The enteric glia: Identity and functions

GLIA

Volumn 63, Issue 6, 2015, Pages 921-935

  Coelho Aguiar, Juliana de Mattos ^a,b   Bon Frauches, Ana Carina ^a   Gomes, Ana Lúcia Tavares ^c   Veríssimo, Carla Pires ^a,b   Aguiar, Diego Pinheiro ^b,d   Matias, Diana ^a   Thomasi, Beatriz Bastos de Moraes ^c   Gomes, Antoniella Souza ^e   Brito, Gerly Anne de Castro ^e   Moura Neto, Vivaldo ^a  

^a Secretaria de Estado da Saude de Sao Paulo   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^d Institute de Pesquisas   (Brazil)

^e Federal University of Ceará   (Brazil)

Author keywords

Astrocytes; Differentiation; Enteric glia; Enteric nervous system; Neural crest

Indexed keywords

ASTROCYTE; CELL FUNCTION; DEGENERATIVE DISEASE; ENTEROPATHY; GASTROINTESTINAL TRACT; GLIA CELL; HOMEOSTASIS; HUMAN; INTESTINE INJURY; INTESTINE INNERVATION; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PARKINSON DISEASE; PRION DISEASE; PRIORITY JOURNAL; REVIEW; STEM CELL; ANIMAL; CELL COMMUNICATION; GLIA; NERVOUS SYSTEM DEVELOPMENT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CELL COMMUNICATION; ENTERIC NERVOUS SYSTEM; HUMANS; NEUROGENESIS; NEUROGLIA;

EID: 84927965446     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22795     Document Type: Review

References (158)

1. Abbott NJ, Ronnback L, Hansson E. 2006. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7:41-53.
2. Abdo H, Mahe MM, Derkinderen P, Bach-Ngohou K, Neunlist M, Lardeux B. 2012. The omega-6 fatty acid derivative 15-deoxy-Delta(1)(2), (1)(4)-prostaglandin J2 is involved in neuroprotection by enteric glial cells against oxidative stress. J Physiol 590:2739-2750.
3. Albanese V, Lawson VA, Hill AF, Cappai R, Di Guardo G, Staikopoulos V, Thacker M, Furness JB, Chiocchetti R. 2008. Evidence for prion protein expression in enteroglial cells of the myenteric plexus of mouse intestine. Auton Neurosci 140:17-23.
4. Almond S, Lindley RM, Kenny SE, Connell MG, Edgar DH. 2007. Characterisation and transplantation of enteric nervous system progenitor cells. Gut 56:489-496.
5. 2+ elevations in astrocytes in hippocampal slices. J Neurosci 22:2443-2450.
6. Araque A, Parpura V, Sanzgiri RP, Haydon PG. 1999. Tripartite synapses: Glia, the unacknowledged partner. Trends Neurosci 22:208-215.
7. Aube AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, Doulay F, Liblau R, Galmiche JP, Neunlist M. 2006. Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55:630-637.
8. Auerbach L. 1864. Fernere vorlaufige Mitteilung über den Nervenapparat des Darmes. Arch Pathol Anat Physiol 30:457-460.
9. Bach-Ngohou K, Mahe MM, Aubert P, Abdo H, Boni S, Bourreille A, Denis MG, Lardeux B, Neunlist M, Masson D. 2010. Enteric glia modulate epithelial cell proliferation and differentiation through 15-deoxy-12, 14-prostaglandin J2. J Physiol 588:2533-2544.
10. Bayliss WM, Starling EH. 1899. The movements and innervation of the small intestine. J Physiol 24:99-143.
11. Becker L, Peterson J, Kulkarni S, Pasricha PJ. 2013. Ex vivo neurogenesis within enteric ganglia occurs in a PTEN dependent manner. PLoS One 8:e59452.
12. Bergami M, Santi S, Formaggio E, Cagnoli C, Verderio C, Blum R, Berninger B, Matteoli M, Canossa M. 2008. Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J Cell Biol 183:213-221.
