Development of the intrinsic and extrinsic innervation of the gut

Developmental Biology

Volumn 417, Issue 2, 2016, Pages 158-167

  Uesaka, Toshihiro ^a,b,c   Young, Heather M ^d   Pachnis, Vassilis ^e   Enomoto, Hideki ^a,b,c  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Enteric nervous system; Extrinsic nerve innervation; Neuronal and glial differentiation; Neuronal projection; Schwann cell precursors

Indexed keywords

ARTEMIN; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALBINDIN; CALRETININ; ENDOTHELIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; NEURONAL NITRIC OXIDE SYNTHASE; NEUROTROPHIN 3; NEUROTROPHIN RECEPTOR P75; NEURTURIN; SEROTONIN; SONIC HEDGEHOG PROTEIN;

ASTROCYTE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MIGRATION; CELL SURVIVAL; GASTROINTESTINAL TRACT; GENE MUTATION; GLIA CELL; HETEROZYGOSITY; HIRSCHSPRUNG DISEASE; HUMAN; IMMUNOPHENOTYPING; IMMUNOREACTIVITY; INTESTINE INNERVATION; INTESTINE MUCOSA; LAMINA PROPRIA; MESENCHYME; MOLECULAR DYNAMICS; MORPHOLOGY; MYENTERIC PLEXUS; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION; STEM CELL; SUBMUCOUS PLEXUS; SYMPATHETIC NERVE; ANATOMY AND HISTOLOGY; ANIMAL; CELL MOTION; CYTOLOGY; EFFERENT NERVE; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; INNERVATION; MOUSE; NEURAL CREST; PHYSIOLOGY; SENSORY NERVE CELL;

ANIMALS; CELL MOVEMENT; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL TRACT; HUMANS; MICE; NEURAL CREST; NEUROGENESIS; NEURONS, AFFERENT; NEURONS, EFFERENT; SIGNAL TRANSDUCTION;

EID: 84964627503     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2016.04.016     Document Type: Review

References (178)

1. Adameyko, I., Lallemend, F., Aquino, J.B., Pereira, J.A., Topilko, P., Muller, T., Fritz, N., Beljajeva, A., Mochii, M., Liste, I., Usoskin, D., Suter, U., Birchmeier, C., Ernfors, P., Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139 (2009), 366–379.
2. Allen, B.L., Tenzen, T., McMahon, A.P., The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev. 21 (2007), 1244–1257.
3. Amiel, J., Attie, T., Jan, D., Pelet, A., Edery, P., Bidaud, C., Lacombe, D., Tam, P., Simeoni, J., Flori, E., Nihoul-Fekete, C., Munnich, A., Lyonnet, S., Heterozygous endothelin receptor B (EDNRB) mutations in isolated Hirschsprung disease. Hum. Mol. Genet. 5 (1996), 355–357.
4. Anderson, R.B., Stewart, A.L., Young, H.M., Phenotypes of neural-crest-derived cells in vagal and sacral pathways. Cell Tissue Res. 323 (2006), 11–25.
5. Anderson, R.B., Bergner, A.J., Taniguchi, M., Fujisawa, H., Forrai, A., Robb, L., Young, H.M., Effects of different regions of the developing gut on the migration of enteric neural crest-derived cells: a role for Sema3A, but not Sema3F. Dev. Biol. 305 (2007), 287–299.
6. Auricchio, A., Casari, G., Staiano, A., Ballabio, A., Endothelin-B receptor mutations in patients with isolated Hirschsprung disease from a non-inbred population. Hum. Mol. Genet. 5 (1996), 351–354.
7. Avetisyan, M., Schill, E.M., Heuckeroth, R.O., Building a second brain in the bowel. J. Clin. Investig. 125 (2015), 899–907.
8. Badizadegan, K., Thomas, A.R., Nagy, N., Ndishabandi, D., Miller, S.A., Alessandrini, A., Belkind-Gerson, J., Goldstein, A.M., Presence of intramucosal neuroglial cells in normal and aganglionic human colon. Am. J. Physiol. 307 (2014), G1002–G1012.
9. Baetge, G., Gershon, M.D., Transient catecholaminergic (TC) cells in the vagus nerves and bowel of fetal mice: relationship to the development of enteric neurons. Dev. Biol. 132 (1989), 189–211.
10. Balemba, O.B., Hay-Schmidt, A., Assey, R.J., Kahwa, C.K., Semuguruka, W.D., Dantzer, V., An immunohistochemical study of the organization of ganglia and nerve fibres in the mucosa of the porcine intestine. Anat. Histol. Embryol. 31 (2002), 237–246.
11. Balemba, O.B., Grondahl, M.L., Mbassa, G.K., Semuguruka, W.D., Hay-Smith, A., Skadhauge, E., Dantzer, V., The organisation of the enteric nervous system in the submucous and mucous layers of the small intestine of the pig studied by VIP and neurofilament protein immunohistochemistry. J. Anat. 192 (1998), 257–267.
12. Bamji, S.X., Majdan, M., Pozniak, C.D., Belliveau, D.J., Aloyz, R., Kohn, J., Causing, C.G., Miller, F.D., The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J. Cell Biol. 140 (1998), 911–923.
