Plasticity and neural stem cells in the enteric nervous system

Anatomical Record

Volumn 292, Issue 12, 2009, Pages 1940-1952

  Schäfer, Karl Herbert ^a   Van Ginneken, Chris ^b   Copray, Sjef ^c  

^a UNIVERSITY OF APPLIED SCIENCES KAISERSLAUTERN   (Germany)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Enteric nervous system; Nestin; Neural crest derived stem cells

Indexed keywords

BOTULINUM TOXIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; LAXATIVE; NERVE CELL ADHESION MOLECULE; NEUROMODULIN; PROTEIN S 100;

ABDOMINAL DISTENSION; CALCIUM CELL LEVEL; CONFERENCE PAPER; CONSTIPATION; EMBRYO DEVELOPMENT; ENTERITIS; ENTEROCOLITIS; HIPPOCAMPUS; HIRSCHSPRUNG DISEASE; HUMAN; INTESTINE FLORA; INTESTINE INNERVATION; MYENTERIC PLEXUS; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL DIFFERENTIATION; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL DISEASES; HUMANS; NERVE NET; NEURAL CREST; NEURONAL PLASTICITY; NEURONS; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 73849122703     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21033     Document Type: Conference Paper

References (128)

1. Amariglio N, Hirshberg A, Scheithauer BW, Cohen Y, Loewenthal R, Trakhtenbrot L, Paz N, Koren-Michowitz M, Waldman D, Leider-Trejo L, Toren A, Constantini S, Rechavi G. 2009. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med 6:e1000029.
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 PL, 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. Arciszewski,MB, Sand E, Ekblad E. 2008. Vasoactive intestinal peptide rescues cultured rat myenteric neurons from lipopolysaccharide induced cell death. Regul Pept 146:218-223.
4. Barlow A, de Graaf E, Pachnis V. 2003. Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron 40:905-916.
5. Barlow AJ, Wallace AS, Thapar N, Burns AJ. 2008. Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 135:1681-1691.
6. Bertoni S, Gabella G, Ballabeni V, Ghirardi A, Impicciatore M, Barocelli E. 2006. Plasticity of rat small intestine after removal of a chronic mechanical obstruction. Neurogastroenterol Motil 18:862-872.
7. Bondurand N, Natarajan D, Thapar N, Atkins C, Pachnis V. 2003. Neuron and glia generating progenitors of the mammalian enteric nervous system isolated from foetal and postnatal gut cultures. Development 130:6387-6400.
8. Braak H, de Vos RA, Bohl J, Del Tredici K. 2006. Gastric alpha-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci Lett 396:67-72.
9. Bredt DS. 1999. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res 31:577-596.
10. Brehmer A, Frieser M, Graf M, Radespiel-Troger M, Gobel D, Neuhuber W. 2001. Dendritic hypertrophy of Stach type VI neurons within experimentally altered ileum of pigs. Auton Neurosci 89:31-37.
11. Brehmer A, Gobel D, Frieser M, Graf M, Radespiel-Troger M, Neuhuber W. 2000. Experimental hypertrophy of myenteric neurones in the pig: a morphometric study. Neurogastroenterol Motil 12:155-162.
12. Brooks AS, Oostra BA, Hofstra RM. 2005. Studying the genetics of Hirschsprung's disease: unraveling an oligogenic disorder. Clin Genet 67:6-14.
13. Burns AJ, Le Douarin NM. 1999. The sacral neural crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system. Development 125:4335-4347.
14. Burns AJ, Thapar N. 2006. Advances in ontogeny of the enteric nervous system. Neurogastroenterol Motil 18:876-887.
15. Cabarrocas J, Savidge TC, Liblau RS. 2003. Role of enteric glial cells in inflammatory bowel disease. Glia 41:81-93.
16. Chaumette T, Lebouvier T, Aubert P, Lardeux B, Qin C, Li Q, Accary D, Bézard E, Bruley des Varannes S, Derkinderen P, Neunlist M. 2009. Neurochemical plasticity in the enteric nervous system of a primate animal model of experimental Parkinsonism. Neurogastroenterol Motil 21:215-222.