13. Bernstein CN, Vidrich A. 1994. Isolation, identification, and culture of normal mouse colonic glia. Glia 12:108-116.
14. Bezzi P, Volterra A. 2001. A neuron-glia signalling network in the active brain. Curr Opin Neurobiol 11:387-394.
15. Blandini F, Balestra B, Levandis G, Cervio M, Greco R, Tassorelli C, Colucci M, Faniglione M, Bazzini E, Nappi G, Clavenzani P, Vigneri S, De Giorgio R, Tonini M. 2009. Functional and neurochemical changes of the gastrointestinal tract in a rodent model of Parkinson's disease. Neurosci Lett 467:203-207.
16. Blum AE, Joseph SM, Przybylski RJ, Dubyak GR. 2008. Rho-family GTPases modulate Ca(2+)-dependent ATP release from astrocytes. Am J Physiol Cell Physiol 295:C231-C241.
17. Boesmans W, Martens MA, Weltens N, Hao MM, Tack J, Cirillo C, Vanden Berghe P. 2013. Imaging neuron-glia interactions in the enteric nervous system. Front Cell Neurosci 7:183.
18. Bohorquez DV, Samsa LA, Roholt A, Medicetty S, Chandra R, Liddle RA. 2014. An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy. PLoS One 9:e89881.
19. Bondurand N, Natarajan D, Barlow A, Thapar N, Pachnis V. 2006. Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development 133:2075-2086.
20. 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.
21. Bondurand N, Sham MH. 2013. The role of SOX10 during enteric nervous system development. Dev Biol 382:330-343.
22. Bowman CC, Rasley A, Tranguch SL, Marriott I. 2003. Cultured astrocytes express toll-like receptors for bacterial products. Glia 43:281-291.
23. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. 2003. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24:197-211.
24. Braga CA, Follmer C, Palhano FL, Khattar E, Freitas MS, Romão L, Di Giovanni S, Lashuel HA, Silva JL, Foguel D. 2011. The anti-Parkinsonian drug selegiline delays the nucleation phase of alpha-synuclein aggregation leading to the formation of nontoxic species. J Mol Biol 405:254-273.
25. 2+ transients in myenteric glial cells during the colonic migrating motor complex in the isolated murine large intestine. J Physiol 590:335-350.
26. Burns AJ. 2005. Migration of neural crest-derived enteric nervous system precursor cells to and within the gastrointestinal tract. Int J Dev Biol 49:143-150.
27. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH, Sofroniew MV. 1998. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93:189-201.
28. Cersosimo MG, Benarroch EE. 2012. Pathological correlates of gastrointestinal dysfunction in Parkinson's disease. Neurobiol Dis 46:559-564.
29. Chadwick VS, Chen W, Shu D, Paulus B, Bethwaite P, Tie A, Wilson I. 2002. Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 122:1778-1783.
30. Chalazonitis A, D'Autréaux F, Guha U, Pham TD, Faure C, Chen JJ, Roman D, Kan L, Rothman TP, Kessler JA, Gershon MD. 2004. Bone morphogenetic protein-2 and -4 limit the number of enteric neurons but promote development of a TrkC-expressing neurotrophin-3-dependent subset. J Neurosci 24:4266-4282.
31. Chalazonitis A, D'Autréaux F, Pham TD, Kessler JA, Gershon MD. 2011. Bone morphogenetic proteins regulate enteric gliogenesis by modulating ErbB3 signaling. Dev Biol 350:64-79.
32. Cheadle GA, Costantini TW, Lopez N, Bansal V, Eliceiri BP, Coimbra R. 2013. Enteric glia cells attenuate cytomix-induced intestinal epithelial barrier breakdown. PLoS One 8:e69042.
33. Christofi FL, Hanani M, Maudlej N, Wood JD. 1993. Enteric glial cells are major contributors to formation of cyclic AMP in myenteric plexus cultures from adult guinea-pig small intestine. Neurosci Lett 159:107-110.