13. Barlow, A., de Graaff, E., Pachnis, V., Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron 40 (2003), 905–916.
14. Bayliss, W.M., Starling, E.H., The movements and innervation of the small intestine. J. Physiol. 24 (1899), 99–143.
15. Becker, L., Kulkarni, S., Tiwari, G., Micci, M.A., Pasricha, P.J., Divergent fate and origin of neurosphere-like bodies from different layers of the gut. Am. J. Physiol. 302 (2012), G958–G965.
16. Behar, O., Golden, J.A., Mashimo, H., Schoen, F.J., Fishman, M.C., Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383 (1996), 525–528.
17. Belkind-Gerson, J., Hotta, R., Nagy, N., Thomas, A.R., Graham, H., Cheng, L., Solorzano, J., Nguyen, D., Kamionek, M., Dietrich, J., Cherayil, B.J., Goldstein, A.M., Colitis induces enteric neurogenesis through a 5-HT4-dependent mechanism. Inflamm. Bowel Dis. 21 (2015), 870–878.
18. Bergner, A.J., Stamp, L.A., Gonsalvez, D.G., Allison, M.B., Olson, D.P., Myers, M.G. Jr., Anderson, C.R., Young, H.M., Birthdating of myenteric neuron subtypes in the small intestine of the mouse. J. Comp. Neurol. 522 (2014), 514–527.
19. Berne, R.M., Levy, M.N., Koeppen, B.M., Stanton, B.A., Berne & Levy Physiology. 6th ed., 2009, Mosby/Elsevier, Philadelphia, PA.
20. Berthoud, H.R., Carlson, N.R., Powley, T.L., Topography of efferent vagal innervation of the rat gastrointestinal tract. Am. J. Physiol. 260 (1991), R200–R207.
21. Biau, S., Jin, S., Fan, C.M., Gastrointestinal defects of the Gas1 mutant involve dysregulated Hedgehog and Ret signaling. Biol. Open 2 (2013), 144–155.
22. Biddinger, J.E., Fox, E.A., Reduced intestinal brain-derived neurotrophic factor increases vagal sensory innervation of the intestine and enhances satiation. J. Neurosci. 34 (2014), 10379–10393.
23. Boesmans, W., Lasrado, R., Vanden Berghe, P., Pachnis, V., Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia 63 (2015), 229–241.
24. Boesmans, W., Martens, M.A., Weltens, N., Hao, M.M., Tack, J., Cirillo, C., Vanden Berghe, P., Imaging neuron-glia interactions in the enteric nervous system. Front. Cell Neurosci., 7, 2013, 183.
25. Bondurand, N., Natarajan, D., Barlow, A., Thapar, N., Pachnis, V., Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development 133 (2006), 2075–2086.
26. Brennan, A., Dean, C.H., Zhang, A.L., Cass, D.T., Mirsky, R., Jessen, K.R., Endothelins control the timing of Schwann cell generation in vitro and in vivo. Dev. Biol. 227 (2000), 545–557.
27. Britsch, S., Li, L., Kirchhoff, S., Theuring, F., Brinkmann, V., Birchmeier, C., Riethmacher, D., The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 12 (1998), 1825–1836.
28. Britsch, S., Goerich, D.E., Riethmacher, D., Peirano, R.I., Rossner, M., Nave, K.A., Birchmeier, C., Wegner, M., The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 15 (2001), 66–78.
29. Brunet, I., Gordon, E., Han, J., Cristofaro, B., Broqueres-You, D., Liu, C., Bouvree, K., Zhang, J., del Toro, R., Mathivet, T., Larrivee, B., Jagu, J., Pibouin-Fragner, L., Pardanaud, L., Machado, M.J., Kennedy, T.E., Zhuang, Z., Simons, M., Levy, B.I., Tessier-Lavigne, M., Grenz, A., Eltzschig, H., Eichmann, A., Netrin-1 controls sympathetic arterial innervation. J. Clin. Investig. 124 (2014), 3230–3240.
30. Burns, A.J., Le Douarin, N.M., The sacral neural crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system. Development 125 (1998), 4335–4347.
31. Bush, T.G., Savidge, T.C., Freeman, T.C., Cox, H.J., Campbell, E.A., Mucke, L., Johnson, M.H., Sofroniew, M.V., Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93 (1998), 189–201.
32. Calmont, A., Thapar, N., Scambler, P.J., Burns, A.J., Absence of the vagus nerve in the stomach of Tbx1−/− mutant mice. Neurogastroenterol. Motil. 23 (2011), 125–130.
33. Calmont, A., Ivins, S., Van Bueren, K.L., Papangeli, I., Kyriakopoulou, V., Andrews, W.D., Martin, J.F., Moon, A.M., Illingworth, E.A., Basson, M.A., Scambler, P.J., Tbx1 controls cardiac neural crest cell migration during arch artery development by regulating Gbx2 expression in the pharyngeal ectoderm. Development 136 (2009), 3173–3183.
34. Chakravarti, A., Endothelin receptor-mediated signaling in hirschsprung disease. Hum. Mol. Genet. 5 (1996), 303–307.
35. Chalazonitis, A., Rothman, T.P., Chen, J., Gershon, M.D., 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 (1998), 385–406.
36. Chalazonitis, A., D'Autreaux, F., Pham, T.D., Kessler, J.A., Gershon, M.D., Bone morphogenetic proteins regulate enteric gliogenesis by modulating ErbB3 signaling. Dev. Biol. 350 (2011), 64–79.