17. Clarke SR, Shetty AK, Bradley JL, Turner DA. 1994. Reactive astrocytes express the embryonic intermediate neurofilament nestin. Neuroreport 5:1885-1888.
18. Collins SM, Hurst SM, Main C, Stanley E, Khan I, Blennerhassett P, Swain M. 1992. Effect of inflammation of enteric nerves. Cytokine-induced changes in neurotransmitter content and release. Ann NY Acad Sci 664:415-424.
19. Cooke HJ. 2000. Neurotransmitters in neuronal reflexes regulating intestinal secretion. Ann NY Acad Sci 915:77-80.
20. Coskun N, Sindel M, Elpek GO. 2002. Mast cell density, neuronal hypertrophy and nerve growth factor expression in patients with acute appendicitis. Folia Morphol (Warsz ) 61:237-243.
21. Da Silveira ABM, Freitas MA, Oliveira EC, Neto SG, Luquetti AO, Furness JB, Correa-Oliveira R, Reis D. 2009. Glial fibrillary acidic protein and S-100 colocalization in the enteroglial cells in dilated and nondilated portions of colon from chagasic patients. Hum Pathol 40:244-251.
22. De Giorgio R, Guerrini S, Barbara G, Stanghellini V, De Ponti F, Corinaldesi R, Moses PL, Sharkey KA, Mawe GM. 2004. Inflammatory neuropathies of the enteric nervous system. Gastroenterology 126:1872-1883.
23. De Pelet A, Trochet D, Jaubert F, Espinosa-Parrilla Y, Munnich A, Brunet JF, Goridis C, Feingold J, Lyonnet S, Amiel J. 2006. Mutations of the RET gene in isolated and syndromic Hirschsprung's disease in human disclose major and modifier alleles at a single locus. J Med Genet 43:419-423.
24. Dimaline R, Miller SM, Evans D, Noble PJ, Brown P, Poat JA. 1995. Expression of immediate early genes in rat gastric myenteric neurones: a physiological response to feeding. J Physiol 488 (Pt 2):493-499.
25. Di Nardo G, Blandizzi C, Volta U, Colucci R, Stanghellini V, Barbara G, Del Tacca M, Tonini M, Corinaldesi R, De Giorgio R. 2008. Review article: molecular, pathological and therapeutic features of human enteric neuropathies. Aliment Pharmacol Ther 28:25-42.
26. Druckenbrod NR, Epstein ML. 2005. The pattern of neural crest advance in the cecum and colon. Dev Biol 287:123-133.
27. Druckenbrod NR, Epstein ML. 2007. Behavior of enteric enteric neural crest-derived cells varies with respect to the migratory wavefront. Dev Dyn 236:84-92.
28. Druckenbrod NR, Powers PA, Bartley CR, Walker JW, Epstein ML. 2008. Targeting of endothelin receptor-B to the neural crest. Genesis 46:396-400.
29. El-Salhy M, Sandström O, Holmlund F. 1999. Age-induced changes in the enteric nervous system in the mouse. Mech Ageing Dev 107:93-103.
30. Faure C, Chalazonitis A, Rhéaume C, Bouchard G, Sampathkumar SG, Yarema KJ, Gershon MD. 2007. Gangliogenesis in the enteric nervous system: roles of the polysialylation of the neural cell adhesion molecule and its regulation by bone morphogenetic protein-4. Dev Dyn 236:44-59.
31. Feher E, Penzes L. 1987. Density of substance P, vasoactive intestinal polypeptide and somatostatin-containing nerve fibers in the ageing small intestine of the rats. Gerontology 33:341-348.