34. Cirillo C, Sarnelli G, Esposito G, Grosso M, Petruzzelli R, Izzo P, Cali G, D'Armiento FP, Rocco A, Nardone G, Iuvone T, Steardo L, Cuomo R. 2009. Increased mucosal nitric oxide production in ulcerative colitis is mediated in part by the enteroglial-derived S100B protein. Neurogastroenterol Motil 21:e1209-e1112.
35. Cirillo C, Sarnelli G, Turco F, Mango A, Grosso M, Aprea G, Masone S, Cuomo R. 2011. Proinflammatory stimuli activates human-derived enteroglial cells and induces autocrine nitric oxide production. Neurogastroenterol Motil 23:e372-e382.
36. Clairembault T, Kamphuis W, Leclair-Visonneau L, Rolli-Derkinderen M, Coron E, Neunlist M, Hol EM, Derkinderen P. 2014. Enteric GFAP expression and phosphorylation in Parkinson's disease. J Neurochem 130:805-815.
37. Coelho-Aguiar JM, Le Douarin NM, Dupin E. 2013. Environmental factors unveil dormant developmental capacities in multipotent progenitors of the trunk neural crest. Dev Biol 384:13-25.
38. Colombel JF, Sandborn WJ, Reinisch W, Mantzaris GJ, Kornbluth A, Rachmilewitz D, Lichtiger S, D'Haens G, Diamond RH, Broussard DL, Tang KL, van der Woude CJ, Rutgeerts P, SONIC Study Group. 2010. Infliximab, azathioprine, or combination therapy for Crohn's disease. N Engl J Med 362:1383-1395.
39. Cornet A, Savidge TC, Cabarrocas J, Deng WL, Colombel JF, Lassmann H, Desreumaux P, Liblau RS. 2001. Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease? Proc Natl Acad Sci U S A 98:13306-13311.
40. Cronier S, Carimalo J, Schaeffer B, Jaumain E, Beringue V, Miquel MC, Laude H, Peyrin JM. 2012. Endogenous prion protein conversion is required for prion-induced neuritic alterations and neuronal death. FASEB J 26:3854-3861.
41. De Giorgio R, Giancola F, Boschetti E, Abdo H, Lardeux B, Neunlist M. 2012. Enteric glia and neuroprotection: Basic and clinical aspects. Am J Physiol Gastrointest Liver Physiol 303:G887-G893.
42. Devos D, Lebouvier T, Lardeux B, Biraud M, Rouaud T, Pouclet H, Coron E, Bruley des Varannes S, Naveilhan P, Nguyen JM, Neunlist M, Derkinderen P. 2013. Colonic inflammation in Parkinson's disease. Neurobiol Dis 50:42-48.
43. Diniz LP, Almeida JC, Tortelli V, Vargas Lopes C, Setti-Perdigao P, Stipursky J, Kahn SA, Romão LF, de Miranda J, Alves-Leon SV, de Souza JM, Castro NG, Panizzutti R, Gomes FC. 2012. Astrocyte-induced synaptogenesis is mediated by transforming growth factor beta signaling through modulation of d-serine levels in cerebral cortex neurons. J Biol Chem 287:41432-41445.
44. Dogiel AS. 1899. Über den Bau der Ganglien in den Gefl echten des Darmes und der Gallenblase des Menschen und der Säugetiere. Arch Anat Physiol Leipzig Anat Abt Jg 1899:130-158.
45. Dulac C, Le Douarin NM. 1991. Phenotypic plasticity of Schwann cells and enteric glial cells in response to the microenvironment. Proc Natl Acad Sci U S A 88:6358-6362.
46. Dupin E, Coelho-Aguiar JM. 2013. Isolation and differentiation properties of neural crest stem cells. Cytometry A 83:38-47.
47. 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.
48. Erlich RB, Kahn SA, Lima FR, Muras AG, Martins RA, Linden R, Chiarini LB, Martins VR, Moura Neto V. 2007. STI1 promotes glioma proliferation through MAPK and PI3K pathways. Glia 55:1690-1698.
