibuya H., Taga T. Inhibition of BMP2-induced, TAK1 kinase-mediated neurite outgrowth by Smad6 and Smad7. Genes Cells 2001, 6:1091-1099.
71. Zou H., Ho C., Wong K., Tessier-Lavigne M. Axotomy-induced Smad1 activation promotes axonal growth in adult sensory neurons. J. Neurosci. 2009, 29:7116-7123.