37. Chalazonitis, A., Pham, T.D., Li, Z., Roman, D., Guha, U., Gomes, W., Kan, L., Kessler, J.A., Gershon, M.D., Bone morphogenetic protein regulation of enteric neuronal phenotypic diversity: relationship to timing of cell cycle exit. J. Comp. Neurol. 509 (2008), 474–492.
38. Chuang, P.T., McMahon, A.P., Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 397 (1999), 617–621.
39. Conner, P.J., Focke, P.J., Noden, D.M., Epstein, M.L., Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells. Dev. Dyn. 226 (2003), 91–98.
40. Coppola, E., Rallu, M., Richard, J., Dufour, S., Riethmacher, D., Guillemot, F., Goridis, C., Brunet, J.F., Epibranchial ganglia orchestrate the development of the cranial neurogenic crest. Proc. Natl. Acad. Sci. USA 107 (2010), 2066–2071.
41. Cornet, A., Savidge, T.C., Cabarrocas, J., Deng, W.L., Colombel, J.F., Lassmann, H., Desreumaux, P., Liblau, R.S., Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease?. Proc. Natl. Acad. Sci. USA 98 (2001), 13306–13311.
42. Costa, M., Brookes, S.H., Zagorodnyuk, V., How many kinds of visceral afferents?. Gut 53:Suppl 2 (2004), ii1–ii4.
43. Crone, S.A., Negro, A., Trumpp, A., Giovannini, M., Lee, K.F., Colonic epithelial expression of ErbB2 is required for postnatal maintenance of the enteric nervous system. Neuron 37 (2003), 29–40.
44. Crowley, C., Spencer, S.D., Nishimura, M.C., Chen, K.S., Pitts-Meek, S., Armanini, M.P., Ling, L.H., McMahon, S.B., Shelton, D.L., Levinson, A.D., et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76 (1994), 1001–1011.
45. Dulac, C., Le Douarin, N.M., Phenotypic plasticity of Schwann cells and enteric glial cells in response to the microenvironment. Proc. Natl. Acad. Sci. USA 88 (1991), 6358–6362.
46. Dupin, E., Glavieux, C., Vaigot, P., Le Douarin, N.M., Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glial-melanocytic progenitor. Proc. Natl. Acad. Sci. USA 97 (2000), 7882–7887.
47. Dupin, E., Real, C., Glavieux-Pardanaud, C., Vaigot, P., Le Douarin, N.M., Reversal of developmental restrictions in neural crest lineages: transition from Schwann cells to glial-melanocytic precursors in vitro. Proc. Natl. Acad. Sci. USA 100 (2003), 5229–5233.
48. Dyachuk, V., Furlan, A., Shahidi, M.K., Giovenco, M., Kaukua, N., Konstantinidou, C., Pachnis, V., Memic, F., Marklund, U., Muller, T., Birchmeier, C., Fried, K., Ernfors, P., Adameyko, I., Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science 345 (2014), 82–87.
49. Enomoto, H., Crawford, P.A., Gorodinsky, A., Heuckeroth, R.O., Johnson, E.M. Jr., Milbrandt, J., RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128 (2001), 3963–3974.
50. Erickson, J.T., Conover, J.C., Borday, V., Champagnat, J., Barbacid, M., Yancopoulos, G., Katz, D.M., Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J. Neurosci. 16 (1996), 5361–5371.
51. Erickson, S.L., O'Shea, K.S., Ghaboosi, N., Loverro, L., Frantz, G., Bauer, M., Lu, L.H., Moore, M.W., ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 124 (1997), 4999–5011.
52. Ernfors, P., Merlio, J.P., Persson, H., Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur. J. Neurosci. 4 (1992), 1140–1158.
53. Ernfors, P., Lee, K.F., Kucera, J., Jaenisch, R., Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77 (1994), 503–512.
54. Espinosa-Medina, I., Outin, E., Picard, C.A., Chettouh, Z., Dymecki, S., Consalez, G.G., Coppola, E., Brunet, J.F., Neurodevelopment. Parasympathetic ganglia derive from Schwann cell precursors. Science 345 (2014), 87–90.
55. Fang, S., Wu, R., Christensen, J., Intramucosal nerve cells in human small intestine. J. Auton. Nerv. Syst. 44 (1993), 129–136.
56. Farinas, I., Neurotrophin actions during the development of the peripheral nervous system. Microsc. Res. Tech. 45 (1999), 233–242.
57. Farinas, I., Jones, K.R., Backus, C., Wang, X.Y., Reichardt, L.F., Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369 (1994), 658–661.
58. Ferri, G.L., Probert, L., Cocchia, D., Michetti, F., Marangos, P.J., Polak, J.M., Evidence for the presence of S-100 protein in the glial component of the human enteric nervous system. Nature 297 (1982), 409–410.
59. Flamant, M., Aubert, P., Rolli-Derkinderen, M., Bourreille, A., Neunlist, M.R., Mahe, M.M., Meurette, G., Marteyn, B., Savidge, T., Galmiche, J.P., Sansonetti, P.J., Neunlist, M., Enteric glia protect against Shigella flexneri invasion in intestinal epithelial cells: a role for S-nitrosoglutathione. Gut 60 (2011), 473–484.
