Bone Morphogenetic Protein-2 and -4 Limit the Number of Enteric Neurons but Promote Development of a TrkC-Expressing Neurotrophin-3-Dependent Subset

Journal of Neuroscience

Volumn 24, Issue 17, 2004, Pages 4266-4282

  Chalazonitis, Alcmène ^a,e   D'Autréaux, Fabien ^a   Guha, Udayan ^b   Pham, Tuan D ^a   Faure, Christophe ^c   Chen, Jason J ^a   Roman, Daniel ^a   Kan, Lixin ^d   Rothman, Taube P ^a   Kessler, John A ^d   Gershon, Michael D ^a  

^a College of Physicians and Surgeons ^*  (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MONTREAL   (Canada)

^d NORTHWESTERN UNIVERSITY   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Autonomic nervous system; Enteric nervous system; GDNF; Gut; Neural crest; p75NTR; Smad protein

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN ANTAGONIST; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; BONE MORPHOGENETIC PROTEIN RECEPTOR IA; BONE MORPHOGENETIC PROTEIN RECEPTOR IB; CHORDIN; FOLLISTATIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GREMLIN; MAD RELATED PROTEIN; NEURON SPECIFIC ENOLASE; NEUROTROPHIN 3; NOGGIN; P75 NTR PROTEIN; PROTEIN; PROTEIN P75; SMAD 1 PROTEIN; SMAD PROTEIN; TRKC PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; INTESTINE; INTESTINE INNERVATION; MESENCHYME; NERVE CELL DIFFERENTIATION; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SMOOTH MUSCLE FIBER; TRANSGENIC MOUSE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL COUNT; CELLS, CULTURED; DNA-BINDING PROTEINS; ENTERIC NERVOUS SYSTEM; FEMALE; FOLLISTATIN; GLYCOPROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTESTINES; MICE; MICE, TRANSGENIC; NEURAL CREST; NEURONS; NEUROTROPHIN 3; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKC; RECEPTORS, GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMAD PROTEINS; SMAD1 PROTEIN; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 2442609883     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3688-03.2004     Document Type: Article

References (110)

1. Baetge G, Pintar JE, Gershon MD (1990a) Transiently catecholaminergic (TC) cells in the bowel of fetal rats and mice: precursors of non-catecholaminergic enteric neurons. Dev Biol 141:353-380.
2. Baetge G, Schneider KA, Gershon MD (1990b) Development and persistence of catecholaminergic neurons in cultured explants of fetal murine vagus nerves and bowel. Development 110:689-701.
3. Belliveau DJ, Krivko I, Kohn J, Lachance C, Pozniak C, Rusakov D, Kaplan D, Miller FD (1997) NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J Cell Biol 136:375-388.
4. Bishop AE, Carlei F, Lee V, Trojanowski J, Marangos PJ, Dahl D, Polak JM (1985) Combined immunostaining of neurofilaments, neuron specific enolase, GFAP, and S-100. A possible method for assessing the morphological and functional status of the enteric nervous system. Histochemistry 82:93-97.
5. Bixby S, Kruger GM, Mosher JT, Joseph NM, Morrison SJ (2002) Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron 35:643-656.
6. Blaugrund E, Pham TD, Tennyson VM, Lo L, Sommer L, Anderson DJ, Gershon MD (1996) Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers, and Mash-1-dependence. Development 122:309-320.
7. Burns AJ, Le Douarin NM (1998) The sacral crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system. Development 125:4335-4347.
8. Burns AJ, Le Douarin NM (2001) Enteric nervous system development: analysis of the selective developmental potentialities of vagal and sacral neural crest cells using quail-chick chimeras. Anat Rec 262:16-28.
9. 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.
10. Chalazonitis A, Tennyson VM, Kibbey MC, Rothman TP, Gershon MD (1997) The α-1 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.
11. 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.
12. Chalazonitis A, Rothman TP, Chen J-X, 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 GFRα-1 in vitro and in vivo. Dev Biol 204:385-406.
13. Chalazonitis A, Chen J, Rothman TP, Gershon MD (1999) Role(s) of bone morphogenetic proteins in the development of enteric neurons in the fetal rat: interaction with NT-3. Soc Neurosci Abstr 25:1785.