49. Esposito G, Capoccia E, Turco F, Palumbo I, Lu J, Steardo A, Cuomo R, Sarnelli G, Steardo L. 2013. Palmitoylethanolamide improves colon inflammation through an enteric glia/toll like receptor 4-dependent PPAR-α activation. Gut 63:1300-1312.
50. Esposito G, Cirillo C, Sarnelli G, De Filippis D, D'Armiento FP, Rocco A, Nardone G, Petruzzelli R, Grosso M, Izzo P, Iuvone T, Cuomo R. 2007. Enteric glial-derived S100B protein stimulates nitric oxide production in celiac disease. Gastroenterology 133:918-925.
51. Faria J, Romão L, Martins S, Alves T, Mendes FA, de Faria GP, Hollanda R, Takiya C, Chimelli L, Morandi V, de Souza JM, Abreu JG, Moura Neto V. 2006. Interactive properties of human glioblastoma cells with brain neurons in culture and neuronal modulation of glial laminin organization. Differentiation 74:562-572.
52. Ferri G-L, Probert L, Cocchia D, Michetti F, Marangos PJ, Polak JM. 1982. Evidence for the presence of S-100 protein in the glial component of the human enteric nervous system. Nature 297:409-410.
53. Flamant M, Aubert P, Rolli-Derkinderen M, Bourreille A, Neunlist MR, Mahe MM, Meurette G, Marteyn B, Savidge T, Galmiche JP, Sansonetti PJ, Neunlist M. 2011. Enteric glia protect against Shigella flexneri invasion in intestinal epithelial cells: A role for S-nitrosoglutathione. Gut 60:473-84.
54. Fonseca AC, Romao L, Amaral RF, Assad Kahn S, Lobo D, Martins S, Marcondes de Souza J, Moura-Neto V, Lima FR. 2012. Microglial stress inducible protein 1 promotes proliferation and migration in human glioblastoma cells. Neuroscience 200:130-141.
55. Froes MM, Correia AH, Garcia-Abreu J, Spray DC, Campos de Carvalho AC, Neto MV. 1999. Gap-junctional coupling between neurons and astrocytes in primary central nervous system cultures. Proc Natl Acad Sci U S A 96:7541-7546.
56. Fu M, Lui VC, Sham MH, Pachnis V, Tam PK. 2004. Sonic hedgehog regulates the proliferation, differentiation, and migration of enteric neural crest cells in gut. J Cell Biol 166:673-684.
57. Fujita T, Tozaki-Saitoh H, Inoue K. 2009. P2Y1 receptor signaling enhances neuroprotection by astrocytes against oxidative stress via IL-6 release in hippocampal cultures. Glia 57:244-257.
58. Furness JB. 2006. The enteric nervous system. Oxford: Blackwell.
59. Furness JB, Costa M. 1980. Types of nerves in the enteric nervous system. Neuroscience 5:1-20.
60. Gabella G. 1972. Fine structure of the myenteric plexus in the guinea-pig ileum. J Anat 111:69-97.
61. Gabella G. 1981. Ultrastructure of the nerve plexuses of the mammalian intestine: The enteric glial cells. Neuroscience 6:425.
62. Garcia-Abreu J, Silva LC, Tovar FF, Onofr GR, Cavalcante LA, Moura Neto V. 1996. Compartmental distribution of sulfated glycosaminoglycans in lateral and medial midbrain astroglial cultures. Glia 17:339-344.
63. Gomes FC, Garcia-Abreu J, Galou M, Paulin D, Moura Neto V. 1999a. Neurons induce GFAP gene promoter of cultured astrocytes from transgenic mice. Glia 26:97-108.
64. Gomes FC, Maia CG, de Menezes JR, Neto VM. 1999b. Cerebellar astrocytes treated by thyroid hormone modulate neuronal proliferation. Glia 25:247-255.
65. Grinspan JB, Edell E, Carpio DF, Beesley JS, Lavy L, Pleasure D, Golden JA. 2000. Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J Neurobiol 43:1-17.
66. Gulbransen BD, Bains JS, Sharkey KA. 2010. Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J Neurosci 30:6801-6809.
