Genes and lineages in the formation of the enteric nervous system

Current Opinion in Neurobiology

Volumn 7, Issue 1, 1997, Pages 101-109

  Gershon, Michael D ^a  

^a Coll Phys Surgs ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR; TRANSCRIPTION FACTOR;

CELL LINEAGE; CELL MIGRATION; DEVELOPMENT; GENE; INTESTINE INNERVATION; NEURAL CREST; PRECURSOR; PRIORITY JOURNAL; REVIEW;

EID: 0031059861     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(97)80127-4     Document Type: Article

References (81)

1. Gershon MD, Kirchgessner AL, Wade PR. Functional anatomy of the enteric nervous system. Johnson LR, Alpers DH, Jacobson ED, Walsh JH. edn 3 Physiology of the Gastrointestinal Tract. 1:1994;381-422 Raven Press, New York.
2. Furness JB, Costa M. The Enteric Nervous System. 1987;Churchill Livingstone, New York.
3. Le Douarin NM, Teillet MA. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol. 30:1973;31-48.
4. Le Douarin NM, Teillet MA. 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. 41:1974;162-184.
5. Yntema CL, Hammond WS. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol. 101:1954;515-542.
6. Yntema CL, Hammond WS. Experiments on the origin and development of the sacral autonomic nerves in the chick embryo. J Exp Zool. 129:1955;375-414.
7. Pomeranz HD, Gershon MD. Colonization of the avian hindgut by cells derived from the sacral neural crest. Dev Biol. 137:1990;378-394.
8. Pomeranz HD, Rothman TP, Gershon MD. 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. 111:1991;647-655.
9. Serbedzija GN, Burgan S, Fraser SE, Bronner-Fraser M. Vital dye labeling demonstrates a sacral neural crest contribution to the enteric nervous system of chick and mouse embryos. Development. 111:1991;857-866.
10. Epstein ML, Mikawa T, Brown AMC, McFarlin DR. Mapping the origin of the avian enteric nervous system with a retroviral marker. Dev Dyn. 201:1994;236-244.
11. Durbec PL, Larsson-Blomberg LB, Schuchardt A, Costantini F, Pachnis V. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development. 122:1996;349-358.
12. Le Douarin NM, Renaud D, Teillet M-A, LeDouarin GH. Cholinergic differentiation of presumptive adrenergic neuroblasts in interspecific chimaeras after heterotopic transplantations. Proc Natl Acad Sci USA. 72:1975;728-732.
13. Fontaine-Pérus JC, Chanconie M, Le Douarin NM. Differentiation of peptidergic neurons in quail - chick chimeric embryos. Cell Differentiation. 11:1982;183-193.
14. Rothman TP, Sherman D, Cochard P, Gershon MD. Development of the monoaminergic innervation of the avian gut: transient and permanent expression of phenotypic markers. Dev Biol. 116:1986;357-380.
15. Sieber-Blum M, Cohen AM. Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of non-crest cells. Dev Biol. 80:1980;96-106.
16. Duff RS, Langtimm CJ, Richardson MK, Sieber-Blum M. In vitro clonal analysis of progenitor cell patterns in dorsal root and sympathetic ganglia of the quail embryo. Dev Biol. 147:1991;451-459.
17. Ito K, Morita T, Sieber-Blum M. In vitro analysis of mouse neural crest development. Dev Biol. 157:1993;517-525.
18. Ito K, Sieber-Blum M. Pluripotent and developmentally restricted neural-crest-derived cells in posterior visceral arches. Dev Biol. 156:1993;191-200.
19. Artinger KB, Bronner-Fraser M. Partial restriction in the developmental potentail of late emigrating avian neural crest cells. Dev Biol. 149:1992;149-157.
20. Bronner-Fraser M, Fraser SE. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature. 335:1988;161-164.
21. Bronner-Fraser M, Fraser S. Developmental potential of avian trunk neural crest cells in situ. Neuron. 3:1989;755-766.
22. Fraser SE, Bronner-Fraser M. Migrating neural crest cells in the trunk of the avian embryo are multipotent. Development. 112:1991;913-920.
23. Sextier-Sainte-Claire Deville F, Ziller C, Le Douarin NM. Developmental potentialities of cells derived from the truncal neural crest in clonal cultures. Dev Brain Res. 66:1992;1-10.
