Pleiotropic effects of the bone morphogenetic proteins on development of the enteric nervous system

Developmental Neurobiology

Volumn 72, Issue 6, 2012, Pages 843-856

  Chalazonitis, Alcmène ^a   Kessler, John A ^b  

^a New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Enteric nervous system; ErbB3; GGF 2; Neural crest; Neurotransmitters; Noggin; NT 3; P75 NTR; PSA NCAM; PSmad1 5 8; Transgenic mice; TrkC

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; EPIDERMAL GROWTH FACTOR RECEPTOR 3; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; NERVE CELL ADHESION MOLECULE; NEUROTRANSMITTER; NEUROTROPHIN 3 RECEPTOR;

ANTERIOR POSTERIOR AXIS; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; FETUS DEVELOPMENT; GANGLION; GLIA; HUMAN; INTESTINE INNERVATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEUROBIOLOGY; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SMOOTH MUSCLE;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; ENTERIC NERVOUS SYSTEM; NEURAL CREST; NEUROGLIA; NEURONS;

EID: 84860895274     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22002     Document Type: Article

References (75)

1. Attisano L, Wrana JL. 2000. Smads as transcriptional comodulators. Curr Opin Cell Biol 12: 235-243.
2. Baetge G, Pintar JE, Gershon MD. 1990. Transiently catecholaminergic (TC) cells in the bowel of fetal rats and mice: Precursors of non-catecholaminergic enteric neurons. Dev Biol 141: 353-380.
3. Black IB, Bloom FE, Hendry IA, Iversen LL. 1971. Growth and development of sympathetic ganglion: Maturation of transmitter enzymes and synapse formation in the mouse superior cervical ganglion. J Physiol 215: 24P-25P.
4. Brewer KC, Mwizerva O, Goldstein AM. 2005. BMPRIA is a promising marker for evaluating ganglion cells in the enteric nervous system-A pilot study. Hum Pathol 36: 1120-1126.
5. Bruses JL, Rutishauser U. 2001. Roles, regulation and mechanism of polysialic acid function during neural development. Biochimie 83: 635-643.
6. Burns AJ, Thapar N. 2006. Advances in ontogeny of the enteric nervous system. Neurogastroenterol Motil 18: 876-887.
7. Chalazonitis A. 2004. Neurotrophin-3 in the development of the enteric nervous system. Prog Brain Res 146: 243-263.
8. Chalazonitis A, D'Autreaux F, Guha U, Pham TD, Faure C, Chen JJ, Roman D, et al. 2004. 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: 4266-4282.
9. Chalazonitis A, D'Autreaux F, Pham TD, Kessler JA, Gershon MD. 2011a. Bone morphogenetic proteins regulate enteric gliogenesis by modulating ErbB3 signaling. Dev Biol 350: 64-79.
10. Chalazonitis A, Pham TD, Li Z, Roman D, Guha U, Gomes W, Kan L, et al. 2008. Bone morphogenetic protein regulation of enteric neuronal phenotypic diversity: Relationship to timing of cell cycle exit. J Comp Neurol 509: 474-492.
11. Chalazonitis A, Pham TD, Rothman TP, DiStefano PS, Bothwell M, Blair-Flynn J, Tessarollo L, et al. 2001. Neurotrophin-3 is required for the survival-differentiation of subsets of developing enteric neurons. J Neurosci 21: 5620-5636.
12. Chalazonitis A, Rothman TP, Chen J, Gershon MD. 1998b. Age-dependent differences in the effects of GDNF and NT-3 on the development of neurons and glia from neural crest-derived precursors immunoselected from the fetal rat gut: Expression of GFRalpha-1 in vitro and in vivo. Dev Biol 204: 385-406.
13. Chalazonitis A, Rothman TP, Chen J, Lamballe F, Barbacid M, Gershon MD. 1994. Neurotrophin-3 induces neural crest-derived cells from fetal rat gut to develop in vitro as neurons or glia. J Neurosci 14: 6571-6584.
