The timing and location of glial cell line-derived neurotrophic factor expression determine enteric nervous system structure and function

Journal of Neuroscience

Volumn 30, Issue 4, 2010, Pages 1523-1538

  Wang, Hongtao ^a   Hughes, Inna ^a   Planer, William ^a   Parsadanian, Alexander ^a   Grider, John R ^b   Vohra, Bhupinder P S ^a   Keller Peck, Cynthia ^a   Heuckeroth, Robert O ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINE ACETYLTRANSFERASE; DIHYDROLIPOAMIDE DEHYDROGENASE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; TRYPTOPHAN HYDROXYLASE;

ANIMAL TISSUE; ARTICLE; CELL CYCLE; CONTROLLED STUDY; ESOPHAGUS; INTESTINE FUNCTION; INTESTINE INNERVATION; MOUSE; NERVE CELL; NERVE GROWTH; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; ENTERIC NERVOUS SYSTEM; ESOPHAGUS; GASTROINTESTINAL MOTILITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYENTERIC PLEXUS; NADPH DEHYDROGENASE; NEURITES; NEUROGENESIS; NEURONS; PROTO-ONCOGENE PROTEINS C-RET; STEM CELLS;

EID: 75349102681     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3861-09.2010     Document Type: Article

References (68)

1. Airaksinen MS, Saarma M (2002) The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 3:383-394.
2. Amiel J, Sproat-Emison E, Garcia-Barcelo M, Lantieri F, Burzynski G, Borrego S, Pelet A, Arnold S, Miao X, Griseri P, Brooks AS, Antinolo G, de Pontual L, Clement-Ziza M, Munnich A, Kashuk C, West K, Wong KK, Lyonnet S, Chakravarti A, Tam PK, Ceccherini I, Hofstra RM, Fernandez R (2008) Hirschsprung disease, associated syndromes and genetics: a review. J Med Genet 45:1-14.
3. Baloh RH, Enomoto H, Johnson EM Jr, Milbrandt J (2000) The GDNF family ligands and receptors: implications for neural development. Curr Opin Neurobiol 10:103-110.
4. 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.
5. Cacalano G, Fariñas I, Wang LC, Hagler K, Forgie A, Moore M, Armanini M, Phillips H, Ryan AM, Reichardt LF, Hynes M, Davies A, Rosenthal A (1998) GFRα1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21:53-62.
6. Chalazonitis A, Rothman TP, Chen J, Gershon MD (1998) 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 GFRa-1 in vitro and in vivo. Dev Biol 204:385-406.
7. 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.
8. Charbel Issa P, Lever IJ, Michael GJ, Bradbury EJ, Malcangio M (2001) Intrathecally delivered glial cell line-derived neurotrophic factor produces electrically evoked release of somatostatin in the dorsal horn of the spinal cord. J Neurochem 78:221-229.
9. Cheng TC, Hanley TA, Mudd J, Merlie JP, Olson EN (1992) Mapping of myogenin transcription during embyrogenesis using transgenes linked to the myogenin control region. J Cell Biol 119:1649-1656.
10. Creedon DJ, Tansey MG, Baloh RH, Osborne PA, Lampe PA, Fahrner TJ, Heuckeroth RO, Milbrandt J, Johnson EM Jr (1997) Neurturin shares receptors and signal transduction pathways with glial cell line-derived neurotrophic factor in sympathetic neurons. Proc Natl Acad Sci U S A 94:7018-7023.
11. Durbec PL, Larsson-Blomberg LB, Schuchardt A, Costantini F, Pachnis V (1996) Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development 122:349-358.
12. Enomoto H, Araki T, Jackman A, Heuckeroth RO, Snider WD, Johnson EM Jr, Milbrandt J (1998) GFRα1 deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21:317-324.
13. Enomoto H, Hughes I, Golden J, Baloh RH, Yonemura S, Heuckeroth RO, Johnson EM Jr, Milbrandt J (2004) GFRalpha1 expression in cells lacking RET is dispensable for organogenesis and nerve regeneration. Neuron 44:623-636.
14. Feng L, Wang CY, Jiang H, Oho C, Mizuno K, Dugich-Djordjevic M, Lu B (1999) Differential effects of GDNF and BDNF on cultured ventral mesencephalic neurons. Brain Res Mol Brain Res 66:62-70.
15. Furness JB (2000) Types of neurons in the enteric nervous system. J Auton Nerv Syst 81:87-96.
16. Gabriel SB, Salomon R, Pelet A, Angrist M, Amiel J, Fornage M, Attié-Bitach T, Olson JM, Hofstra R, Buys C, Steffann J, Munnich A, Lyonnet S, Chakravarti A (2002) Segregation at three loci explains familial and population risk in Hirschsprung disease. Nat Genet 31:89-93.
17. Gariepy CE (2001) Intestinal motility disorders and development of the enteric nervous system. Pediatr Res 49:605-613.