24. Lo L, Anderson DJ. Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. of outstanding interest Neuron. 15:1995;527-539 A fascinating paper that clearly demonstrate that the colonizing crest-derived cells that arrive in the mammalian bowel are not the same as the cells of the premigratory crest, in that the developmental potential of the émigrés has been reduced: fewer options are open to them and they proliferate less. The authors take advantage of the transient expression of the Ret receptor by enteric neuronal progenitors early in ontogeny to immunoselect these cells and isolate them from their neighbors in the enteric mesenchyme. They use an elegant technique of clonal analysis to study the developmental potential of individual progenitors.
25. Rothman TP, Le Douarin NM, Fontaine-Pérus JC, Gershon MD. Developmental potential of neural crest-derived cells migrating from segments of developing quail bowel back-grafted into younger chick host embryos. Development. 109:1990;411-423.
26. Rothman TP, Le Douarin NM, Fontaine-Pérus JC, Gershon MD. Colonization of the bowel by neural crest-derived cells remigrating from foregut backtransplanted to vagal or sacral regions of host embryos. Dev Dyn. 196:1993;217-233.
27. Coulter HD, Gershon MD, Rothman TP. Neural and glial phenotypic expression by neural crest cells in culture: effects of control and presumptive aganglionic bowel from ls/ls mice. J Neurobiol. 19:1988;507-531.
28. Mackey HM, Payette RF, Gershon MD. Tissue effects on the expression of serotonin, tyrosine hydroxylase and GABA in cultures of neurogenic cells from the neuraxis and branchial arches. Development. 104:1988;205-217.
29. of outstanding interest Trupp M, Arenas E, Fainzilber M, Nilsson A-S, Sieber B-A, Grigoriou M, Kilkenny C, Salazar-Grueso E, Pachnis V, Arumäe U, et al. Functional receptor for GDNF encoded by the c-ret proto-oncogene. of outstanding interest Nature. 381:1996;785-789 One of an important series of papers [30,31,34,37] that identifies GDNF as the functional ligand of the Ret receptor, which had previously been an orphan receptor known to play a critical role in the formation of the ENS.
30. of special interest Treanor JJS, Goodman L, De Sauvage F, Stone DM, Poulsen KT, Beck CD, Gray C, Armanini MP, Pollock RA, Hefti F, et al. Characterization of a multicomponent receptor for GDNF. of outstanding interest Nature. 382:1996;80-83 An important paper that helped to establish that Ret is the functional receptor for GDNF. This report and the ones that follow [31] show that activation of Ret by GDNF requires the interaction of multiple receptor components.
31. Jing S, Wen D, Yu Y, Holst PL, Luo Y, Fang M, Tamir R, Antonio L, Hu Z, Cupples R, et al. GDNF-induced activation of the Ret protein tyrosine kinase is mediated by GDNFR-α, a novel receptor for GDNF. of outstanding interest Cell. 85:1996;1113-1124 Reveals that the receptor for GDNF is not, strictly speaking, the Ret receptor itself. GDNF evidently binds to an α component that, in turn, forms a complex with Ret. The multicomponent nature of this receptor is analogous to that for CNTF, where, again, there is an α component that actually combines the ligand and contributes to the active multicomponent receptor complex.
32. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V. Defect in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature. 367:1994;380-383.
33. Pachnis V, Mankoo B, Costantini F. Expression of the c-ret proto-oncogene during mouse embryogenesis. Development. 119:1993;1005-1017.
34. Moore MW, Klein RD, Farias I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. of outstanding interest Nature. 382:1996;76-79 Reports some of the first evidence that GDNF is vital for the development of the ENS and the kidneys. The observations reveal that the targeted deletion of the ligand, GDNF, induces a syndrome that is similar to the one previously characterized in knock-outs of the receptor, Ret.
35. Pichel JG, Shen L, Sheng HZ, Granholm A-C, Drago J, Grinberg A, Lee EJ, Huang SB, Saarma M, Hoffer BJ, et al. Defects in enteric innervation and kidney development in mice lacking GDNF. of outstanding interest Nature. 382:1996;73-76 Like the preceding paper [34], this study establishes that the knock-out of GDNF leads to the same developmental defects as the knock-out of Ret. In addition to the contribution that these observations make toward demonstrating that Ret is the functional receptor for GDNF, they also show that GDNF plays a previously unsuspected critical role in the development of the ENS.