67. Gulbransen BD, Bashashati M, Hirota SA, Gui X, Roberts JA, MacDonald JA, Muruve DA, McKay DM, Beck PL, Mawe GM, Thompson RJ, Sharkey KA. 2012. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med 18:600-604.
68. Gulbransen BD, Sharkey KA. 2009. Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136:1349-1358.
69. Gulbransen BD, Sharkey KA. 2012. Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev: Gastroenterol Hepatol 9:625-632.
70. Hamby ME, Sofroniew MV. 2010. Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics 7:494-506.
71. Hanani M, Reichenbach A. 1994. Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res 278:153-160.
72. Hartmann CA, Martins VR, Lima FR. 2013. High levels of cellular prion protein improve astrocyte development. FEBS Lett 587:238-244.
73. 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.
74. Heanue TA, Pachnis V. 2011. Prospective identification and isolation of enteric nervous system progenitors using Sox2. Stem Cells 29:128-140.
75. Heinrich C, Blum R, Gascon S, Masserdotti G, Tripathi P, Sanchez R, Tiedt S, Schroeder T, Gotz M, Berninger B. 2010. Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol 8:e1000373.
76. Hetz S, Acikgoez A, Voss U, Nieber K, Holland H, Hegewald C, Till H, Metzger R, Metzger M. 2014. In vivo transplantation of neurosphere-like bodies derived from the human postnatal and adult enteric nervous system: a pilot study. PLoS One 9:e93605.
77. 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.
78. Hinkle JL. 1998. Biological and behavioral correlates of stroke and depression. J Neurosci Nurs 30:25-31.
79. Hoff S, Zeller F, Weyhrn CWHV, Wegner M, Schemann M, Michel K, Ruhl A. 2008. Quantitative Assessment of glial cells in the human and guinea pig enteric nervous system with an anti-Sox8/9/10 antibody. J Comp Neurol 509:356-371.
80. Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R, Rauvala H. 2000. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem 275:40096-40105.
81. Ihrie RA, Alvarez-Buylla A. 2008. Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331:179-191.
82. Izmiryan A, Cheraud Y, Khanamiryan L, Leterrier JF, Federici T, Peltekian E, Moura-Neto V, Paulin D, Li Z, Xue ZG. 2006. Different expression of synemin isoforms in glia and neurons during nervous system development. Glia 54:204-213.
83. Jessen KR, Mirsky R. 1980. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 286:736-737.
84. Jessen KR, Mirsky R. 1983. Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3:2206-2218.
85. Jessen KR, Mirsky R. 1985. Glial fibrillary acidic polypeptides in peripheral glia. Molecular weight, heterogeneity and distribution. J Neuroimmunol 8:377-393.
86. Joseph NM, He S, Quintana E, Kim YG, Núñez G, Morrison SJ. 2011. Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J Clin Invest 121:3398-3411.
87. Kang N, Peng H, Yu Y, Stanton PK, Guilarte TR, Kang J. 2013. Astrocytes release d-serine by a large vesicle. Neuroscience 240:243-257.
88. Komuro T, Baluk P, Burnstock G. 1982. An ultrastructural study of neurons and non-neuronal cells in the myenteric plexus of the rabbit colon. Neuroscience 7:1797-806.
89. Kovacs GG, Budka H. 2008. Prion diseases: from protein to cell pathology. Am J Pathol 172:555-565.
90. 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.
91. Kujala P, Raymond CR, Romeijn M, Godsave SF, van Kasteren SI, Wille H, Prusiner SB, Mabbott NA, Peters PJ. 2011. Prion uptake in the gut: identification of the first uptake and replication sites. PLoS Pathog 7:e1002449.
92. Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Berghe PV, Pachnis V. 2011. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest 121:3412-3424.
93. Le Douarin NM, Creuzet S, Couly G, Dupin E. 2004. Neural crest cell plasticity and its limits. Development 131:4637-4650.
94. Le Douarin NM, Kalcheim C. 1999. The neural crest: Cambridge, New York: Cambridge University Press.
95. 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.