14. Chalazonitis A, Pham TD, Rothman TP, DiStefano PS, Bothwell M, Blair-Flynn J, Tessarollo L, Gershon MD (2001) Neurotrophin-3 is required for the survival/differentiation of subsets of developing enteric neurons. J Neurosci 21:5620-5636.
15. Chalazonitis A, Guha U, Pham TD, D'Autréaux F, Roman D, Rothman TP, Kessler JA, Gershon MD (2003a) BMPs-2 and-4 regulate neurogenesis and specification of TrkC-expressing/NT-3-dependent neurons in the enteric nervous system (ENS). Soc Neurosci Abstr 29:351.1.
16. Chalazonitis A, D'Autréaux F, Guha U, Pham TD, Faure CF, Chen JJ, Rothman TP, Kessler JA, Gershon MD (2003b) Regulation of enteric neuronal development and specification of NT-3 dependence by bone morphogenetic proteins (BMPs)-2 and -4. Neurogastroenterol Motil 15:196-197.
17. Chandler CE, Parsons LM, Hosang M, Shooter EM (1984) A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J Biol Chem 259:6882-6889.
18. Cho KW, Blitz IL (1998) BMPs, Smads and metalloproteases: extracellular and intracellular modes of negative regulation. Curr Opin Genet Dev 8:443-449.
19. Cooke HJ (2000) Neurotransmitters in neuronal reflexes regulating intestinal secretion. Ann NY Acad Sci 915:77-80.
20. Donovan MJ, Hahn R, Tessarollo L, Hempstead BL (1996) Identification of an essential non-neuronal function of neurotrophin-3 in mammalian cardiac development. Nat Genet 14:210-213.
21. Enomoto H, Araki T, Jackman A, Heuckeroth R, Snider WD, Johnson EM, Milbrandt J (1998) GFRα1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21:317-324.
22. Epstein M, Poulsen KT, Thiboldeaux R (1991) Formation of ganglia in the gut of the chick embryo. J Comp Neurol 307:189-199.
23. Faure C, Rhéaume C, Chalazonitis A, Gershon MD (2003) Expression of polysialylated neural cell adhesion molecule (PSA-NCAM) in the developing and mature rat enteric nervous system (ENS): relationship to neuronal differentiation and plasticity. Neurogastroenterol Motil 15:197.
24. Forss-Petter S, Danielson PE, Catsicas S, Battenberg E, Price J, Nerenberg M, Sutcliffe JG (1990) Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron 5:187-197.
25. Furuta Y, Piston DW, Hogan BL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124:2203-2212.
26. Gershon MD (1998) Genes, lineages, and tissue interactions in the development of the enteric nervous system. Am J Physiol 275:G869-G873.
27. Gomes WA, Kessler JA (2001) Msx-2 and p21 mediate the pro-apoptotic but not the anti-proliferative effects of BMP4 on cultured sympathetic neuroblasts. Dev Biol 237:212-221.
28. Guha U (2003) Multiple roles of BMP signaling in mouse development. PhD thesis, Albert Einstein College of Medicine.
29. Guha U, Gomes WA, Samanta J, Gupta M, Rice FL, Kessler JA (2004) Target-derived BMP signaling limits sensory neuron number and the extent of peripheral innervation in vivo. Development 131:1175-1186.
30. Gurdon JB, Bourillot PY (2001) Morphogen gradient interpretation. Nature 413:797-803.
31. Hearn C, Newgreen D (2000) Lumbo-sacral neural crest contributes to the avian enteric nervous system independently of vagal neural crest. Dev Dyn 218:525-530.
32. Hearn CJ, Murphy M, Newgreen D (1998) GDNF and ET-3 differentially modulate the numbers of avian enteric neural crest cells and enteric neurons in vitro. Dev Biol 197:93-105.
33. Hearn CJ, Young HM, Ciampoli D, Lomax AE, Newgreen D (1999) Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dyn 214:239-247.
34. Heinicke EA, Kiernan JA, Wijsman J (1987) Specific, selective, and complete staining of neurons of the myenteric plexus, using Cuprolinic blue. J Neurosci Methods 21:45-54.