36. Sénchez M, Silos-Santiago I, Frisén J, He B, Lira S, Barbacid M. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. of outstanding interest Nature. 382:1996;70-73 One of the series of manuscripts that appeared at about the same time [34-37] that demonstrate the potent in situ developmental actions of GDNF. The series, taken as a whole, elevates GDNF from a crowd of natural factors of unknown significance to one of transcendent importance. GDNF not only influences the development of the ENS, but its action is critical for the development of any ENS at all.
37. Durbec P, Marcos-Gutierrez CV, Kilkenny C, Grigoriou M, Wartiowaara K, Suvanto P, Smith D, Ponder B, Costantini F, Saarma M, et al. GDNF signalling through the Ret receptor tyrosine kinase. of outstanding interest Nature. 381:1996;789-793 A very important study from the laboratory of Pachnis, who discovered the critical role played by Ret in the development of the ENS. This study clearly shows that GDNF is the physiological ligand responsible for activating Ret.
38. Johnson JE, Birren SJ, Saito T, Anderson DJ. DNA binding and transcriptional regulatory activity of mammalian achaete-scute homologous (MASH) proteins revealed by interaction with a muscle-specific enhancer. Proc Natl Acad Sci USA. 89:1992;3596-3600.
39. Lo L, Guillemot F, Joyner AL, Anderson DJ. MASH-1: a marker and a mutation for mammalian neural crest development. Perspect Dev Neurobiol. 2:1994;191-201.
40. Guillemot F, Joyner AL. Dynamic expression of the murine achaete-scute homolog (MASH-1) in the developing nervous system. Mech Dev. 42:1993;171-185.
41. Clark MS, Lanigan TM, Page NM, Russo AF. Induction of a serotonergic and neuronal phenotype in thyroid C-cells. of special interest J Neurosci. 15:1995;6167-6178 An excellent investigation and review of the literature that follows up the original observations of Barasch et al. (see [44]), who were the first to show that the crest-derived parafollicular cells of the thyroid are capable of becoming neurons. This study both confirms those findings and documents the neuralization of the serotonergic parafollicular cells in molecular terms. The observations support the idea that parafollicular cells, which like enteric neurons express Mash-1, are members of a common developmental lineage.
42. Guillemot F, Lo L-C, Johnson JE, Auerbach A, Anderson DJ, Joyner AL. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell. 75:1993;463-476.
43. Blaugrund E, Pham TD, Tennyson VM, Lo L, Sommer L, Anderson DJ, Gershon MD. Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers, and Mash-1-dependence. of outstanding interest Development. 122:1996;309-320 The first study to show that the ENS is formed by multiple lineages of precursor cells. Previous investigations had suggested that there might be a common sympathoadrenal/sympathoenteric neuronal progenitor [46]. This investigation, however, indicates that there are at least two progenitor lineages giving rise to the ENS of the bowel below the rostral foregut. One of these, which is like sympathetic neurons (albeit only transiently), is catecholaminergic and shares the Mash-1 dependence of sympathetic neurons as well as the expression of common cell-surface differentiation antigens. Neurons derived from these cells are born early and give rise to all enteric serotonergic neurons. Another lineage of enteric neurons is completely unlike sympathetic neurons in that they are Mash-1 independent and never catecholaminergic. Neurons derived from precursors in this lineage are born late and include CGRP-containing cells.
44. Barasch JM, Mackey H, Tamir H, Nunez EA, Gershon MD. Induction of a neural phenotype in a serotonergic endocrine cell derived from the neural crest. J Neurosci. 7:1987;2874-2883.
45. Anderson DJ, Carnahan JF, Michelsohn A, Patterson PH. Antibody markers identify a common progenitor to sympathetic neurons and chromaffin cells in vivo and reveal the timing of commitment to neuronal differentiation in the sympathoadrenal lineage. J Neurosci. 11:1991;3507-3519.
46. Carnahan JF, Anderson DJ, Patterson PH. Evidence that enteric neurons may derive from the sympathoadrenal lineage. Dev Biol. 148:1991;552-561.