14. Chalazonitis A, Rothman TP, Chen J, Vinson EN, MacLennan AJ, Gershon MD. 1998a. Promotion of the development of enteric neurons and glia by neuropoietic cytokines: Interactions with neurotrophin-3. Dev Biol 198: 343-365.
15. Chalazonitis A, Tang AA, Shang Y, Pham TD, Hsieh I, Setlik W, Gershon MD, et al. 2011b. Homeodomain interacting protein kinase 2 regulates postnatal development of enteric dopaminergic neurons and glia via BMP signaling. J Neurosci 31: 13746-13757.
16. Chalazonitis A, Tennyson VM, Kibbey MC, Rothman TP, Gershon MD. 1997. The alpha1 subunit of laminin-1 promotes the development of neurons by interacting with LBP110 expressed by neural crest-derived cells immunoselected from the fetal mouse gut. J Neurobiol 33: 118-138.
17. Charter NW, Mahal LK, Koshland DEJr, Bertozzi CR. 2002. Differential effects of unnatural sialic acids on the polysialylation of the neural cell adhesion molecule and neuronal behavior. J Biol Chem 277: 9255-9261.
18. Cho KW, Blitz IL. 1998. BMPs, Smads and metalloproteases: Extracellular and intracellular modes of negative regulation. Curr Opin Gen Dev 8: 443-449.
19. Cochard P, Goldstein M, Black IB. 1978. Ontogenetic appearance and disappearance of tyrosine hydroxylase and catecholamines in the rat embryo. Proc Natl Acad Sci USA 75: 2986-2990.
20. Crossin KL, Krushel LA. 2000. Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn 218: 260-279.
21. De Santa Barbara P, Williams J, Goldstein AM, Doyle AM, Nielsen C, Winfield S, Faure S, et al. 2005. Bone morphogenetic protein signaling pathway plays multiple roles during gastrointestinal tract development. Dev Dyn 234: 312-322.
22. Eckhardt M, Bukalo O, Chazal G, Wang L, Goridis C, Schachner M, Gerardy-Schahn R, et al. 2000. Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J Neurosci 20: 5234-5244.
23. Eisaki A, Kuroda H, Fukui A, Asashima M. 2000. XSIP1, a member of two-handed zinc finger proteins, induced anterior neural markers in Xenopus laevis animal cap. Biochem Biophys Res Commun 271: 151-157.
24. Epstein ML, Poulsen KT, Thiboldeaux R. 1991. Formation of ganglia in the gut of the chick embryo. J Comp Neurol 307: 189-199.
25. Faure C, Chalazonitis A, Rheaume C, Bouchard G, Sampathkumar SG, Yarema KJ, Gershon MD. 2007. Gangliogenesis in the enteric nervous system: Roles of the polysialylation of the neural cell adhesion molecule and its regulation by bone morphogenetic protein-4. Dev Dyn 236: 44-59.
26. Fu M, Lui VC, Sham MH, Pachnis V, Tam PK. 2004. Sonic hedgehog regulates the proliferation, differentiation, and migration of enteric neural crest cells in gut. J Cell Biol 166: 673-684.
27. Fu M, Vohra BP, Wind D, Heuckeroth RO. 2006. BMP signaling regulates murine enteric nervous system precursor migration, neurite fasciculation, and patterning via altered Ncam1 polysialic acid addition. Dev Biol 299: 137-150.
28. Furness JB. 2006. The Enteric Nervous System. Blackwell Publishing. Narayana Press, Odder, Denmark.
29. Gershon MD. 2005. Nerves, reflexes, and the enteric nervous system: Pathogenesis of the irritable bowel syndrome. J Clin Gastroenterol 39: S184-S193.
30. Gershon MD. 2010. Developmental determinants of the independence and complexity of the enteric nervous system. Trends Neurosci 33: 446-456.
31. Goldstein AM, Brewer KC, Doyle AM, Nagy N, Roberts DJ. 2005. BMP signaling is necessary for neural crest cell migration and ganglion formation in the enteric nervous system. Mech Dev 122: 821-833.
32. Gomes WA, Mehler MF, Kessler JA. 2003. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 255: 164-177.