32. Fitze G, Appelt H, Konig IR, Gorgens H, Stein U, Walther W, Gossen M, Schreiber M, Ziegler A, Roesner D, Schackert HK. 2003. Functional haplotypes of the RET proto-oncogene promoter are associated with Hirschsprung disease (HSCR). Hum Mol Genet 12:3207-3214.
33. Fu M, Chi Hang Lui V, Har Sham M, NgaYin Cheung A, Kwong Hang Tam P. 2003. HOXB5 expression is spatially and temporarily regulated in human embryonic gut during neural crest cell colonization and differentiation of enteric neuroblasts. Dev Dyn 228:1-10.
34. Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T. 2003. Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23:9357-9366.
35. Furness JB, Costa M. 1987.The enteric nervous system. Churchill Livingstone: Edinburgh.
36. Furness JB, Johnson PJ, Pompolo S, Bornstein JC. 1995. Evidence that enteric motility reflexes can be initiated through entirely intrinsic mechanisms in the guinea-pig small intestine. Neurogastroenterol Motil 7:89-96.
37. Furness JB, Jones C, Nurgali K, Clerc N. 2004. Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol 72:143-164.
38. Gabella G. 1989. Fall in the number of myenteric neurons in aging guinea pigs. Gastroenterology 96:1487-1493.
39. Gabella G. 2001. Development and ageing of intestinal musculature and nerves: the guinea-pig taenia coli. J Neurocytol 30:733-766.
40. Gershon MD. 1999. The enteric nervous system: a second brain. Hosp Pract (Minneap ) 34:31-38, 41.
41. Gershon MD, Rothman TP. 1991. Enteric glia. Glia 4:195-204.
42. Giaroni C, De Ponti F, Cosentino M, Lecchini S, Frigo G. 1999. Plasticity in the enteric nervous system. Gastroenterology 117:1438-1458.
43. Götz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788.
44. Haschke G, Schäfer KH, Diener M. 2002. Effect of butyrate on membrane potential, ionic currents and intracellular Ca2+ concentration in cultured rat myenteric neurones. Neurogastroenterol Motil 14:133-142.
45. 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.
46. Ihrie RA, Avarez-Buylla A. 2008. Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331:179-191.
47. Jaeger CB, Toombs JP, Borgens RB. 1993. Grafting in acute spinal cord injury: morphological and immunological aspects of transplanted adult rat enteric ganglia. Neuroscience 52:333-346.
48. Jessen KR, Mirsky R. 1985. Glial fibrillary acidic polypeptides in peripheral glia. Molecular weight, heterogeneity and distribution. J Neuroimmunol 8:377-393.
49. Jiang S, Khan MI, Lu Y, Werstiuk ES, Rathbone MP. 2005. Acceleration of blood-brain barrier formation after transplantation of enteric glia into spinal cords of rats. Exp Brain Res 162:56-62.
50. Jiang S, Khan MI, Wang J, Middlemiss PJ, Werstiuk ES, Wickson R, Rathbone MP. 2003a. Enteric glia promote functional recovery of CTMreflex after dorsal root transection. Neuroreport 14:1301-1304.
51. Jiang S, Wang J, Khan MI, Middlemiss PJ, Salgado-Ceballos H, Werstiuk ES, Wickson R, Rathbone MP. 2003b. Enteric glia promote regeneration of transected dorsal root axons into spinal cord of adult rats. Exp Neurol 181:79-83.
52. Knutson TW, Knutson LF, Hogan DL, Koss MA, Isenberg JI. 1995. Human proximal duodenal ion and water transport. Role of enteric nervous system and carbonic anhydrase. Dig Dis Sci 40:241-246.
53. Krauter EM, Linden DR, Sharkey KA, Mawe GM. 2007. Synaptic plasticity in myenteric neurons of the guinea-pig distal colon: presynaptic mechanisms of inflammation-induced synaptic facilitation. J Physiol 581 (Pt 2):787-800.
54. 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.