35. Heuckeroth RO, Lampe PA, Johnson EM, Milbrandt J (1998) Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev Biol 200:116-129.
36. Hogan BLM (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Gen Dev 10:1580-1594.
37. Hollenberg SM, Sternglanz R, Cheng PF, Weintraub H (1995) Identification of a new family of tissue-specific basic helix loop-helix proteins with a two-hybrid system. Mol Cell Biol. 15:3813-3822.
38. Holst MC, Powley TL (1995) Cuprolinic blue (quinolinic phthalocyanine) counterstaining of enteric neurons for peroxidase immunocytochemistry. J Neurosci Methods 62:121-127.
39. Huber LJ, Chao, MV (1995) Mesenchymal and neuronal cell expression of the p75, neurotrophin gene occur by different mechanism. Dev Biol 167:237-238
40. Jing S, Wen D, Yu Y, Holst PL, Luo Y, Fang M, Tamir R, Antonio L, Hu Z, Cupples R, Louis J-C, Hu S, Altrock BW, Fox GM (1996) GDNF-induced activation of the Ret protein tyrosine kinase is mediated by GDNFR-α, a novel-receptor for GDNF. Cell 85:1113-1124.
41. 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.
42. Kietzschmar M, Doody J, Massagué J (1997) Opposing BMP and EGF signaling pathways converge on the TGF-β family mediator Smad1. Nature 389:618-622.
43. Kruger GM, Mosher JT, Bixby S, Joseph N, Iwashita T, Morrison SJ (2002) Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35:657-669.
44. LaBonne C, Bronner-Fraser M (1998) Neural crest induction in Xenopus: evidence for a two-signal model. Development 125:2403-2414.
45. Laemmli UK (1970) Cleavage of structural protein during assembly of bacteriophage T4. Nature 227:680-685.
46. 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.
47. Le Douarin NM, Teillet MA (1974) Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev Biol 41:162-184.
48. Liem KF, Tremmi G, Roelink H, Jessell TM (1995) Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82:969-979.
49. Liu DX, Greene LA (2001) Neuronal apoptosis at the G1/S cell cycle checkpoint. Cell Tissue Res 305:217-228.
50. Lo L, Anderson DJ (1995) Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron 15:527-539.
51. 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.
52. Marchant L, Linker C, Ruiz P, Guerrero N, Mayor R (1998) The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Dev Biol 198:319-329.
53. Mehler MF, Mabie PC, Zhang D, Kessler JA (1997) Bone morphogenetic proteins in the nervous system. Trends Neurosci 20:309-317.
54. Merino R, Rodriguez-Leon J, Macias D, Ganan Y, Economides AN, Hurle JM (1999) The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 126:5515-5522.
55. Mizuseki K, Sakamoto T, Watanabe K, Muguruma K, Ikeya M, Nishiyama A, Arakawa A, Suemori H, Nakatsuji N, Kawasaki H, Murakami F, Sasai Y (2003) Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells. Proc Natl Acad Sci USA 100:5828-5833.
56. Moore MW, Klein RD, Fariñas I, Sauer H, Armanini M, Phillips HLFR, Ryan AM, Carver-Moore K, Rosenthal A (1996) Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76-79.
57. Newgreen D, Young HM (2002a) Enteric nervous system: development and developmental disturbances-part 1. Pediatr Dev Pathol 5:224-247.
58. Newgreen D, Young HM (2002b) Enteric nervous system: development and developmental disturbances-part 2. Pediatr Dev Pathol 5:329-349.
59. Pachnis V, Durbec P, Taraviras S, Grigoriou M, Natarajan D (1998) III. Role Of the RET signal transduction pathway in development of the mammalian enteric nervous system. Am J Physiol 275:G183-G186.
60. Pan H, Gershon MD (2000) Activation of intrinsic afferent pathways in submucosal ganglia of the guinea pig small intestine. J Neurosci 20:3295-3309.
61. Pham TD, Gershon MD, Rothman TP (1991) Time of origin of neurons in the murine enteric nervous system. J Comp Neurol 314:789-798.