60. Focke, P.J., Schiltz, C.A., Jones, S.E., Watters, J.J., Epstein, M.L., Enteric neuroblasts require the phosphatidylinositol 3-kinase pathway for GDNF-stimulated proliferation. J. Neurobiol. 47 (2001), 306–317.
61. Fox, E.A., Murphy, M.C., Factors regulating vagal sensory development: potential role in obesities of developmental origin. Physiol. Behav. 94 (2008), 90–104.
62. Fox, E.A., McAdams, J., Smooth-muscle-specific expression of neurotrophin-3 in mouse embryonic and neonatal gastrointestinal tract. Cell Tissue Res. 340 (2010), 267–286.
63. Fox, E.A., Biddinger, J.E., Baquet, Z.C., Jones, K.R., McAdams, J., Loss of neurotrophin-3 from smooth muscle disrupts vagal gastrointestinal afferent signaling and satiation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305 (2013), R1307–R1322.
64. Fox, E.A., Biddinger, J.E., Jones, K.R., McAdams, J., Worman, A., Mechanism of hyperphagia contributing to obesity in brain-derived neurotrophic factor knockout mice. Neuroscience 229 (2013), 176–199.
65. Francis, N.J., Landis, S.C., Cellular and molecular determinants of sympathetic neuron development. Annu. Rev. Neurosci. 22 (1999), 541–566.
66. Furness, J.B., Types of neurons in the enteric nervous system. J. Auton. Nerv. Syst. 81 (2000), 87–96.
67. Furness, J.B., Johnson, P.J., Pompolo, S., Bornstein, J.C., Evidence that enteric motility reflexes can be initiated through entirely intrinsic mechanisms in the guinea-pig small intestine. Neurogastroenterol. Motil. 7 (1995), 89–96.
68. Garcia-Barcelo, M.M., Tang, C.S., Ngan, E.S., Lui, V.C., Chen, Y., So, M.T., Leon, T.Y., Miao, X.P., Shum, C.K., Liu, F.Q., Yeung, M.Y., Yuan, Z.W., Guo, W.H., Liu, L., Sun, X.B., Huang, L.M., Tou, J.F., Song, Y.Q., Chan, D., Cheung, K.M., Wong, K.K., Cherny, S.S., Sham, P.C., Tam, P.K., Genome-wide association study identifies NRG1 as a susceptibility locus for Hirschsprung's disease. Proc. Natl. Acad. Sci. USA 106 (2009), 2694–2699.
69. Garg, V., Yamagishi, C., Hu, T., Kathiriya, I.S., Yamagishi, H., Srivastava, D., Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev. Biol. 235 (2001), 62–73.
70. Garratt, A.N., Britsch, S., Birchmeier, C., Neuregulin, a factor with many functions in the life of a schwann cell. Bioessays 22 (2000), 987–996.
71. Garratt, A.N., Voiculescu, O., Topilko, P., Charnay, P., Birchmeier, C., A dual role of erbB2 in myelination and in expansion of the schwann cell precursor pool. J. Cell Biol. 148 (2000), 1035–1046.
72. Genc, B., Ozdinler, P.H., Mendoza, A.E., Erzurumlu, R.S., A chemoattractant role for NT-3 in proprioceptive axon guidance. PLoS Biol., 2, 2004, e403.
73. Gianino, S., Grider, J.R., Cresswell, J., Enomoto, H., Heuckeroth, R.O., GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 130 (2003), 2187–2198.
74. Glebova, N.O., Ginty, D.D., Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J. Neurosci. 24 (2004), 743–751.
75. Glebova, N.O., Ginty, D.D., Growth and survival signals controlling sympathetic nervous system development. Annu. Rev. Neurosci. 28 (2005), 191–222.
76. Goldberg, D., Borojevic, R., Anderson, M., Chen, J.J., Gershon, M.D., Ratcliffe, E.M., Slit/Robo-mediated chemorepulsion of vagal sensory axons in the fetal gut. Dev. Dyn. 242 (2013), 9–15.
77. Golden, J.P., DeMaro, J.A., Osborne, P.A., Milbrandt, J., Johnson, E.M. Jr., Expression of neurturin, GDNF, and GDNF family-receptor mRNA in the developing and mature mouse. Exp. Neurol. 158 (1999), 504–528.
78. Goldstein, A.M., Hofstra, R.M., Burns, A.J., Building a brain in the gut: development of the enteric nervous system. Clin. Genet. 83 (2013), 307–316.
79. Grundy, D., Signalling the state of the digestive tract. Auton. Neurosci. 125 (2006), 76–80.
80. Gui, H., Tang, W.K., So, M.T., Proitsi, P., Sham, P.C., Tam, P.K., Ngan, E.S., Cherny, S.S., Garcia-Barcelo, M.M., RET and NRG1 interplay in Hirschsprung disease. Hum. Genet. 132 (2013), 591–600.
81. Gulbransen, B.D., Sharkey, K.A., Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136 (2009), 1349–1358.
82. Gulbransen, B.D., Sharkey, K.A., Novel functional roles for enteric glia in the gastrointestinal tract. Nat. Rev. Gastroenterol. Hepatol. 9 (2012), 625–632.
83. Gulbransen, B.D., Bains, J.S., Sharkey, K.A., Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J. Neurosci. 30 (2010), 6801–6809.