55. Lawrence JM, Raisman G, Mirsky R, Jessen KR. 1991. Transplantation of postnatal rat enteric ganglia into denervated adult rat hippocampus. Neuroscience 44:371-379.
56. LeDouarin 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
57. Lin RC, Matesic DF, Marvin M, McKay RD, Brustle O. 1995. Reexpression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 2:79-85.
58. Lindley RM, Hawcutt DB, Connell MG, Almond SN, Vannucchi MG, Faussone-Pellegrini MS, Edgar DH, Kenny SE. 2008. Human and mouse enteric nervous system neurosphere transplants regulate the function of aganglionic embryonic distal colon. Gastroenterology 135:205-216.
59. Metzger M, Caldwell C, Barlow A, Burns AJ, Thapar N. 2008. Enteric nervous system stem cells can be derived from human gut mucosa obtained at endoscopy and used for the treatment of aganglionic gut disorders. Neurogastroenterol Motil 20 (Suppl):11.
60. Micci MA, Kahrig KM, Simmons RS, Sarna SK, Espejo-Navarro MR, Pasricha PJ. 2005a. Neural stem cell transplantation in the stomach rescues gastric function in neuronal nitric oxide synthase-deficient mice. Gastroenterology 129:1817-1824.
61. Micci MA, Pattillo MT, Kahrig KM, Pasricha PJ. 2005b. Caspase inhibition increases survival of neural stem cells in the gastrointestinal tract. Neurogastroenterol Motil 17:557-564.
62. Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G. 2004. Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469:311-324.
63. Milla PJ. 1998. Motility disorders in childhood. Baillieres Clin Gastroenterol 12:775-797.
64. Milla PJ. 1999. Acquired motility disorders in childhood. Can J Gastroenterol 13 Suppl A:76A-84A.
65. MooreMW, Klein RD, Farinas 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.
66. Moriez R, Abdo H, Chaumette T, Faure M, Lardeux B, Neunlist M. 2009. Neuroplasticity and neuroprotection in enteric neurons: role of epithelial cells. Biochem Biophys Res Commun 382:577-582.
67. Natarajan D, Grigoriou M, Marcos-Gutierrez CV, Atkins C, Pachnis V. 1999. Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture. Development 126:157-168.
68. Neunlist M, Aubert P, Bonnaud S, Van LL, Coron E, Wedel T, Naveilhan P, Ruhl A, Lardeux B, Savidge T, Paris F, Galmiche JP. 2007. Enteric glia inhibit intestinal epithelial cell proliferation partly through a TGF-beta1-dependent pathway. Am J Physiol Gastrointest Liver Physiol 292:G231-G241.
69. Neunlist M, Barouk J, Michel K, Just I, Oreshkova T, Schemann M, Galmiche JP. 2003. Toxin B of Clostridium difficile activates human VIP submucosal neurons, in part via an IL-1beta-dependent pathway. Am J Physiol Gastrointest Liver Physiol 285:G1049-G1055.
70. Oste M, Van Ginneken CJ, Van Haver ER, Bjornvad CR, Thymann T, Sangild PT. 2005. The intestinal trophic response to enteral food is reduced in parenterally fed preterm pigs and is associated with more nitrergic neurons. J Nutr 135:2657-2663.
71. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. 1999. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:366-370.
72. Pawlik WW, Gustaw P, Jacobson ED, Sendur R, Czarnobilski K. 1995. Nitric oxide mediates intestinal hyperaemic responses to intraluminal bile-oleate. Pflugers Arch 429:301-305.
73. Pingault V, Bondurand N, Kuhlbrodt K, Goerich DE, Prehu MO, Puliti A, Herbarth B, Hermans-Borgmeyer I, Legius E, Matthijs G, Amiel J, Lyonnet S, Ceccherini I, Romeo G, Smith JC, Read AP, Wegner M, Goossens M. 1998. SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet 18:171-173.