33. Grosskortenhaus R, Pearson BJ, Marusich A, Doe CQ. 2005. Regulation of temporal identity transitions in Drosophila neuroblasts. Dev Cell 8: 193-202.
34. Guha U, Mecklenburg L, Cowin P, Kan L, O'Guin WM, D'Vizio D, Pestell RG, et al. 2004. Bone morphogenetic protein signaling regulates postnatal hair follicle differentiation and cycling. Am J Pathol 165: 729-740.
35. Hao MM, Anderson RB, Kobayashi K, Whitington PM, Young HM. 2009. The migratory behavior of immature enteric neurons. Dev Neurobiol 69: 22-35.
36. Hao MM, Young HM. 2009. Development of enteric neuron diversity. J Cell Mol Med 13: 1193-1210.
37. Harada J, Kokura K, Kanei-Ishii C, Nomura T, Khan MM, Kim Y, Ishii S. 2003. Requirement of the corepressor homeodomain-interacting protein kinase 2 for ski-mediated inhibition of bone morphogenetic protein-induced transcriptional activation. J Biol Chem 278: 38998-39005.
38. Harris WA. 2003. Developmental biology: Clocking the birth of neurons. Nature 425: 568-569.
39. Hearn CJ, Murphy M, Newgreen D. 1998. GDNF and ET-3 differentially modulate the numbers of avian neural crest cells and enteric neurons in vitro. Dev Biol 197: 93-105.
40. Heuckeroth RO, Lampe PA, Johnson Jr. EM, Milbrandt J. 1998. Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev Biol 200: 116-129.
41. Hogan BLM. 1996. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Gen Dev 10: 1580-1594.
42. Karaosmanoglu T, Aygun B, Wade PR, Gershon MD. 1996. Regional differences in the number of neurons in the myenteric plexus of the guinea pig small intestine and colon: An evaluation of markers used to count neurons. Anat Rec 244: 470-480.
43. Le Douarin NM, Teillet MA. 1973. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol 30: 31-48.
44. Levanti MB, Esteban I, Ciriaco E, Perez-Pinera P, Cabo R, Garcia-Suarez O, Pardo B, et al. 2009. Enteric glial cells express full-length TrkB and depend on TrkB expression for normal development. Neurosci Lett 454: 16-21.
45. Mabie PC, Mehler MF, Kessler JA. 1999. Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci 19: 7077-7088.
46. Mahal LK, Charter NW, Angata K, Fukuda M, Koshland DEJr., Bertozzi CR. 2001. A small-molecule modulator of poly-alpha 2, 8-sialic acid expression on cultured neurons and tumor cells. Science 294: 380-381.
47. Marchionni MA, Goodearl ADJ, Chen MS, Bermingham-McDonogh O, Kirk C, Hendricks M, Danehy F, et al. 1993. Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362: 312-318.
48. Mehler MF, Mabie PC, Zhang D, Kessler JA. 1997. Bone morphogenetic proteins in the nervous system. TINS 20: 309-317.
49. Newgreen DF, Hartley L. 1995. Extracellular matrix and adhesive molecules in the early development of the gut and its innervation in normal and spotting lethal rat embryos. Acta Anat (Basel) 154: 243-260.
50. Nielsen C, Murtaugh LC, Chyung JC, Lassar A, Roberts DJ. 2001. Gizzard formation and the role of Bapx1. Dev Biol 231: 164-174.
51. Pearson BJ, Doe CQ. 2003. Regulation of neuroblast competence in Drosophila. Nature 425: 624-628.
52. Pham TD, Gershon MD, Rothman TP. 1991. Time of origin of neurons in the murine enteric nervous system: Sequence in relation to phenotype. J Comp Neurol 1991: 789-798.
53. Pisano JM, Colon-Hastings F, Birren SJ. 2000. Postmigratory enteric and sympathetic neural precursors share common, developmentally regulated, responses to BMP2. Dev Biol 227: 1-11.
54. Riethmacher D, Sonnenberg-Riethmacher E, Brinkmann V, Yamaai T, Lewin GR, Birchmeier C. 1997. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389: 725-730.