84. Gunadi, Kapoor, A., Ling, A.Y., Rochadi, Makhmudi, A., Herini, E.S., Sosa, M.X., Chatterjee, S., Chakravarti, A., Effects of RET and NRG1 polymorphisms in Indonesian patients with Hirschsprung disease. J. Pediatr. Surg. 49 (2014), 1614–1618.
85. Hanani, M., Reichenbach, A., Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res. 278 (1994), 153–160.
86. Hatch, J., Mukouyama, Y.S., Spatiotemporal mapping of vascularization and innervation in the fetal murine intestine. Dev. Dyn. 244 (2015), 56–68.
87. Heanue, T.A., Pachnis, V., Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat. Rev. Neurosci. 8 (2007), 466–479.
88. Hearn, C.J., Murphy, M., Newgreen, D., GDNF and ET-3 differentially modulate the numbers of avian enteric neural crest cells and enteric neurons in vitro. Dev. Biol. 197 (1998), 93–105.
89. Henderson, C.E., Phillips, H.S., Pollock, R.A., Davies, A.M., Lemeulle, C., Armanini, M., Simmons, L., Moffet, B., Vandlen, R.A., Simpson, L.C.c.t.S.L., Koliatsos, V.E., Rosenthal, A., et al. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266 (1994), 1062–1064.
90. Heuckeroth, R.O., Enomoto, H., Grider, J.R., Golden, J.P., Hanke, J.A., Jackman, A., Molliver, D.C., Bardgett, M.E., Snider, W.D., Johnson, E.M. Jr., Milbrandt, J., Gene targeting reveals a critical role for neurturin in the development and maintenance of enteric, sensory, and parasympathetic neurons. Neuron 22 (1999), 253–263.
91. Hoff, S., Zeller, F., von Weyhern, C.W., Wegner, M., Schemann, M., Michel, K., Ruhl, A., Quantitative assessment of glial cells in the human and guinea pig enteric nervous system with an anti-Sox8/9/10 antibody. J. Comp. Neurol. 509 (2008), 356–371.
92. Honjo, Y., Kniss, J., Eisen, J.S., Neuregulin-mediated ErbB3 signaling is required for formation of zebrafish dorsal root ganglion neurons. Development 135 (2008), 2615–2625.
93. Honma, Y., Araki, T., Gianino, S., Bruce, A., Heuckeroth, R., Johnson, E., Milbrandt, J., Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35 (2002), 267–282.
94. Hosoda, K., Hammer, R.E., Richardson, J.A., Baynash, A.G., Cheung, J.C., Giaid, A., Yanagisawa, M., Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice. Cell 79 (1994), 1267–1276.
95. Huang, E.J., Reichardt, L.F., Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24 (2001), 677–736.
96. Jessen, K.R., Mirsky, R., Signals that determine Schwann cell identity. J. Anat. 200 (2002), 367–376.
97. Jiang, Y., Liu, M.T., Gershon, M.D., Netrins and DCC in the guidance of migrating neural crest-derived cells in the developing bowel and pancreas. Dev. Biol. 258 (2003), 364–384.
98. Jin, S., Martinelli, D.C., Zheng, X., Tessier-Lavigne, M., Fan, C.M., Gas1 is a receptor for sonic hedgehog to repel enteric axons. Proc. Natl. Acad. Sci. USA 112 (2015), E73–E80.
99. Jones, K.R., Farinas, I., Backus, C., Reichardt, L.F., Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76 (1994), 989–999.
100. Joseph, N.M., He, S., Quintana, E., Kim, Y.G., Nunez, G., Morrison, S.J., Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J. Clin. Investig. 121 (2011), 3398–3411.
101. Joseph, N.M., Mukouyama, Y.S., Mosher, J.T., Jaegle, M., Crone, S.A., Dormand, E.L., Lee, K.F., Meijer, D., Anderson, D.J., Morrison, S.J., Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131 (2004), 5599–5612.
102. Kabouridis, P.S., Lasrado, R., McCallum, S., Chng, S.H., Snippert, H.J., Clevers, H., Pettersson, S., Pachnis, V., Microbiota controls the homeostasis of glial cells in the gut lamina propria. Neuron 85 (2015), 289–295.
103. Kapur, R.P., Yost, C., Palmiter, R.D., A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development 116 (1992), 167–175.
104. Kawaja, M.D., Smithson, L.J., Elliott, J., Trinh, G., Crotty, A.M., Michalski, B., Fahnestock, M., Nerve growth factor promoter activity revealed in mice expressing enhanced green fluorescent protein. J. Comp. Neurol. 519 (2011), 2522–2545.
105. Kenchappa, R.S., Zampieri, N., Chao, M.V., Barker, P.A., Teng, H.K., Hempstead, B.L., Carter, B.D., Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50 (2006), 219–232.
106. Kruger, G.M., Mosher, J.T., Bixby, S., Joseph, N., Iwashita, T., Morrison, S.J., Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35 (2002), 657–669.
107. Kuruvilla, R., Zweifel, L.S., Glebova, N.O., Lonze, B.E., Valdez, G., Ye, H., Ginty, D.D., A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118 (2004), 243–255.
108. Kusafuka, T., Wang, Y., Puri, P., Novel mutations of the endothelin-B receptor gene in isolated patients with Hirschsprung's disease. Hum. Mol. Genet. 5 (1996), 347–349.
109. Lake, J.I., Heuckeroth, R.O., Enteric nervous system development: migration, differentiation, and disease. Am. J. Physiol. 305 (2013), G1–24.