74. Rauch U, Hansgen A, Hagl C, Holland-Cunz S, Schäfer KH. 2006a. Isolation and cultivation of neuronal precursor cells from the developing human enteric nervous system as a tool for cell therapy in dysganglionosis. Int J Colorectal Dis 21:554-559.
75. Rauch U, Klotz M, Maas-Omlor S, Wink E, Hansgen A, Hagl C, Holland-Cunz S, Schäfer KH. 2006b. Expression of intermediate filament proteins and neuronal markers in the human fetal gut. J Histochem Cytochem 54:39-46.
76. Reinshagen M, von BG, Adler G, Steinkamp M. 2002. Role of neurotrophins in inflammation of the gut. Curr Opin Investig Drugs 3:565-568.
77. Rumio C, Besusso D, Arnaboldi F, Palazzo M, Selleri S, Gariboldi S, Akira S, Uematsu S, Bignami P, Ceriani V, Me0 Nard S, Balsari A. 2006. Activation of smooth muscle and myenteric plexus cells of jejunum via toll-like receptor 4. J Cell Physiol 208:47-54
78. Saffrey MJ. 2004. Ageing of the enteric nervous system. Mech Ageing Dev 125:899-906.
79. Sakakibara R, Uchiyama T, Yamanishi T, Shirai K, Hattori T. 2008. Bladder and bowel dysfunction in Parkinson's disease. J Neural Transm 115:443-460.
80. Sandgren K, Ekblad E, Larsson LT. 2000. Survival of neurons and interstitial cells of Cajal after autotransplantation of myenteric ganglia from small intestine in the lethal spotted mouse. Pediatr Surg Int 16:272-276.
81. Sandgren K, Larsson LT, Ekblad E. 2002. Widespread changes in neurotransmitter expression and number of enteric neurons and interstitial cells of Cajal in lethal spotted mice: an explanation for persisting dysmotility after operation for Hirschsprung's disease? Dig Dis Sci 47:1049-1064.
82. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R, Sofroniew MV. 2007a. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 132:1344-1358.
83. Savidge TC, Sofroniew MV, Neunlist M. 2007b. Starring roles for astroglia in barrier pathologies of gut and brain. Lab Invest 87:731-736.
84. Schäfer KH. 2000.Reaggregation of dissociated myenteric plexus in an ECM-Gel as a model for the transplantation of enteric neurons. In: Krammer H-J,Singer MV, editor. Neurogastroenterology-from the basics to the clinics. Kluwer Academic Publishers: Dordrecht/Boston/London. p 123-128.
85. Schäfer KH, Hagl CI, Rauch U. 2003. Differentiation of neurospheres from the enteric nervous system. Ped Surg Int 19:340-344.
86. Schäfer KH, Hansgen A, Mestres P. 1999. Morphological changes of the myenteric plexus during early postnatal development of the rat. Anat Rec 256:20-28.
87. Schäfer KH, Mestres P. 1997. Human newborn and adult myenteric plexus display different growth patterns in tissue culture. Cell Mol Biol 43:1171-1180.
88. Schäfer KH, Mestres P. 1999. Trophic effects of GDNF upon myenteric neurones in vitro decrease with age. Exp Brain Res 125:447-452.
89. Schäfer KH, Mestres P. 2000. Reaggregation of rat dissociated myenteric plexus in extracellular matrix gels. Dig Dis Sci 45:1631-1638.
90. Schäfer KH, Mestres P, März P, Rose-John S. 1999. The IL-6/sIL-6 fusion protein promotes neuronal survival and neurite outgrowth in cultured enteric neurons of the rat small intestine. J Interferon Cytokine Res 19:527-532.
91. Schäfer KH, Micci MA, Pasricha PJ. 2009. Neural stem cell transplantation in the enteric nervous system: roadmaps and roadblocks. Neurogastroenterol Motil 21:103-112.