96. Lebouvier T, Neunlist M, Bruley des Varannes S, Coron E, Drouard A, N'Guyen JM, Chaumette T, Tasselli M, Paillusson S, Flamand M, Jean-Paul Galmiche, Philippe Damier, Pascal Derkinderen. 2010. Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms. PLoS One 5:e12728.
97. Lee HU, Yamazaki Y, Tanaka KF, Furuya K, Sokabe M, Hida H, Takao K, Miyakawa T, Fujii S, Ikenaka K. 2013. Increased astrocytic ATP release results in enhanced excitability of the hippocampus. Glia 61:210-224.
98. Lee M, McGeer EG, McGeer PL. 2011. Mechanisms of GABA release from human astrocytes. Glia 59:1600-1611.
99. Lee SI, Jeon MH, Kim JS, Park JK, Park EW, Jeon IS, Byun SJ. 2014. The miR-302 cluster transcriptionally regulated by POUV, SOX and STAT5B controls the undifferentiated state through the post-transcriptional repression of PBX3 and E2F7 in early chick development. Mol Reprod Dev 81:1103-1114.
100. Lima FR, Arantes CP, Muras AG, Nomizo R, Brentani RR, Martins VR. 2007. Cellular prion protein expression in astrocytes modulates neuronal survival and differentiation. J Neurochem 103:2164-2176.
101. Lindley RM, Hawcutt DB, Connell MG, Almond SL, 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 e6.
102. Lindley RM, Hawcutt DB, Connell MG, Edgar DH, Kenny SE. 2009. Properties of secondary and tertiary human enteric nervous system neurospheres. J Pediatr Surg 44:1249-1255; discussion 1255-1256.
103. Liu MT, Kuan YH, Wang J, Hen R, Gershon MD. 2009. 5-HT4 receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice. J Neurosci 29:9683-9699.
104. 2+ dynamics and consequent glutamate release from rat astrocytes. Glia 56:821-835.
105. Metzger M, Caldwell C, Barlow AJ, Burns AJ, Thapar N. 2009. Enteric nervous system stem cells derived from human gut mucosa for the treatment of aganglionic gut disorders. Gastroenterology 136:2214-2225 e1-3.
106. Miampamba M, Sharkey AK. 1999. c-Fos expression in the myenteric plexus, spinal cord and brainstem following injection of formalin in the rat colonic wall. J Auton Nerv Syst 77:140-151.
107. Mucke L, Eddleston M. 1993. Astrocytes in infectious and immune-mediated diseases of the central nervous system. FASEB J 7:1226-1232.
108. Mundell NA, Labosky PA. 2011. Neural crest stem cell multipotency requires Foxd3 to maintain neural potential and repress mesenchymal fates. Development 138:641-652.
109. Mundell NA, Plank JL, LeGrone AW, Frist AY, Zhu L, Shin MK, Southard-Smith EM, Labosky PA. 2012. Enteric nervous system specific deletion of Foxd3 disrupts glial cell differentiation and activates compensatory enteric progenitors. Dev Biol 363:373-387.
110. Neunlist M, Aubert P, Bonnaud S, Van Landeghem L, 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.
111. Neunlist M, Van Landeghem L, Mahe MM, Derkinderen P, des Varannes SB, Rolli-Derkinderen M. 2013. The digestive neuronal-glial-epithelial unit: a new actor in gut health and disease. Nat Rev Gastroenterol Hepatol 10:90-100.
112. Ngan ES, Garcia-Barcelo MM, Yip BH, Poon HC, Lau ST, Kwok CK, Sat E, Sham MH, Wong KK, Wainwright BJ, Cherny SS, Hui CC, Sham PC, Lui VC, Tam PK. 2011. Hedgehog/Notch-induced premature gliogenesis represents a new disease mechanism for Hirschsprung disease in mice and humans. J Clin Invest 121:3467-3478.
113. Nishiyama C, Uesaka T, Manabe T, Yonekura Y, Nagasawa T, Newgreen DF, Young HM, Enomoto H. 2012. Trans-mesenteric neural crest cells are the principal source of the colonic enteric nervous system. Nat Neurosci 15:1211-1218.
114. Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M. 2009. Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276-3287.
115. Okamura Y, Saga Y. 2008. Notch signaling is required for the maintenance of enteric neural crest progenitors. Development 135:3555-3565.
116. Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, Honda Y, Takahashi M. 2004. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A 101:13654-13659.
117. Oppenheim RW, Houenou LJ, Parsadanian AS, Prevette D, Snider WD, Shen L. 2000. Glial cell line-derived neurotrophic factor and developing mammalian motoneurons: regulation of programmed cell death among motoneuron subtypes. J Neurosci 20:5001-5011.
118. Pardal R. 2007. As elites de Évora ao tempo da dominação Filipina: estratégias de controlo do poder local (1580-1640). Lisbon: Edições Colibri. pp 210.
119. Perea G, Araque A. 2005. Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25:2192-2203.
120. Rauch U, Hansgen A, Hagl C, Holland-Cunz S, Schafer KH. 2006. 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.
121. Romão LF, Mendes FA, Feitosa NM, Faria JC, Coelho-Aguiar JM, de Souza JM, Moura Neto V, Abreu JG. 2013. Connective tissue growth factor (CTGF/CCN2) is negatively regulated during neuron-glioblastoma interaction. PLoS One 8:e55605.
122. Romão LF, Sousa Vde O, Neto VM, Gomes FC. 2008. Glutamate activates GFAP gene promoter from cultured astrocytes through TGF-beta1 pathways. J Neurochem 106:746-756.
123. Rothermundt M, Peters M, Prehn JH, Arolt V. 2003. S100B in brain damage and neurodegeneration. Microsc Res Tech 60:614-632.
124. 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.
125. Ruhl A. 2005. Glial cells in the gut. Neurogastroenterol Motil 17:777-790.
126. Ruhl A, Trotter J, Stremmel W. 2001. Isolation of enteric glia and establishment of transformed enteroglial cell lines from the myenteric plexus of adult rat. Neurogastroenterol Motil 13:95-106.
127. Sasselli V, Pachnis V, Burns AJ. 2012. The enteric nervous system. Dev Biol 366:64-73.
128. 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.
129. Savidge TC, Sofroniew MV, Neunlist M. 2007b. Starring roles for astroglia in barrier pathologies of gut and brain. Lab Invest 87:731-736.
130. Schafer KH, Hagl CI, Rauch U. 2003. Differentiation of neurospheres from the enteric nervous system. Pediatr Surg Int 19:340-344.
131. Seelig DM, Mason GL, Telling GC, Hoover EA. 2011. Chronic wasting disease prion trafficking via the autonomic nervous system. Am J Pathol 179:1319-1328.
132. Segura BJ, Zhang W, Cowles RA, Xiao L, Lin TR, Logsdon C, Mulholland MW. 2004. Lysophosphatidic acid stimulates calcium transients in enteric glia. Neuroscience 123:687-693.
133. Shannon KM, Keshavarzian A, Dodiya HB, Jakate S, Kordower JH. 2012. Is alpha-synuclein in the colon a biomarker for premotor Parkinson's disease? Evidence from 3 cases. Mov Disord 27:716-719.
134. Sigge W, Wedel T, Kuhnel W, Krammer HJ. 1998. Morphologic alterations of the enteric nervous system and deficiency of non-adrenergic non-cholinergic inhibitory innervation in neonatal necrotizing enterocolitis. Eur J Pediatr Surg 8:87-94.
135. Sokol H, Polin V, Lavergne-Slove A, Panis Y, Treton X, Dray X, Bouhnik Y, Valleur P, Marteau P. 2009. Plexitis as a predictive factor of early postoperative clinical recurrence in Crohn's disease. Gut 58:1218-1225.
136. Steinkamp M, Gundel H, Schulte N, Spaniol U, Pflueger C, Zizer E, von Boyen GB. 2012a. GDNF protects enteric glia from apoptosis: Evidence for an autocrine loop. BMC Gastroenterol 12:6.