110. Langley, J.N., Magnus, R., Some observations of the movements of the intestine before and after degenerative section of the mesenteric nerves. J. Physiol. 33 (1905), 34–51.
111. Laranjeira, C., Sandgren, K., Kessaris, N., Richardson, W., Potocnik, A., Vanden Berghe, P., Pachnis, V., Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J. Clin. Investig. 121 (2011), 3412–3424.
112. Lee, H.O., Levorse, J.M., Shin, M.K., The endothelin receptor-B is required for the migration of neural crest-derived melanocyte and enteric neuron precursors. Dev. Biol. 259 (2003), 162–175.
113. Leibl, M.A., Ota, T., Woodward, M.N., Kenny, S.E., Lloyd, D.A., Vaillant, C.R., Edgar, D.H., Expression of endothelin 3 by mesenchymal cells of embryonic mouse caecum. Gut 44 (1999), 246–252.
114. Levi-Montalcini, R., Booker, B., Destruction of the sympathetic ganglia in mammals by an antiserum to a nerve-growth protein. Proc. Natl. Acad. Sci. USA 46 (1960), 384–391.
115. Liebl, D.J., Tessarollo, L., Palko, M.E., Parada, L.F., Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. J. Neurosci. 17 (1997), 9113–9121.
116. Liu, M.T., Kuan, Y.H., Wang, J., Hen, R., Gershon, M.D., 5-HT4 receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice. J. Neurosci. 29 (2009), 9683–9699.
117. Macrae, I.M., Furness, J.B., Costa, M., Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guinea-pig. Cell Tissue Res. 244 (1986), 173–180.
118. Makita, T., Sucov, H.M., Gariepy, C.E., Yanagisawa, M., Ginty, D.D., Endothelins are vascular-derived axonal guidance cues for developing sympathetic neurons. Nature 452 (2008), 759–763.
119. Mao, J., Kim, B.M., Rajurkar, M., Shivdasani, R.A., McMahon, A.P., Hedgehog signaling controls mesenchymal growth in the developing mammalian digestive tract. Development 137 (2010), 1721–1729.
120. Marigo, V., Davey, R.A., Zuo, Y., Cunningham, J.M., Tabin, C.J., Biochemical evidence that patched is the Hedgehog receptor. Nature 384 (1996), 176–179.
121. Martinelli, D.C., Fan, C.M., Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev. 21 (2007), 1231–1243.
122. Matsuyoshi, H., Kuniyasu, H., Okumura, M., Misawa, H., Katsui, R., Zhang, G.X., Obata, K., Takaki, M., A 5-HT(4)-receptor activation-induced neural plasticity enhances in vivo reconstructs of enteric nerve circuit insult. Neurogastroenterol. Motil., 22(806–813), 2010, e226.
123. McKeown, S.J., Chow, C.W., Young, H.M., Development of the submucous plexus in the large intestine of the mouse. Cell Tissue Res. 303 (2001), 301–305.
124. McKeown, S.J., Stamp, L., Hao, M.M., Young, H.M., Hirschsprung disease: a developmental disorder of the enteric nervous system. Wiley Interdiscip. Rev. Dev. Biol. 2 (2013), 113–129.
125. Metzger, M., Caldwell, C., Barlow, A.J., Burns, A.J., Thapar, N., Enteric nervous system stem cells derived from human gut mucosa for the treatment of aganglionic gut disorders. Gastroenterology 136:2214–2225 (2009), e2211–e2213.
126. Murphy, M.C., Fox, E.A., Anterograde tracing method using DiI to label vagal innervation of the embryonic and early postnatal mouse gastrointestinal tract. J. Neurosci. Methods 163 (2007), 213–225.
127. Murphy, M.C., Fox, E.A., Mice deficient in brain-derived neurotrophic factor have altered development of gastric vagal sensory innervation. J. Comp. Neurol. 518 (2010), 2934–2951.
128. Nagy, N., Goldstein, A.M., Endothelin-3 regulates neural crest cell proliferation and differentiation in the hindgut enteric nervous system. Dev. Biol. 293 (2006), 203–217.
129. Narita, T., Ishii, Y., Nohno, T., Noji, S., Yasugi, S., Sonic hedgehog expression in developing chicken digestive organs is regulated by epithelial-mesenchymal interactions. Dev. Growth Differ. 40 (1998), 67–74.
130. Nataf, V., Le Douarin, N.M., Induction of melanogenesis by tetradecanoylphorbol-13 acetate and endothelin 3 in embryonic avian peripheral nerve cultures. Pigment Cell Res. 13 (2000), 172–178.
131. Natarajan, D., Marcos-Gutierrez, C., Pachnis, V., de Graaff, E., Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development 129 (2002), 5151–5160.
132. Obermayr, F., Hotta, R., Enomoto, H., Young, H.M., Development and developmental disorders of the enteric nervous system. Nat. Rev. Gastroenterol. Hepatol. 10 (2013), 43–57.
133. Okamura, Y., Saga, Y., Notch signaling is required for the maintenance of enteric neural crest progenitors. Development 135 (2008), 3555–3565.
134. Paratore, C., Eichenberger, C., Suter, U., Sommer, L., Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum. Mol. Genet. 11 (2002), 3075–3085.