18. Gariepy CE (2004) Developmental disorders of the enteric nervous system: genetic and molecular bases. J Pediatr Gastroenterol Nutr 39:5-11.
19. Gershon MD (1997) Genes and lineages in the formation of the enteric nervous system. Curr Opin Neurobiol 7:101-109.
20. Gershon MD (1999) Lessons from genetically engineered animal models. II. Disorders of enteric neuronal development: insights from transgenic mice. Am J Physiol 277:G262-G267.
21. Gianino S, Grider JR, Cresswell J, Enomoto H, Heuckeroth RO (2003) GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 130:2187-2198.
22. Golden JP, DeMaro JA, Osborne PA, Milbrandt J, Johnson EM Jr (1999) Expression of neurturin, GDNF, and GDNF family-receptor mRNA in the developing and mature mouse. Exp Neurol 158:504-528.
23. Gomes CA, Vaz SH, Ribeiro JA, Sebastião AM (2006) Glial cell line-derived neurotrophic factor (GDNF) enhances dopamine release from striatal nerve endings in an adenosine A2A receptor-dependent manner. Brain Res 1113:129-136.
24. Heanue TA, Pachnis V (2007) Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8:466-479.
25. 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.
26. 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.
27. Heuckeroth RO, Enomoto H, Grider JR, Golden JP, Hanke JA, Jackman A, Molliver DC, Bardgett ME, Snider WD, Johnson EM Jr, Milbrandt J (1999) Gene targeting reveals a critical role for neurturin in the development and maintenance of enteric, sensory, and parasympathetic neurons. Neuron 22:253-263.
28. Iwashita T, Kruger GM, Pardal R, Kiel MJ, Morrison SJ (2003) Hirschsprung disease is linked to defects in neural crest stem cell function. Science 301:972-976.
29. Kablar B, Tajbakhsh S, Rudnicki MA (2000) Transdifferentiation of esophageal smooth to skeletal muscle is myogenic bHLH factor-dependent. Development 127:1627-1639.
30. 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.
31. Keller-Peck CR, Feng G, Sanes JR, Yan Q, Lichtman JW, Snider WD (2001) Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. J Neurosci 21:6136-6146.
32. Kirik D, Rosenblad C, Björklund A (2000) Preservation of a functional nigrostriatal dopamine pathway by GDNF in the intrastriatal 6-OHDA lesion model depends on the site of administration of the trophic factor. Eur J Neurosci 12:3871-3882.
33. 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.
34. Merlie JP, Mudd J, Cheng TC, Olson EN (1994) Myogenin and acetylcholine receptor alpha gene promoters mediate transcriptional regulation in response to motor innervation. J Biol Chem 269:2461-2467.
35. Miller MS, Galligan JJ, Burks TF (1981) Accurate measurement of intestinal transit in the rat. J Pharmacol Methods 6:211-217.
36. Moore BA, Otterbein LE, Türler A, Choi AM, Bauer AJ (2003) Inhaled carbon monoxide suppresses the development of postoperative ileus in the murine small intestine. Gastroenterology 124:377-391.
37. Moore MW, Klein RD, Fariñas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A (1996) Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76-79.
38. Natarajan D, Marcos-Gutierrez C, Pachnis V, de Graaff E (2002) Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development 129:5151-5160.
39. Neuhuber WL,Wörl J, Berthoud HR, Conte B (1994) NADPH-diaphorase- positive nerve fibers associated with motor endplates in the rat esophagus: new evidence for co-innervation of striated muscle by enteric neurons. Cell Tissue Res 276:23-30.
40. Newgreen D, Young HM (2002a) Enteric nervous system: development and developmental disturbances. Part 1. Pediatr Dev Pathol 5:224-247.
41. Newgreen D, Young HM (2002b) Enteric nervous system: development and developmental disturbances. Part 2. Pediatr Dev Pathol 5:329-349.
42. Nguyen QT, Parsadanian AS, Snider WD, Lichtman JW (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279:1725-1729.
43. Passarge E (2002) Dissecting Hirschsprung disease. Nat Genet 31:11-12.
44. 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 314:789-798.
45. Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, Sariola H, Westphal H (1996) Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73-76.
