Emerging roles for enteric glia in gastrointestinal disorders

Journal of Clinical Investigation

Volumn 125, Issue 3, 2015, Pages 918-925

  Sharkey, Keith A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DISEASE; CELL FUNCTION; DIGESTIVE SYSTEM INFLAMMATION; DISEASE ASSOCIATION; ENTERIC GLIA; GASTROINTESTINAL DISEASE; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL MOTILITY DISORDER; GASTROINTESTINAL MUCOSA; GASTROINTESTINAL TRACT; GLIA; HUMAN; INTESTINE INNERVATION; NEUROLOGIC DISEASE; NEUROTRANSMISSION; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; REVIEW; ANIMAL; INTESTINE MUCOSA; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN DISEASES; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL DISEASES; GASTROINTESTINAL MOTILITY; HUMANS; INTESTINAL MUCOSA; NEUROGLIA;

EID: 84924061427     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI76303     Document Type: Review

References (91)

1. Kurahashi M, et al. A functional role for the 'fibroblast-like cells' in gastrointestinal smooth muscles. J Physiol. 2011;589(pt 3):697-710.
2. Muller PA, et al. Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell. 2014;158(2):300-313.
3. Furness JB. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol. 2012;9(5):286-294.
4. Gulbransen BD, Sharkey KA. Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol. 2012;9(11):625-632.
5. Gershon MD, Rothman TP. Enteric glia. Glia. 1991;4(2):195-204.
6. Ruhl A, Nasser Y, Sharkey KA. Enteric glia. Neurogastroenterol Motil. 2004;16(suppl 1):44-49.
7. Neunlist M, et al. Enteric glial cells: recent developments and future directions. Gastroenterology. 2014;147(6):1230-1237.
8. Neunlist M, et al. The digestive neuronal-glial-epithelial unit: a new actor in gut health and disease. Nat Rev Gastroenterol Hepatol. 2013;10(2):90-100.
9. Boesmans W, Lasrado R, Vanden Berghe P, Pachnis V. Heterogeneity phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia. 2014;63(2):229-241.
10. Gabella G. Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience. 1981;6(3):425-436.
11. Gabella G. Fine structure of the myenteric plexus in the guinea-pig ileum. J Anat. 1972; 111(pt 1):69-97.
12. Jessen KR, Mirsky R. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature. 1980;286(5774):736-737.
13. Hanani M, Zamir O, Baluk P. Glial cells in the guinea pig myenteric plexus are dye coupled. Brain Res. 1989;497(2):245-249.
14. Geboes K, et al. Major histocompatibility class II expression on the small intestinal nervous system in Crohn's disease. Gastroenterology. 1992;103(2):439-447.
15. Koretz K,Momburg F,Otto HF,Moller P Sequential induction of MHC antigens on autochthonous cells of ileum affected by Crohn's disease Am J Pathol. 1987, 129, 3, 493-502.
16. Bush TG, et al. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell. 1998;93(2):189-201.
17. Cornet A, et al. Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease? Proc Natl Acad Sci U S A. 2001;98(23):13306-13311.
18. Aikawa H, Suzuki K. Lesions in the skin, intestine, and central nervous system induced by an antimetabolite of niacin. Am J Pathol. 1986;122(2):335-342.
19. Aikawa H, Suzuki K. Enteric gliopathy in niacindeficiency induced by CNS glio-toxin. Brain Res. 1985;334(2):354-356.
20. Aubé AC, et al. Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut. 2006;55(5):630-637.
21. Nasser Y, et al. Role of enteric glia in intestinal physiology: effects of the gliotoxin fluorocitrate on motor and secretory function. Am J Physiol Gastrointest Liver Physiol. 2006;291(5):G912-G927 .
22. Bassotti G, et al. Enteric neuropathology of the terminal ileum in patients with intractable slow-transit constipation. Hum Pathol. 2006;37(10):1252-1258.
23. Bassotti G, Villanacci V, Antonelli E, Morelli A, Salerni B. Enteric glial cells: new players in gastrointestinal motility? Lab Invest. 2007;87(7):628-632.
24. Bassotti G, et al. Enteric glial cells and their role in gastrointestinal motor abnormalities: introducing the neuro-gliopathies. World J Gastroenterol. 2007;13(30):4035-4041.
25. Gulbransen BD, Bains JS, Sharkey KA. Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J Neurosci. 2010;30(19):6801-6809.
26. Gulbransen BD, et al. Activati on of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med. 2012;18(4):600-604.
27. Gulbransen BD, Sharkey KA. Purinergic neuronto-glia signaling in the enteric nervous system. Gastroenterology. 2009;136(4):1349-1358.
28. McClain JL, et al. Ca2+ responses in enteric glia are mediated by connexin-43 hemichannels and modulate colonic transit in mice. Gastroenterology. 2014;146(2):497-507.