55. Roberts DJ. 2000. Molecular mechanisms of development of the gastrointestinal tract. Dev Dyn 219: 109-120.
56. Roberts DJ, Johnson RL, Burke AC, Nelson CE, Morgan BA, Tabin C. 1995. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121: 3163-3174.
57. Roberts DJ, Smith DM, Goff DJ, Tabin CJ. 1998. Epithelial-mesenchymal signaling during the regionalization of the chick gut. Development 125: 2791-2801.
58. Rothman TP, Nilaver G, Gershon MD. 1984. Colonization of the developing murine enteric nervous system and subsequent phenotypic expression by the precursors of peptidergic neurons. J Comp Neurol 225: 13-23.
59. Sang Q, Young HM. 1998. The identification and chemical coding of cholinergic neurons in the small and large intestine of the mouse. Anat Rec 251: 185-199.
60. Sela-Donenfeld D, Kalcheim C. 1999. Regulation of the onset of neural crest migration by coordinated activity of BMP4 and Noggin in the dorsal neural tube. Development 126: 4749-4762.
61. Selleck MA, Garcia-Castro MI, Artinger KB, Bronner-Fraser M. 1998. Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm. Development 125: 4919-4930.
62. Shah NM, Marchionni MA, Isaacs I, Stroobant P, Anderson DA. 1994. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77: 349-360.
63. Smith DM, Nielsen C, Tabin CJ, Roberts DJ. 2000. Roles of BMP signaling and Nkx2.5 in patterning at the chick midgut-foregut boundary. Development 127: 3671-3681.
64. Smith VV, Eng C, Milla PJ. 1999. Intestinal ganglioneuromatosis and multiple endocrine neoplasia type 2B: Implications for treatment. Gut 45: 143-146.
65. Song Q, Mehler M, Kessler JA. 1998. Bone morphogenetic proteins induce apoptosis and growth factor dependence of cultured sympathoadrenal progenitor cells. Dev Biol 196: 119-127.
66. Sukegawa A, Narita T, Kameda T, Saitoh K, Nohno T, Iba H, Yasugi S, et al. 2000. The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endoderm epithelium. Development 127: 1971-1980.
67. Ten Dijke P, Goumans MJ, Itoh F, Itoh S. 2002. Regulation of cell proliferation by Smad proteins. J Cell Physiol 191: 1-16.
68. Torihashi S, Hattori T, Hasegawa H, Kurahashi M, Ogaeri T, Fujimoto T. 2009. The expression and crucial roles of BMP signaling in development of smooth muscle progenitor cells in the mouse embryonic gut. Differentiation 77: 277-289.
69. Van de Putte T, Maruhashi M, Francis A, Nelles L, Kondoh H, Huylebroeck D, Higashi Y. 2003. Mice lacking ZFHX1B, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease-mental retardation syndrome. Am J Hum Genet 72: 465-470.
70. Wakamatsu N, Yamada Y, Yamada K, Ono T, Nomura N, Taniguchi H, Kitoh H, et al. 2001. Mutations in SIP1, encoding Smad interacting protein-1, cause a form of Hirschsprung disease. Nat Genet 27: 369-370.
71. Weinhold B, Seidenfaden R, Rockle I, Muhlenhoff M, Schertzinger F, Conzelmann S, Marth JD, et al. 2005. Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J Biol Chem 280: 42971-42977.
72. Yamashita H, ten Dijke P, Heldin C-H, Miyazono K. 1996. Bonemorphogenetic protein receptors. Bone 19: 569-574.
73. Yntema C, Hammond WS. 1954. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol 101: 515-542.
74. Young HM, Bergner AJ, Anderson RB, Enomoto H, Milbrandt J, Newgreen DF, Whitington PM. 2004. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 270: 455-473.
75. Zhang D, Mehler MF, Song Q, Kessler JA. 1998. Development of bone morphogenetic protein receptors in the nervous system and possible roles in regulating trkC expression. J Neurosci 18: 3314-3326.