REVIEW

BMP signaling pathway and spinal cord development

  • Zhihui XIE ,
  • Nengyin SHENG ,
  • Naihe JING
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  • State Key Laboratory of Cell Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China

Received date: 18 Aug 2011

Accepted date: 22 Sep 2011

Published date: 01 Feb 2012

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

Zhihui XIE , Nengyin SHENG , Naihe JING . BMP signaling pathway and spinal cord development[J]. Frontiers in Biology, 2012 , 7(1) : 24 -29 . DOI: 10.1007/s11515-011-1178-7

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).
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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

11
Derynck R, Zhang Y E (2003). Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature, 425(6958): 577-584

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

15
Götz M, Huttner W B (2005). The cell biology of neurogenesis. Nat Rev Mol Cell Biol, 6(10): 777-788

DOI PMID

16
Guillemot F (2007). Spatial and temporal specification of neural fates by transcription factor codes. Development, 134(21): 3771-3780

DOI PMID

17
Guo X, Wang X F (2009). Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res, 19(1): 71-88

DOI PMID

18
Helms A W, Johnson J E (2003). Specification of dorsal spinal cord interneurons. Curr Opin Neurobiol, 13(1): 42-49

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

22
Jessell T M (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet, 1(1): 20-29

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

26
Lillien L (1998). Neural progenitors and stem cells: mechanisms of progenitor heterogeneity. Curr Opin Neurobiol, 8(1): 37-44

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

31
Louvi A, Artavanis-Tsakonas S (2006). Notch signalling in vertebrate neural development. Nat Rev Neurosci, 7(2): 93-102

DOI PMID

32
Maden M (2007). Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci, 8(10): 755-765

DOI PMID

33
Massagué J, Seoane J, Wotton D (2005). Smad transcription factors. Genes Dev, 19(23): 2783-2810

DOI PMID

34
McConnell S K (1995). Strategies for the generation of neuronal diversity in the developing central nervous system. J Neurosci, 15(11): 6987-6998

PMID

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

PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

45
Ruzinova M B, Benezra R (2003). Id proteins in development, cell cycle and cancer. Trends Cell Biol, 13(8): 410-418

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

50
Shi Y, Massagué J (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 113(6): 685-700

DOI PMID

51
Shirasaki R, Pfaff S L (2002). Transcriptional codes and the control of neuronal identity. Annu Rev Neurosci, 25(1): 251-281

DOI PMID

52
Temple S (2001). The development of neural stem cells. Nature, 414(6859): 112-117

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

57
Wrighton K H, Lin X, Feng X H (2009). Phospho-control of TGF-beta superfamily signaling. Cell Res, 19(1): 8-20

DOI PMID

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

DOI PMID

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

DOI PMID

60
Yokota Y (2001). Id and development. Oncogene, 20(58): 8290-8298

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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