47. Carnahan JF, Patterson PH. The generation of monoclonal antibodies that bind preferentially to adrenal chromaffin cells and the cells of embryonic sympathetic ganglia. J Neurosci. 11:1991;3493-3506.
48. Baetge G, Gershon MD. 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.
49. Baetge G, Pintar JE, Gershon MD. Transiently catecholaminergic (TC) cells in the bowel of fetal rats and mice: precursorsa of non-catecholaminergic enteric neurons. Dev Biol. 141:1990;353-380.
50. NTR can itself mediate responses.
51. Teitelman G, Gershon MD, Rothman TP, Joh TH, Reis DJ. Proliferation and distribution of cells that transiently express a catecholaminergic phenotype during development in mice and rats. Dev Biol. 86:1981;348-355.
52. Gershon MD, Rothman TP, Joh TH, Teitelman GN. Transient and differential expression of aspects of the catecholaminergic phenotype during development of the fetal bowel of rats and mice. J Neurosci. 4:1984;2269-2280.
53. Cochard P, Goldstein M, Black IB. Ontogenetic appearance and disappearance of tyrosine hydroxylase and catecholamines. Proc Natl Acad Sci USA. 75:1978;2986-2990.
54. Teitelman G, Joh TH, Reis DJ. Transient expression of a noradrenergic phenotype in cells of the rat embryonic gut. Brain Res. 158:1978;229-234.
55. Jonakait GM, Wolf J, Cochard P, Goldstein M, Black IB. Selective loss of noradrenergic phenotypic characters in neuroblasts of the rat embryo. Proc Natl Acad Sci USA. 76:1979;4683-4686.
56. Jonakait GM, Rosenthal M, Morrell JI. Regulation of tyrosine hydroxylase mRNA in the catecholaminergic cells of embryonic rat: analysis by in situ hybridization. J Histochem Cytochem. 37:1989;1-5.
57. Baetge G, Schneider KA, Gershon MD. Development and persistence of catecholaminergic neurons in cultured explants of fetal murine vagus nerves and bowel. Development. 110:1990;689-701.
58. Pham TD, Gershon MD, Rothman TP. Time of origin of neurons in the murine enteric nervous system. J Comp Neurol. 314:1991;789-798.
59. Rothman TP, Gershon MD. Phenotypic expression in the developing murine enteric nervous system. J Neurosci. 2:1982;381-393.
60. Chalazonitis A, Rothman TP, Chen J, Lamballe F, Barbacid M, Gershon MD. Neurotrophin-3 induces neural crest-derived cells from fetal rat gut to develop in vitro as neurons or glia. J Neurosci. 14:1994;6571-6584.
61. Pomeranz HD, Rothman TP, Chalazonitis A, Tennyson VM, Gershon MD. Neural crest-derived cells isolated from the gut by immunoselection develop neuronal and glial phenotypes when cultured on laminin. Dev Biol. 156:1993;341-361.
62. Erickson CA, Loring JF, Lester SM. Migratory pathways of HNK-1-immunoreactive neural crest cells in the rat embryo. Dev Biol. 134:1989;112-118.
63. C mRNA in the enteric nervous system. of special interest J Comp Neurol. 368:1996;597-607 Presents an excellent morphological description of cells that express TrkC in the developing and mature ENS and demonstrates that TrkC is probably the only Trk expressed by intrinsic components of the rat ENS.
64. Hoehner JC, Wester T, Páhlman S, Olsen L. Localization of neurotrophin and their high affinity receptors during human enteric nervous system development. Gastroenterology. 110:1996;756-767.
65. Farias I, Jones KR, Backus C, Wang X-Y, Reichardt LF. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature. 369:1994;658-661.
66. Tojo H, Kaisho Y, Nakata M, Matsuoka K, Kitagawa M, Abe T, Takami K, Yamamoto M, Shino A, Igarashi K, et al. Targeted disruption of the neurotrophin-3 gene with lacZ induces loss of trkC-positive neurons in sensory ganglia but not in spinal cords. Brain Res. 669:1995;163-175.
67. Klein R, Silos-Santiago I, Smeyne RJ, Lira SA, Brambilla R, Bryant S, Zhang L, Snider WD, Barbacid M. Disruption of the neurotrophin-3 receptor gene trkC eliminates 1a muscle afferents and results in abnormal movements. Nature. 368:1994;249-251.