135. Paratore, C., Goerich, D.E., Suter, U., Wegner, M., Sommer, L., Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128 (2001), 3949–3961.
136. Pham, T.D., Gershon, M.D., Rothman, T.P., Time of origin of neurons in the murine enteric nervous system: sequence in relation to phenotype. J. Comp. Neurol. 314 (1991), 789–798.
137. Phusantisampan, T., Sangkhathat, S., Phongdara, A., Chiengkriwate, P., Patrapinyokul, S., Mahasirimongkol, S., Association of genetic polymorphisms in the RET-protooncogene and NRG1 with Hirschsprung disease in Thai patients. J. Hum. Genet. 57 (2012), 286–293.
138. Qu, Z.D., Thacker, M., Castelucci, P., Bagyanszki, M., Epstein, M.L., Furness, J.B., Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res. 334 (2008), 147–161.
139. Ramalho-Santos, M., Melton, D.A., McMahon, A.P., Hedgehog signals regulate multiple aspects of gastrointestinal development. Development 127 (2000), 2763–2772.
140. Rao, M., Nelms, B.D., Dong, L., Salinas-Rios, V., Rutlin, M., Gershon, M.D., Corfas, G., Enteric glia express proteolipid protein 1 and are a transcriptionally unique population of glia in the mammalian nervous system. Glia, 2015.
141. Ratcliffe, E.M., D'Autreaux, F., Gershon, M.D., Laminin terminates the Netrin/DCC mediated attraction of vagal sensory axons. Dev. Neurobiol. 68 (2008), 960–971.
142. Ratcliffe, E.M., Setru, S.U., Chen, J.J., Li, Z.S., D'Autreaux, F., Gershon, M.D., Netrin/DCC-mediated attraction of vagal sensory axons to the fetal mouse gut. J. Comp. Neurol. 498 (2006), 567–580.
143. Ratcliffe, E.M., Fan, L., Mohammed, T.J., Anderson, M., Chalazonitis, A., Gershon, M.D., Enteric neurons synthesize netrins and are essential for the development of the vagal sensory innervation of the fetal gut. Dev. Neurobiol. 71 (2011), 362–373.
144. Rauch, U., Klotz, M., Maas-Omlor, S., Wink, E., Hansgen, A., Hagl, C., Holland-Cunz, S., Schafer, K.H., Expression of intermediate filament proteins and neuronal markers in the human fetal gut. J. Histochem. Cytochem. 54 (2006), 39–46.
145. Rinaman, L., Levitt, P., Establishment of vagal sensorimotor circuits during fetal development in rats. J. Neurobiol. 24 (1993), 641–659.
146. Roberts, D.J., Johnson, R.L., Burke, A.C., Nelson, C.E., Morgan, B.A., Tabin, C., Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121 (1995), 3163–3174.
147. Rossi, J., Herzig, K.H., Voikar, V., Hiltunen, P.H., Segerstrale, M., Airaksinen, M.S., Alimentary tract innervation deficits and dysfunction in mice lacking GDNF family receptor alpha2. J. Clin. Investig. 112 (2003), 707–716.
148. Rossi, J., Luukko, K., Poteryaev, D., Laurikainen, A., Sun, Y.F., Laakso, T., Eerikainen, S., Tuominen, R., Lakso, M., Rauvala, H., Arumae, U., Pasternack, M., Saarma, M., Airaksinen, M.S., Retarded growth and deficits in the enteric and parasympathetic nervous system in mice lacking GFR alpha2, a functional neurturin receptor. Neuron 22 (1999), 243–252.
149. Sasselli, V., Pachnis, V., Burns, A.J., The enteric nervous system. Dev. Biol. 366 (2012), 64–73.
150. Sasselli, V., Boesmans, W., Vanden Berghe, P., Tissir, F., Goffinet, A.M., Pachnis, V., Planar cell polarity genes control the connectivity of enteric neurons. J. Clin. Investig. 123 (2013), 1763–1772.
151. Savidge, T.C., Newman, P., Pothoulakis, C., Ruhl, A., Neunlist, M., Bourreille, A., Hurst, R., Sofroniew, M.V., Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 132 (2007), 1344–1358.
152. Sextier-Sainte-Claire Deville, F., Ziller, C., Le Douarin, N.M., Developmental potentials of enteric neural crest-derived cells in clonal and mass cultures. Dev. Biol. 163 (1994), 141–151.
153. Steinkamp, M., Geerling, I., Seufferlein, T., von Boyen, G., Egger, B., Grossmann, J., Ludwig, L., Adler, G., Reinshagen, M., Glial-derived neurotrophic factor regulates apoptosis in colonic epithelial cells. Gastroenterology 124 (2003), 1748–1757.
154. Stone, D.M., Hynes, M., Armanini, M., Swanson, T.A., Gu, Q., Johnson, R.L., Scott, M.P., Pennica, D., Goddard, A., Phillips, H., Noll, M., Hooper, J.E., de Sauvage, F., Rosenthal, A., The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384 (1996), 129–134.
155. Sukegawa, A., Narita, T., Kameda, T., Saitoh, K., Nohno, T., Iba, H., Yasugi, S., Fukuda, K., The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endodermal epithelium. Development 127 (2000), 1971–1980.
156. Tan, L.L., Bornstein, J.C., Anderson, C.R., The neurochemistry and innervation patterns of extrinsic sensory and sympathetic nerves in the myenteric plexus of the C57Bl6 mouse jejunum. Neuroscience 166 (2010), 564–579.