92. Schäfer KH, Rauch U, Klotz M, Hagl C, Holland-Cunz S, Jester I. 2008. Protein extracts from HSCR smooth muscle enhance neurite outgrowth of enteric neurones and neural crest derived stem cells in vitro. Neurogastroenterol.Motil 20:112.
93. Sharkey KA, Parr EJ, Keenan CM. 1999. Immediate-early gene expression in the inferior mesenteric ganglion and colonic myenteric plexus of the guinea pig. J Neurosci 19:2755-2764.
94. Sidebotham EL, Kenny SE, Lloyd DA, Vaillant CR, Edgar DH. 2002. Location of stem cells for the enteric nervous system. Pediatr Surg Int 18:581-585.
95. Sidebotham EL, Woodward MN, Kenny SE, Lloyd DA, Vaillant CR, Edgar DH. 2001. Assessment of protein gene product 9.5 as a marker of neural crest-derived precursor cells in the developing enteric nervous system. Pediatr Surg Int 17:304-307.
96. Silva AT, Wardhaugh T, Dolatshad NF, Jones S, Saffrey MJ. 2008. Neural progenitors from isolated postnatal rat myenteric ganglia: expansion as neurospheres and differentiation in vitro. Brain Res 1218:47-53.
97. Simmons AM, Tanyu LH, Horowitz SS, Chapman JA, Brown RA. 2008. Developmental and regional patterns of GAP-43 immunoreactivity in a metamorphosing brain. Brain Behav Evol 71:247-262.
98. Starke-Buzetti WA, Oaks JA. 2008. Increased glial-derived neurotrophic factor in the small intestine of rats infected with the tape-worm, Hymenolepis diminuta. Int J Exp Pathol 89:458-65.
99. Stead RH. 1992. Nerve remodelling during intestinal inflammation. Ann NY Acad Sci 664:443-455.
100. Stewart HJ, Cowen T, Curtis R, Wilkin GP, Mirsky R, Jessen KR. 1992. GAP-43 immunoreactivity is widespread in the autonomic neurons and sensory neurons of the rat. Neuroscience 47:673-684.
101. Suarez-Rodriguez R, Belkind-Gerson J. 2004. Cultured nestin-positive cells from postnatal mouse small bowel differentiate ex vivo into neurons, glia, and smooth muscle. Stem Cells 22:1373-1385.
102. Surprenant A. 1994. Control of the gastrointestinal tract by enteric neurons. Annu Rev Physiol 56:117-140.
103. Takahashi T, Qoubaitary A, Owyang C, Wiley JW. 2000. Decreased expression of nitric oxide synthase in the colonic myenteric plexus of aged rats. Brain Res 883:15-21.
104. Tew EM, Saffrey MJ, Anderson PN, Burnstock G. 1996. NADPH-diaphorase- containing enteric neurones survive for a year in the adult rat striatum. Neuroreport 7:958-960.
105. Timmermans JP, Adriaensen D, Cornelissen W, Scheuermann DW. 1997. Structural organization and neuropeptide distribution in the mammalian enteric nervous system, with special attention to those components involved in mucosal reflexes. Comp Biochem Physiol A Physiol 118:331-340.
106. Timmermans JP, Hens J, Adriaensen D. 2001. Outer submucous plexus: an intrinsic nerve network involved in both secretory and motility processes in the intestine of large mammals and humans. Anat Rec 262:71-78.
107. Timmermans JP, Scheuermann DW, Stach W, Adriaensen D, De Groodt-Lasseel MH. 1992. Functional morphology of the enteric nervous system with special reference to large mammals. Eur J Morphol 30:113-122.
108. Tjwa ET, Bradley JM, Keenan CM, Kroese AB, Sharkey KA. 2003. Interleukin-1beta activates specific populations of enteric neurons and enteric glia in the guinea pig ileum and colon. Am J Physiol Gastrointest Liver Physiol 285:G1268-G1276.