62. Pichel JG, Shen L, Sheng HZ, Granholm A-C, Drago J, Grinberg A, Lee EJ, Huang SB, Saarma M, Hoffer BJ, Sariola H, Westphal H (1996) Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73-76.
63. 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.
64. Pomeranz HD, Rothman TP, Gershon MD (1991) Colonization of the post-umbilical bowel by cells derived from the sacral neural crest: direct tracing of cell migration using an intercalating probe and a replication-deficient retrovirus. Development 111:647-655.
65. Pomeranz HD, Rothman TP, Chalazonitis A, Tennyson VM, Gershon MD (1993) Neural crest-derived cells isolated from the gut by immunoselection develop neuronal and glial phenotypes when cultured on laminin. Dev Biol 156:341-361.
66. Roberts DJ (2000) Molecular mechanisms of development of the gastrointestinal tract. Dev Dyn 219:109-120,
67. 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.
68. Roberts DJ, Smith DM, Goff DJ, Tabin CJ (1998) Epithelial-mesenchymal signaling during the regionalization of the chick gut. Development 125:2791-2801.
69. Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten Dijke P, C-HH, Miyazono K (1995) Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci USA 92:7632-7636.
70. Rothman TP, Gershon MD (1982) Phenotypic expression in the developing murine enteric nervous system. J Neurosci 2:381-393.
71. 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.
72. Rothman TP, Le Douarin NM, Fontaine-Pérus JC, Gershon MD (1990) Developmental potential of neural crest-derived cells migrating from segments of developing quail bowel back-grafted into younger chick host embryos. Development 109:411-423.
73. Rothman TP, Le Douarin NM, Fontaine-Pérus JC, Gershon MD (1993) Colonization of the bowel by neural crest-derived cells re-migrating from foregut backtransplanted to vagal or sacral regions of host embryos. Dev Dyn 196:217-233.
74. Sánchez M, Silos-Santiago I, Frisén J, He B, Lira S, Barbacid M (1996) Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70-73.
75. Sasai Y, De Robertis EM (1997) Ectodermal patterning in vertebrate embryos. Dev Biol 182:5-20.
76. Scheuermann DW, Stach W, Timmermans JP, Adriaensen D, De Groodt-Lasseel MHA (1989) Neuron-specific enolase and S-100 protein immunohistochemistry for defining the structure and topographical relationship of the different enteric nerve plexuses in the small intestine of the pig. Cell Tissue Res 256:65-75.
77. Schmechel DE, Brightman MW, Marangos PJ (1980) Neurons switch from non-neuronal enolase to neuron-specific enolase during differentiation. Brain Res 190:195-214.
78. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367:380-383.
79. 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.
80. Sela-Donenfeld D, Kalcheim C (2002) Localized BMP4-noggin interactions generate the dynamic patterning of noggin expression in somites. Dev Biol 246:311-328.
81. Serbedzija GN, Burgan S, Fraser SE, Bronner-Fraser M (1991) Vital dye labeling demonstrates a sacral neural crest contribution to the enteric nervous system of chick and mouse embryos. Development 111:857-866.
82. Sextier-Sainte-Claire Deville F, Ziller C, Le Douarin NM (1994) Developmental potentials of enteric neural crest-derived cells in clonal and mass cultures. Dev Biol 163:141-151.
83. Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFβ superfamily members. Cell 85:331-343.
84. Siebert PD, Larrick JW (1992) Competitive PCR. Nature 359:557-558.
85. Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G (1986) A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol 103:2787-2796.
86. 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.
87. Sukegawa A, Narita T, Kameda T, Saitoh K, Nohno T, Iba H, Yasugi S, Fukuda K (2000) The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endodermal epithelium. Development 127:1971-1980.
88. Suvanto P, Hiltunen JO, Arumäe U, Moshnyakov M, Sariola H, Sainio K, Saama M (1996) localization of glial cell line-derived neurotrophic factor (GDNF) mRNA in embryonic rat by in situ hybridization. Eur J Neurosci 8:816-822.
89. Tam PKH, Lister J (1986) Development profile of neuron-specific enolase in human gut and its implications in Hirschsprung's disease. Gastroenterology 90:1901-1906.
