BMP signaling pathway and spinal cord development

Zhihui XIE, Nengyin SHENG, Naihe JING

PDF(120 KB)
PDF(120 KB)
Front. Biol. ›› 2012, Vol. 7 ›› Issue (1) : 24-29. DOI: 10.1007/s11515-011-1178-7
REVIEW
REVIEW

BMP signaling pathway and spinal cord development

Author information +
History +

Abstract

The development of spinal cord is a precisely and sequentially regulated process, which is controlled by signaling pathways and transcription factors in each stage. Overwhelming data have shown the essential roles of BMP signaling in different stages of this developmental process. It is also clear that the proper functions of BMP signaling require its cross-talk with several other signaling pathways including Notch, Wnt and retinoic acid (RA) pathways. Here, we highlight the recent advancement in understanding the roles of BMP signaling during neurogenesis, neural tube patterning, axon development and glial differentiation in the spinal cord, and emphasize its integrations with other pathways during these processes.

Keywords

BMP / spinal cord / neurogenesis / patterning / glia

Cite this article

Download citation ▾
Zhihui XIE, Nengyin SHENG, Naihe JING. BMP signaling pathway and spinal cord development. Front Biol, 2012, 7(1): 24‒29 https://doi.org/10.1007/s11515-011-1178-7

References

[1]
Agius E, Decker Y, Soukkarieh C, Soula C, Cochard P (2010). Role of BMPs in controlling the spatial and temporal origin of GFAP astrocytes in the embryonic spinal cord. Dev Biol, 344(2): 611-620
CrossRef Pubmed Google scholar
[2]
Alvarez-Buylla A, García-Verdugo J M, Tramontin A D (2001). A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci, 2(4): 287-293
CrossRef Pubmed Google scholar
[3]
Bai G, Sheng N, Xie Z, Bian W, Yokota Y, Benezra R, Kageyama R, Guillemot F, Jing N (2007). Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev Cell 13: 283-297
[4]
Barnes A P, Polleux F (2009). Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci, 32(1): 347-381
CrossRef Pubmed Google scholar
[5]
Bertrand N, Castro D S, Guillemot F (2002). Proneural genes and the specification of neural cell types. Nat Rev Neurosci, 3(7): 517-530
CrossRef Pubmed Google scholar
[6]
Bonaguidi M A, McGuire T, Hu M, Kan L, Samanta J, Kessler J A (2005). LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development, 132(24): 5503-5514
CrossRef Pubmed Google scholar
[7]
Briscoe J, Pierani A, Jessell T M, Ericson J (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell, 101(4): 435-445
CrossRef Pubmed Google scholar
[8]
Britz O, Mattar P, Nguyen L, Langevin L M, Zimmer C, Alam S, Guillemot F, Schuurmans C (2006). A role for proneural genes in the maturation of cortical progenitor cells. Cereb Cortex, 16(Suppl 1): i138-i151
CrossRef Pubmed Google scholar
[9]
Chesnutt C, Burrus L W, Brown A M, Niswander L (2004). Coordinate regulation of neural tube patterning and proliferation by TGFbeta and WNT activity. Dev Biol, 274(2): 334-347
CrossRef Pubmed Google scholar
[10]
Ciani L, Salinas P C (2005). WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci, 6(5): 351-362
CrossRef Pubmed Google scholar
[11]
Derynck R, Zhang Y E (2003). Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature, 425(6958): 577-584
CrossRef Pubmed Google scholar
[12]
Eom D S, Amarnath S, Fogel J L, Agarwala S (2011). Bone morphogenetic proteins regulate neural tube closure by interacting with the apicobasal polarity pathway. Development, 138(15): 3179-3188
CrossRef Pubmed Google scholar
[13]
Fassier C, Hutt J A, Scholpp S, Lumsden A, Giros B, Nothias F, Schneider-Maunoury S, Houart C, Hazan J (2010). Zebrafish atlastin controls motility and spinal motor axon architecture via inhibition of the BMP pathway. Nat Neurosci, 13(11): 1380-1387
CrossRef Pubmed Google scholar
[14]
Feng X H, Derynck R (2005). Specificity and versatility in TGF-beta signaling through Smads. Annu Rev Cell Dev Biol, 21(1): 659-693
CrossRef Pubmed Google scholar
[15]
Götz M, Huttner W B (2005). The cell biology of neurogenesis. Nat Rev Mol Cell Biol, 6(10): 777-788
CrossRef Pubmed Google scholar
[16]
Guillemot F (2007). Spatial and temporal specification of neural fates by transcription factor codes. Development, 134(21): 3771-3780
CrossRef Pubmed Google scholar
[17]
Guo X, Wang X F (2009). Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res, 19(1): 71-88
CrossRef Pubmed Google scholar
[18]
Helms A W, Johnson J E (2003). Specification of dorsal spinal cord interneurons. Curr Opin Neurobiol, 13(1): 42-49
CrossRef Pubmed Google scholar
[19]
Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N, Gotoh Y (2004). The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development, 131(12): 2791-2801
CrossRef Pubmed Google scholar
[20]
Hirata H, Yoshiura S, Ohtsuka T, Bessho Y, Harada T, Yoshikawa K, Kageyama R (2002). Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science, 298(5594): 840-843
CrossRef Pubmed Google scholar
[21]
Ille F, Atanasoski S, Falk S, Ittner L M, Märki D, Büchmann-Møller S, Wurdak H, Suter U, Taketo M M, Sommer L (2007). Wnt/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord. Dev Biol, 304(1): 394-408
CrossRef Pubmed Google scholar
[22]
Jessell T M (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet, 1(1): 20-29
CrossRef Pubmed Google scholar
[23]
Kasai M, Satoh K, Akiyama T (2005). Wnt signaling regulates the sequential onset of neurogenesis and gliogenesis via induction of BMPs. Genes Cells, 10(8): 777-783
CrossRef Pubmed Google scholar
[24]
Lee K J, Jessell T M (1999). The specification of dorsal cell fates in the vertebrate central nervous system. Annu Rev Neurosci, 22(1): 261-294
CrossRef Pubmed Google scholar
[25]
Liem K F Jr, Jessell T M, Briscoe J (2000). Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development, 127(22): 4855-4866
Pubmed
[26]
Lillien L (1998). Neural progenitors and stem cells: mechanisms of progenitor heterogeneity. Curr Opin Neurobiol, 8(1): 37-44
CrossRef Pubmed Google scholar
[27]
Lin X, Liang Y Y, Sun B, Liang M, Shi Y, Brunicardi F C, Shi Y, Feng X H (2003). Smad6 recruits transcription corepressor CtBP to repress bone morphogenetic protein-induced transcription. Mol Cell Biol, 23(24): 9081-9093
CrossRef Pubmed Google scholar
[28]
Liu A, Niswander L A N R N. (2005). Bone morphogenetic protein signalling and vertebrate nervous system development. 6, 945-954.
[29]
Liu Y, Helms A W, Johnson J E (2004). Distinct activities of Msx1 and Msx3 in dorsal neural tube development. Development, 131(5): 1017-1028
CrossRef Pubmed Google scholar
[30]
Lönn P, Morén A, Raja E, Dahl M, Moustakas A (2009). Regulating the stability of TGFbeta receptors and Smads. Cell Res, 19(1): 21-35
CrossRef Pubmed Google scholar
[31]
Louvi A, Artavanis-Tsakonas S (2006). Notch signalling in vertebrate neural development. Nat Rev Neurosci, 7(2): 93-102
CrossRef Pubmed Google scholar
[32]
Maden M (2007). Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci, 8(10): 755-765
CrossRef Pubmed Google scholar
[33]
Massagué J, Seoane J, Wotton D (2005). Smad transcription factors. Genes Dev, 19(23): 2783-2810
CrossRef Pubmed Google scholar
[34]
McConnell S K (1995). Strategies for the generation of neuronal diversity in the developing central nervous system. J Neurosci, 15(11): 6987-6998
Pubmed
[35]
Megason S G, McMahon A P (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development, 129(9): 2087-2098
Pubmed
[36]
Mekki-Dauriac S, Agius E, Kan P, Cochard P (2002). Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development, 129(22): 5117-5130
Pubmed
[37]
Mizuguchi R, Sugimori M, Takebayashi H, Kosako H, Nagao M, Yoshida S, Nabeshima Y, Shimamura K, Nakafuku M (2001). Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron, 31(5): 757-771
CrossRef Pubmed Google scholar
[38]
Muroyama Y, Fujihara M, Ikeya M, Kondoh H, Takada S (2002). Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev, 16(5): 548-553
CrossRef Pubmed Google scholar
[39]
Muroyama Y, Fujiwara Y, Orkin S H, Rowitch D H (2005). Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature, 438(7066): 360-363
CrossRef Pubmed Google scholar
[40]
Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T (1999). Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science, 284(5413): 479-482
CrossRef Pubmed Google scholar
[41]
Novitch B G, Chen A I, Jessell T M (2001). Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron, 31(5): 773-789
CrossRef Pubmed Google scholar
[42]
Panchision D M, Pickel J M, Studer L, Lee S H, Turner P A, Hazel T G, McKay R D (2001). Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev, 15(16): 2094-2110
CrossRef Pubmed Google scholar
[43]
Polleux F, Ince-Dunn G, Ghosh A (2007). Transcriptional regulation of vertebrate axon guidance and synapse formation. Nat Rev Neurosci, 8(5): 331-340
CrossRef Pubmed Google scholar
[44]
Ruiz i Altaba A, Palma V, Dahmane N (2002). Hedgehog-Gli signalling and the growth of the brain. Nat Rev Neurosci, 3(1): 24-33
CrossRef Pubmed Google scholar
[45]
Ruzinova M B, Benezra R (2003). Id proteins in development, cell cycle and cancer. Trends Cell Biol, 13(8): 410-418
CrossRef Pubmed Google scholar
[46]