109. Vanderwinden JM, Gillard K, De Laet MH, Messam CA, Schiffmann SN. 2002. Distribution of the intermediate filament nestin in the muscularis propria of the human gastrointestinal tract. Cell Tissue Res 309:261-268.
110. Van Ginneken C, Van Meir FJ, Sys S, Weyns A. 2001. Stereologic description of the changing expression of constitutive nitric oxide synthase and heme oxygenase in the enteric plexuses of the pig small intestine during development. J Comp Neurol 437:118-128.
111. Van Ginneken CJ, Van Meir F, Sys S, Weyns A. 2001. Developmental changes in heme-oxygenase-2 and bNOS expression in enteric neurons in the pig duodenum. Auton Neurosci 91:16-25.
112. Van Haver ER, de Vooght L, Oste M, Sangild PT, Thymann T, Weyns AL, Van Ginneken CJ. 2008. Postnatal and diet-dependent increases in enteric glial cells and VIP-containing neurones in preterm pigs. Neurogastroenterol Motil 20:1070-1079.
113. Vasina V, Barbara G, Talamonti L, Stanghellini V, Corinaldesi R, Tonini M, De Ponti F, De Giorgio R. 2006. Enteric neuroplasticity evoked by inflammation. Auton Neurosci 126-127:264-272.
114. Vento P, Kiviluoto T, Keränen U, Heikki JJ, Eero K, Seppo S. 2001. Quantitative comparison of growth-associated Protein-43 and substance P in ulcerative colitis. J Histochem Cytochem 49: 749-757.
115. von Boyen GB, Krammer HJ, Suss A, Dembowski C, Ehrenreich H, Wedel T. 2002a. Abnormalities of the enteric nervous system in heterozygous endothelin B receptor deficient (spotting lethal) rats resembling intestinal neuronal dysplasia. Gut 51:414-419.
116. von Boyen GB, Reinshagen M, Steinkamp M, Adler G, Kirsch J. 2002b. Gut inflammation modulated by the enteric nervous system and neurotrophic factors. Scand J Gastroenterol 37:621-625.
117. von Boyen GB, Steinkamp M, Geerling I, Reinshagen M, Schäfer KH, Adler G, Kirsch J. 2006a. 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.
118. von Boyen GB, Steinkamp M, Reinshagen M, Schäfer KH, Adler G, Kirsch J. 2004. Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 53:222-228.
119. von Boyen GB, Steinkamp M, Reinshagen M, Schäfer KH, Adler G, Kirsch J. 2006b. Nerve growth factor secretion in cultured enteric glia cells is modulated by proinflammatory cytokines. J Neuroendocrinol 18:820-825.
120. Wade PR, Cowen T. 2004. Neurodegeneration: a key factor in the ageing gut. Neurogastroenterol Motil 16:19-23.
121. Wakabayashi K, Takahashi H. 1997. Neuropathology of autonomic nervous system in Parkinson's disease. Eur Neurol 38 (Suppl 2):2-7.
122. Wedel T, Roblick U, Gleiss J, Schiedeck T, Bruch HP, Kuhnel W, Krammer HJ. 1999. Organization of the enteric nervous system in the human colon demonstrated by wholemount immunohistochemistry with special reference to the submucous plexus. Ann Anat 181:327-337.
123. Wood J. 2007. Effects of bacteria on the enteric nervous system. J Clin Gastroenterol 41:7-19.
124. Wood JD. 2008. Enteric Nervous System: reflexes, pattern generators and motility. Curr Opin Gastroenterol 24:149-158.
125. Yamaguchi M, Saito H, Suzuki M, Mori K. 2000. Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport 11:1991-1996.
126. Young HM, Bergner AJ, Anderson RB, Enomoto H, Milbrandt J, Newgreen DF, Whitington. 2004. Dynamics of neural crestderived cell migration in the embryonic mouse gut. Dev Biol 270:455-473.
127. 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.
128. Young HM, 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.