90. Taraviras S, Pachnis V (1999) Development of the mammalian enteric nervous system. Curr Opin Genet Dev 9:321-327,
91. Taraviras S, Marcos-Gutierrez CV, Durbec P, Jani H, Grigoriou M, Sukumaran M, Wang LC, Hynes M, Raisman G, Pachnis V (1999) Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development 126:2785-2797.
92. ten Dijke P, Yamashita H, Sampath TK, Reddi AH, Estevez M, Riddle DL, Ichijo H, Heldin C-H, Miyazono K (1994) Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J Biol Chem 269:16985-16988.
93. ten Dijke P, Goumans MJ, Itoh F, Itoh S (2002) Regulation of cell proliferation by Smad proteins. J Cell Physiol 191:1-16.
94. Treanor JJS, Goodman L, de Sauvage F, Stone DM, Poulsen KT, Beck CD, Gray C, Armanini MP, Pollock RA, Hefti F, Pillips HS, Goddard A, Moore MW, Buj-Bello A, Davies AM, Asai N, Takahashi M, Vandlen R, Henderson CE, Rosenthal A (1996) Characterization of a multicomponent receptor for GDNF. Nature 382:80-83.
95. Trupp M, Arenas E, Fainzilber M, Nilsson A-S, Sieber B-A, Grigoriou M, Kilkenny C, Salazar-Grueso E, Pachnis V, Arumäe U, Sariola H, Saarma M, Ibáñez CF (1996) Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature 381:785-789.
96. Tsoulfas P, Stephens RM, Kaplan DR, Parada LF (1996) TrkC isoforms with inserts in the kinase domain show impaired signaling responses. J Biol Chem 271:5691-5697.
97. Tucker RP, Matus AI (1988) Microtubule-associated proteins characteristic of embryonic brain are found in the adult mammalian retina. Dev Biol 130:423-434.
98. Varley JE, Maxwell GD (1996) BMP-2 and BMP-4 but not BMP-6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp Neurol 140:84-94.
99. von Bubnoff A, Cho KW (2001) Intracellular BMP signaling regulation in vertebrates: pathway or network? Dev Biol 239:1-14.
100. Wakamatsu N, Yamada Y, Yamada K, Ono T, Nomura N, Taniguchi H, Kitoh H, Mutoh N, Yamanaka T, Mushiake K, Kato K, Sonta S, Nagaya M (2001) Mutations in SIP1, encoding Smad interacting protein-1, cause a form of Hirschsprung disease. Nat Genet 27:369-370.
101. Wilkinson LD, Lee K, Deshpande S, Duerksen-Hughes P, Boss JM, Pohl J (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246:670-673.
102. Xu Z, Maroney AC, Dobrzanski P, Kukekov NV, Greene LA (2001) The MLK family mediates c-Jun N-terminal kinase activation in neuronal apoptosis. Mol Cell Biol 21:4713-4724.
103. Yamashita H, Ten Dijke P, Heldin C-H, Miyazono K (1996) Bone morphogenetic protein receptors. Bone 19:569-574.
104. Yntema CL, 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.
105. Yntema CL, Hammond WS (1955) Experiments on the origin and development of the sacral autonomic nerves in the chick embryo. J Exp Zool 129:375-414.
106. Young H, Hearn CJ, Ciampoli D, Southwell BR, Brunet JF, Newgreen DF (1998) A single rostrocaudal colonization of the rodent intestine by enteric neuron precursors is revealed by the expression of Phox2B, Ret, and p75 and by explants grown under the kidney capsule or in organ culture. Dev Biol 202:67-84.
107. Young HM, Ciampoli D, Hsuan J, Canty AJ (1999) Expression of Ret-, p75(NTR)-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut. Dev Dyn 216:137-152.
108. Young HM, Bergner AJ, Muller T (2003) Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1-11.
109. Zhang D, Mehler M, 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.
110. Ziller C, Dupin E, Brazeau P, Paulin D, Le Douarin NM (1983) Early segregation of a neuronal precursor cell line in the neural crest as revealed by culture in a chemically defined medium. Cell 32:627-638.