Samanta J, Kessler J A (2004). Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development, 131(17): 4131-4142
CrossRef Pubmed Google scholar
[47]
See J, Zhang X, Eraydin N, Mun S B, Mamontov P, Golden J A, Grinspan J B (2004). Oligodendrocyte maturation is inhibited by bone morphogenetic protein. Mol Cell Neurosci, 26(4): 481-492
CrossRef Pubmed Google scholar
[48]
Shen Q, Wang Y, Dimos J T, Fasano C A, Phoenix T N, Lemischka I R, Ivanova N B, Stifani S, Morrisey E E, Temple S (2006). The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci, 9(6): 743-751
CrossRef Pubmed Google scholar
[49]
Sheng N, Xie Z, Wang C, Bai G, Zhang K, Zhu Q, Song J, Guillemot F, Chen Y G, Lin A, Jing N (2010). Retinoic acid regulates bone morphogenic protein signal duration by promoting the degradation of phosphorylated Smad1. Proc Natl Acad Sci USA, 107(44): 18886-18891
CrossRef Pubmed Google scholar
[50]
Shi Y, Massagué J (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 113(6): 685-700
CrossRef Pubmed Google scholar
[51]
Shirasaki R, Pfaff S L (2002). Transcriptional codes and the control of neuronal identity. Annu Rev Neurosci, 25(1): 251-281
CrossRef Pubmed Google scholar
[52]
Temple S (2001). The development of neural stem cells. Nature, 414(6859): 112-117
CrossRef Pubmed Google scholar
[53]
Timmer J R, Wang C, Niswander L (2002). BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loop-helix transcription factors. Development, 129(10): 2459-2472
Pubmed
[54]
Vallstedt A, Muhr J, Pattyn A, Pierani A, Mendelsohn M, Sander M, Jessell T M, Ericson J (2001). Different levels of repressor activity assign redundant and specific roles to Nkx6 genes in motor neuron and interneuron specification. Neuron, 31(5): 743-755
CrossRef Pubmed Google scholar
[55]
Wine-Lee L, Ahn K J., Richardson R D, Mishina Y, Lyons K M., Crenshaw E B, (2004). Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord. 3rd Development, 131: 5393-5403
[56]
Woodhead G J, Mutch C A, Olson E C, Chenn A (2006). Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J Neurosci, 26(48): 12620-12630
CrossRef Pubmed Google scholar
[57]
Wrighton K H, Lin X, Feng X H (2009). Phospho-control of TGF-beta superfamily signaling. Cell Res, 19(1): 8-20
CrossRef Pubmed Google scholar
[58]
Xie Z, Chen Y, Li Z, Bai G, Zhu Y, Yan R, Tan F, Chen Y G, Guillemot F, Li L, Jing N (2011). Smad6 promotes neuronal differentiation in the intermediate zone of the dorsal neural tube by inhibition of the Wnt/beta-catenin pathway. Proc Natl Acad Sci USA, 108(29): 12119-12124
CrossRef Pubmed Google scholar
[59]
Yamauchi K, Phan K D, Butler S J (2008). BMP type I receptor complexes have distinct activities mediating cell fate and axon guidance decisions. Development, 135(6): 1119-1128
CrossRef Pubmed Google scholar
[60]
Yokota Y (2001). Id and development. Oncogene, 20(58): 8290-8298
CrossRef Pubmed Google scholar
[61]
Zechner D, Fujita Y, Hülsken J, Müller T, Walther I, Taketo M M, Crenshaw E B 3rd, Birchmeier W, Birchmeier C (2003). BETA-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol, 258(2): 406-418
CrossRef Pubmed Google scholar
[62]
Zechner D, Müller T, Wende H, Walther I, Taketo M M, Crenshaw E B 3rd, Treier M, Birchmeier W, Birchmeier C (2007). Bmp and Wnt/beta-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons. Dev Biol, 303(1): 181-190
CrossRef Pubmed Google scholar
[63]
Zhou Q, Anderson D J (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell, 109(1): 61-73
CrossRef Pubmed Google scholar
[64]
Zhou Q, Choi G, Anderson D J (2001). The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron, 31(5): 791-807
CrossRef Pubmed Google scholar
[65]
Zou H, Ho C, Wong K, Tessier-Lavigne M (2009). Axotomy-induced Smad1 activation promotes axonal growth in adult sensory neurons. J Neurosci, 29(22): 7116-7123
CrossRef Pubmed Google scholar

Acknowledgements

We apologize to all whose original work can't be cited in this review due to space limitations. We thank members of Dr. Jing's lab for comments and suggestions. This work was supported in part by the "Strategic Priority Research Program" of the Chinese Academy of Sciences (N XDA01010201), National Natural Science Foundation of China (Grand Nos. 30830034, 90919046), National Key Basic Research and Development Program of China (2007CB947101, 2008KR0695, 2009CB941100), Shanghai Key Project of Basic Science Research (08DJ1400501), and the Council of Shanghai Municipal Government for Science and Technology (088014199).

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
PDF(120 KB)

Accesses

Citations

Detail

Sections
Recommended

/