68. Lee K-F, Li E, Huber LJ, Landis S, Sharpe AH, Chao MV, Jaenisch R. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell. 69:1992;737-749.
69. DeChiara TM, Vejsada R, Poueymirou WT, Acheson A, Suri C, Conover JC, Friedman B, McClain J, Pan L, Stahl N, et al. Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. of outstanding interest Cell. 83:1995;313-322 A landmark study that establishes the critical role played by CNTFRα in development. The investigation also provides compelling evidence for the existence of a (cytokine) ligand for the CNTFRα receptor that is not CNTF, LIF, or any of the other currently known cytokines.
70. Masu Y, Wold E, Holtmann B, Sendtner M, Brem G, Thoenen H. Disruption of the CNTF gene results in motor neuron degeneration. Nature. 365:1993;27-32.
71. Baynash AG, Hosoda K, Giaid A, Richardson JA, Emoto N, Hammer RE, Yanagisawa M. Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons. Cell. 79:1994;1277-1285.
72. Lane PW. Association of megacolon with two recessive spotting genes in the mouse. J Hered. 57:1966;29-31.
73. Rothman TP, Gershon MD. Regionally defective colonization of the terminal bowel by the precursors of enteric neurons in lethal spotted mutant mice. Neuroscience. 12:1984;1293-1311.
74. Kapur RP, Yost C, Palmiter RD. Aggregation chimeras demonstrate that the primary defect responsible for aganglionic megacolon in lethal spotted mice is not neuroblast autonomous. Development. 117:1993;993-999.
75. Webster W. Embryogenesis of the enteric ganglia in normal mice and in mice that develop congenital aganglionic megacolon. J Embryol Exp Morphol. 30:1973;573-585.
76. Kapur RP, Sweetser DA, Doggett B, Siebert JR, Palmiter RD. Intercellular signals downstream of endothelin receptor-B mediate colonization of the large intestine by enteric neuroblasts. Development. 121:1995;3787-3795.
77. Coventry S, Yost C, Palmiter RD, Kapur RP. Migration of ganglion cell precursors in the ileoceca of normal and lethal spotted embryos, a murine model for Hirschsprung disease. Lab Invest. 71:1994;82-93.
78. Jacobs-Cohen RJ, Payette RF, Gershon MD, Rothman TP. Inability of neural crest cells to colonize the presumptive aganglionic bowel of ls/ls mutant mice: requirement for a permissive microenvironment. J Comp Neurol. 255:1987;425-438.
79. Rothman TP, Goldowitz D, Gershon MD. Inhibition of migration of neural crest-derived cells by the abnormal mesenchyme of the presumptive aganglionic bowel of ls/ls mice: analysis with aggregation and interspecies chimeras. Dev Biol. 159:1993;559-573.
80. Kapur RP, Livingston R, Doggett B, Sweetser DA, Siebert JR, Palmiter RD. Abnormal microenvironmental signals underlie intestinal aganglionosis in Dominant megacolon mutant mice. Dev Biol. 174:1996;360-369.
81. -/- mice. of special interest Dev Biol. 178:1996;498-513 An important investigation that suggests that the EDN-3 mutation in lethal spotted (ls/ls) mice affects the extracellular matrix (causing an increase in the biosynthesis of laminin-1) as well as neurons. The observations support the idea that lack of EDN-3 stimulation exerts two effects on crest-derived enteric neuronal precursors that are attempting to colonize the terminal bowel. One effect may be on the crest-derived cells themselves, but the other is on the extracellular matrix. It seems likely that the effect of EDN-3 deprivation on crest-derived cells is insufficient, by itself, to cause aganglionosis; however, when combined with the excess of laminin-1, the improperly supported crest-derived precursors may differentiate prematurely and fail to complete their colonization of the hindgut. These data are in agreement with observations derived from chimeric mice, which also indicate that the lesion (aganglionosis of the terminal colon) in ls/ls mice (and animals lacking EDN-3 or the EDNRB) is not crest-autonomous [74,76]. The great interest in ls/ls mice and the other EDN/EDNRB knock-out animals is the close resemblance of their developmental defect to that of humans with Hirschsprung's disease [71].