157. Taniguchi, M., Yuasa, S., Fujisawa, H., Naruse, I., Saga, S., Mishina, M., Yagi, T., Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19 (1997), 519–530.
158. Taraviras, S., Marcos-Gutierrez, C.V., Durbec, P., Jani, H., Grigoriou, M., Sukumaran, M., Wang, L.C., Hynes, M., Raisman, G., Pachnis, V., Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development 126 (1999), 2785–2797.
159. Taylor, M.K., Yeager, K., Morrison, S.J., Physiological Notch signaling promotes gliogenesis in the developing peripheral and central nervous systems. Development 134 (2007), 2435–2447.
160. Teng, H.K., Teng, K.K., Lee, R., Wright, S., Tevar, S., Almeida, R.D., Kermani, P., Torkin, R., Chen, Z.Y., Lee, F.S., Kraemer, R.T., Nykjaer, A., Hempstead, B.L., ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J. Neurosci. 25 (2005), 5455–5463.
161. Tenzen, T., Allen, B.L., Cole, F., Kang, J.S., Krauss, R.S., McMahon, A.P., The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev. Cell 10 (2006), 647–656.
162. Tessarollo, L., Tsoulfas, P., Donovan, M.J., Palko, M.E., Blair-Flynn, J., Hempstead, B.L., Parada, L.F., Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis. Proc. Natl. Acad. Sci. USA 94 (1997), 14776–14781.
163. Tran, T.S., Kolodkin, A.L., Bharadwaj, R., Semaphorin regulation of cellular morphology. Annu. Rev. Cell Dev. Biol. 23 (2007), 263–292.
164. Uesaka, T., Enomoto, H., Neural precursor death is central to the pathogenesis of intestinal aganglionosis in Ret hypomorphic mice. J. Neurosci. 30 (2010), 5211–5218.
165. Uesaka, T., Nagashimada, M., Enomoto, H., GDNF signaling levels control migration and neuronal differentiation of enteric ganglion precursors. J. Neurosci. 33 (2013), 16372–16382.
166. Uesaka, T., Nagashimada, M., Enomoto, H., Neuronal differentiation in Schwann cell lineage underlies postnatal neurogenesis in the enteric nervous system. J. Neurosci. 35 (2015), 9879–9888.
167. Van Landeghem, L., Chevalier, J., Mahe, M.M., Wedel, T., Urvil, P., Derkinderen, P., Savidge, T., Neunlist, M., Enteric glia promote intestinal mucosal healing via activation of focal adhesion kinase and release of proEGF. Am. J. Physiol. 300 (2011), G976–G987.
168. Vitelli, F., Morishima, M., Taddei, I., Lindsay, E.A., Baldini, A., Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum. Mol. Genet. 11 (2002), 915–922.
169. Volosin, M., Song, W., Almeida, R.D., Kaplan, D.R., Hempstead, B.L., Friedman, W.J., Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J. Neurosci. 26 (2006), 7756–7766.
170. Wallace, A.S., Burns, A.J., Development of the enteric nervous system, smooth muscle and intestinal cells of Cajal in the human gastrointestinal tract. Cell Tissue Res. 319 (2005), 367–382.
171. Wang, H., Hughes, I., Planer, W., Parsadanian, A., Grider, J.R., Vohra, B.P., Keller-Peck, C., Heuckeroth, R.O., The timing and location of glial cell line-derived neurotrophic factor expression determine enteric nervous system structure and function. J. Neurosci. 30 (2010), 1523–1538.
172. Wetmore, C., Olson, L., Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. J. Comp. Neurol. 353 (1995), 143–159.
173. Wilkinson, D.J., Bethell, G.S., Shukla, R., Kenny, S.E., Edgar, D.H., Isolation of enteric nervous system progenitor cells from the aganglionic gut of patients with Hirschsprung's disease. PLoS One, 10, 2015, e0125724.
174. Woodward, M.N., Kenny, S.E., Vaillant, C., Lloyd, D.A., Edgar, D.H., Time-dependent effects of endothelin-3 on enteric nervous system development in an organ culture model of Hirschsprung's disease. J. Pediatr. Surg. 35 (2000), 25–29.
175. Worley, D.S., Pisano, J.M., Choi, E.D., Walus, L., Hession, C.A., Cate, R.L., Sanicola, M., Birren, S.J., Developmental regulation of GDNF response and receptor expression in the enteric nervous system. Development 127 (2000), 4383–4393.
176. Wu, J.J., Chen, J.X., Rothman, T.P., Gershon, M.D., Inhibition of in vitro enteric neuronal development by endothelin-3: mediation by endothelin B receptors. Development 126 (1999), 1161–1173.
177. Yan, H., Bergner, A.J., Enomoto, H., Milbrandt, J., Newgreen, D.F., Young, H.M., Neural cells in the esophagus respond to glial cell line-derived neurotrophic factor and neurturin, and are RET-dependent. Dev. Biol. 272 (2004), 118–133.
178. Zhang, W., Kang, J.S., Cole, F., Yi, M.J., Krauss, R.S., Cdo functions at multiple points in the Sonic Hedgehog pathway, and Cdo-deficient mice accurately model human holoprosencephaly. Dev. Cell 10 (2006), 657–665.