46. Qiao S, Iwashita T, Ichihara M, Murakumo Y, Yamaguchi A, Isogai M, Sakata K, Takahashi M (2009) Increased expression of glial cell line-derived neurotrophic factor and neurturin in a case of colon adenocarcinoma associated with diffuse ganglioneuromatosis. Clin Neuropathol 28:105-112.
47. Rickard SM, Mummery RS, Mulloy B, Rider CC (2003) The binding of human glial cell line-derived neurotrophic factor to heparin and heparan sulfate: importance of 2-O-sulfate groups and effect on its interaction with its receptor, GFRalpha1. Glycobiology 13:419-426.
48. Rosenblad C, Kirik D, Devaux B, Moffat B, Phillips HS, Björklund A (1999) Protection and regeneration of nigral dopaminergic neurons by neurturin or GDNF in a partial lesion model of Parkinson's disease after administration into the striatum or the lateral ventricle. Eur J Neurosci 11:1554-1566.
49. Rothman TP, Tennyson VM, Gershon MD (1986) Colonization of the bowel by the precursors of enteric glia: studies of normal and congenitally aganglionic mutant mice. J Comp Neurol 252:493-506.
50. Saavedra A, Baltazar G, Duarte EP (2008) Driving GDNF expression: the green and the red traffic lights. Prog Neurobiol 86:186-215.
51. Sánchez MP, Silos-Santiago I, Frisén J, He B, Lira SA, Barbacid M (1996) Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70-73.
52. Sang Q, Young HM (1996) Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 284:39-53.
53. Sato Y, Heuckeroth RO (2008) Retinoic acid regulates murine enteric nervous system precursor proliferation, enhances neuronal precursor differentiation, and reduces neurite growth in vitro. Dev Biol 320:185-198.
54. Schuchardt A, D'Agati V, Larsson-Blomberg L, Constantini F, Pachnis V (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367:380-383.
55. Shen L, Pichel JG, Mayeli T, Sariola H, Lu B, Westphal H (2002) Gdnf haploinsufficiency causes Hirschsprung-like intestinal obstruction and earlyonset lethality in mice. Am J Hum Genet 70:435-447.
56. Skoff AM, Resta C, Swamydas M, Adler JE (2003) Nerve growth factor (NGF) and glial cell line-derived neurotrophic factor (GDNF) regulate substance P release in adult spinal sensory neurons. Neurochem Res 28:847-854.
57. Spiller R, Garsed K (2009) Postinfectious irritable bowel syndrome. Gastroenterology 136:1979-1988.
58. Starke-Buzetti WA, Oaks JA (2008) Increased glial-derived neurotrophic factor in the small intestine of rats infected with the tapeworm, Hymenolepis diminuta. Int J Exp Pathol 89:458-465.
59. Steinkamp M, Geerling I, Seufferlein T, von Boyen G, Egger B, Grossmann J, Ludwig L, Adler G, Reinshagen M (2003) Glial-derived neurotrophic factor regulates apoptosis in colonic epithelial cells. Gastroenterology 124:1748-1757.
60. Taraviras S, Marcos-Gutierrez CV, Durbec P, Jani H, Grigoriou M, Sukumaran M, Wang LC, Hynes M, Raisman G, Pachnis V (1999) Signalling by RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development 126:2785-2797.
61. von Boyen GB, Steinkamp M, Geerling I, Reinshagen M, Schäfer KH, Adler G, Kirsch J (2006) Proinflammatory cytokines induce neurotrophic factor expression in enteric glia: a key to the regulation of epithelial apoptosis in Crohn's disease. Inflamm Bowel Dis 12:346-354.
62. Wallace AS, Barlow AJ, Navaratne L, Delalande JM, Tauszig-Delamasure S, Corset V, Thapar N, Burns AJ (2009) Inhibition of cell death results in hyperganglionosis: implications for enteric nervous system development. Neurogastroenterol Motil 21:768-e49.
63. + channels and transmitter release. Neuron 32:99-112.
64. 2+ channels and excitatory synaptic transmission in midbrain dopaminergic neurons. Neurosignals 12:78-88.
65. Yan H, Bergner AJ, Enomoto H, Milbrandt J, Newgreen DF, Young HM (2004) Neural cells in the esophagus respond to glial cell line-derived neurotrophic factor and neurturin, and are RET-dependent. Dev Biol 272:118-133.
66. Yntema CL, Hammond WS (1954) The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol 101:515-541.
67. Young HM, Hearn CJ, Farlie PG, Canty AJ, Thomas PQ, Newgreen DF (2001) GDNF is a chemoattractant for enteric neural cells. Dev Biol 229:503-516.
68. Zhao Z, Alam S, Oppenheim RW, Prevette DM, Evenson A, Parsadanian A (2004) Overexpression of glial cell line-derived neurotrophic factor in the CNS rescues motoneurons from programmed cell death and promotes their long-term survival following axotomy. Exp Neurol 190:356-372.