137. Steinkamp M, Schulte N, Spaniol U, Pfluger C, Hartmann C, Kirsch J, von Boyen GB. 2012b. Brain derived neurotrophic factor inhibits apoptosis in enteric glia during gut inflammation. Med Sci Monit 18:BR117-BR122.
138. Stutz B, da Conceicao FS, Santos LE, Cadilhe DV, Fleming RL, Acquarone M, Gardino PF, de Melo Reis RA, Dickson PW, Dunkley PR, Rehen S, Houzel JC, de Mello FG. 2014. Murine dopaminergic Muller cells restore motor function in a model of Parkinson's disease. J Neurochem 128:829-840.
139. 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.
140. 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.
141. Turco F, Sarnelli G, Cirillo C, Palumbo I, De Giorgi F, D'Alessandro A, Cammarota M, Giuliano M, Cuomo R. 2014. Enteroglial-derived S100B protein integrates bacteria-induced Toll-like receptor signalling in human enteric glial cells. Gut 63:105-115.
142. Uesaka T, Nagashimada M, Enomoto H. 2013. GDNF signaling levels control migration and neuronal differentiation of enteric ganglion precursors. J Neurosci 33:16372-16382.
143. Van Landeghem L, Chevalier J, Mahe MM, Wedel T, Urvil P, Derkinderen P, Savidge T, Neunlist M. 2011. Enteric glia promote intestinal mucosal healing via activation of focal adhesion kinase and release of proEGF. Am J Physiol Gastrointest Liver Physiol 300:G976-G987.
144. Van Landeghem L, Mahé MM, Teusan R, Léger J, Guisle I, Houlgatte R, Neunlist M. 2009. Regulation of intestinal epithelial cells transcriptome by enteric glial cells: impact on intestinal epithelial barrier functions. BMC Genomics 10:507.
145. Viader A, Wright-Jin EC, Vohra BP, Heuckeroth RO, Milbrandt J. 2011. Differential regional and subtype-specific vulnerability of enteric neurons to mitochondrial dysfunction. PLoS One 6:e27727.
146. von Boyen G, Steinkamp M. 2006. The enteric glia and neurotrophic factors. Z Gastroenterol 44:985-990.
147. von Boyen G, Steinkamp M. 2010. The role of enteric glia in gut inflammation. Neuron Glia Biol 6:231-236.
148. von Boyen GB, Schulte N, Pfluger C, Spaniol U, Hartmann C, Steinkamp M. 2011. Distribution of enteric glia and GDNF during gut inflammation. BMC Gastroenterol 11:3.
149. von Boyen GB, Steinkamp M, Adler G, Kirsch J. 2006a. Glutamate receptor subunit expression in primary enteric glia cultures. J Recept Signal Transduct Res 26:329-336.
150. von Boyen GB, Steinkamp M, Reinshagen M, Schafer KH, Adler G, Kirsch J. 2004. Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 53:222-228.
151. von Boyen GB, Steinkamp M, Reinshagen M, Schafer 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.
152. Wallace AS, Burns AJ. 2005. Development of the enteric nervous system, smooth muscle and interstitial cells of Cajal in the human gastrointestinal tract. Cell Tissue Res 319:367-82.
153. Wedel T, Krammer HJ, Kuhnel W, Sigge W. 1998. Alterations of the enteric nervous system in neonatal necrotizing enterocolitis revealed by whole-mount immunohistochemistry. Pediatr Pathol Lab Med 18:57-70.
154. 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.
155. Young HM, Bergner AJ, Müller T. 2003. Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1-11.
156. Young HM, Ciampoli D, Hsuan J, Canty AJ. 1999. Expression of Ret-, p75(NTR)-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut. Dev Dyn 216:137-152.
157. Young HM, Newgreen D. 2001. Enteric neural crest-derived cells: origin, identification, migration, and differentiation. Anat Rec 262:1-15.
158. Zhuang Z, Yang B, Theus MH, Sick JT, Bethea JR, Sick TJ, Liebl DJ. 2010. EphrinBs regulate d-serine synthesis and release in astrocytes. J Neurosci 30:16015-16024.