29. Broadhead MJ, Bayguinov PO, Okamoto T, Heredia DJ, Smith TK. Ca2+ transients in myenteric glial cells during the colonic migrating motor complex in the isola ted murine large intestine. J Physiol. 2012;590(pt 2):335-350.
30. Gulbransen BD. Enteric Glia. San Rafael, California, USA: Morgan and Claypool; 2014.
31. Boesmans W , et al. Imaging neuron-glia interactions in the enteric nervous system. Front Cell Neurosci. 2013;7:183.
32. Boesmans W, et al. Neurotransmitters involved in fast excitatory neurotransmission directly activate enteric glial cells. Neurogastroenterol Motil. 2013;25(2):e151-e160.
33. Vanden Berghe P, Klingauf J. Spatial organization and dynamic properties of neurotransmitter release sites in the enteric nervous system. Neuroscience. 2007;145(1):88-99.
34. Okamoto T, et al. Extensive projections of myenteric serotonergic neurons suggest they comprise the central processing unit in the col on. Neurogastroenterol Motil. 2014;26(4):556-570.
35. Gautron L, et al. Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen. J Comp Neurol. 2013;521(16):3741-3767.
36. Stoffels B, et al. Postoperative ileus involves interleukin-1 receptor signaling in enteric glia. Gastroenterology. 2014;146(1):176-187e171.
37. Green CL, Ho W, Sharkey KA, McKay DM. Dextran sodium sulfate-induced colitis reveals nicotinic modulation of ion transport via iNOS-derived NO. Am J Physiol Gastrointest Liver Physiol. 2004;287(3):G706-G714.
38. MacEachern SJ, Patel BA, McKay DM, Sharkey KA. Nitric oxide regulation of colonic epithelial ion transport: a novel role for enteric glia in the myenteric plexus. J Physiol. 2011; 589( pt 13):3333-3348.
39. Selgrad M, et al. JC virus infects the enteric glia of patients with chronic idiopathic intestinal pseudo-obstruction. Gut. 2009;58(1):25-32.
40. Abdo H, et al. Enteric glial cells protect neurons from oxidative stress in part via reduced glutathione. FASEB J. 2010;24(4):1082-1094.
41. Fu M, et al. Retinoblastoma protein prevents enteric nervous system defects and intestinal pseudo-obstruction. J Clin Invest. 2013;123(12):5152-5164.
42. Stenkamp-Strahm C, Patterson S, Boren J, Gericke M, Balemba O. High-fat diet and agedepe ndent effects on enteric glial cell populations of mouse small intestine. Auton Neurosci. 2013;177(2):199-210.
43. van Haver ER, et al. Postnatal and diet-dependent increases in enteric glial cells and VIP-containing neurones in preterm pigs. Neurogastroenterol Motil. 2008;20(9):1070-1079.
44. Phillips RJ, Kieffer EJ, Powley TL. Loss of glia and neurons in the myenteric plexus of the aged Fischer 344 rat. Anat Embryol (Berl). 2004;209(1):19-30.
45. Baudry C, et al. Diet-induced obesity has neuroprotective effects in murine gastric enteric nervous system: involvement of leptin and gl ial cell line-derived neurotrophic factor. J Physiol. 2012;590(pt 3):533-544.
46. Schoffen JP, et al. Food restriction enhances oxidative status in aging rats with neuroprotective effects on myenteric n euron populations in the proximal colon. Exp Gerontol. 2014;51:54-64.
47. Voss U, Sand E, Olde B, Ekblad E. Enteric neuropathy can be induced by high fat diet in vivo and palmitic acid exposure in vitro. PLoS One. 2013;8(12):e81413.
48. Liu YA, et al. 3-D imaging, illustration, and quantitation of enteric glial network in transparent human colon mucosa. Neurogastroenterol Motil. 2013;25(5):e324-e338.
49. Badizadegan K, et al. Presence of intramucosal neuroglial cells in normal and aganglionic human colon. Am J Physiol Gastrointest Liver Physiol. 2014;307(10):G1002-G1012.
50. Bohórquez DV, et al. An enteroendocrine cellenteric glia connection revealed by 3D electron microscopy. PLoS One. 2014;9(2):e89881.
51. Raybould HE. Gut chemosensing: interactions between gut endocrine cells and visceral afferents. Auton Neurosci. 2010;153(1-2):41-46.
52. Sternini C, Anselmi L, Rozengurt E. Enteroendocrine cells: a site of 'taste' in gastrointestinal chemosensing. Curr Opin Endocrinol Diabetes Obes. 2008;15(1):73-78.
53. Drucker DJ, Yusta B. Physiology and pharmacology of the enteroendocrine hormone glucagonlike peptide-2. Annu Rev Physiol. 2014; 76:561-583.
54. de Heuvel E, Wallace L, Sharkey KA, Sigalet DL. Glucagon-like peptide 2 induces vasoactive intestinal polypep tide expression in enteric neurons via phophatidylinositol 3-kinase-? signaling. Am J Physiol Endocrinol Metab. 2012;303(8):E994-E1005.
55. Savidge TC, et al. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology. 2007;132(4):1344-1358.
56. Neunlist M, et al. Enteric glia inhibit intestinal epithelial cell proliferation partly through a TGF-?1-dependent pathway. Am J Physiol Gastrointest Liver Physiol. 2007;292(1):G231-G241.
57. Xiao W, et al. GDNF is involved in the barrier-inducing effect of enteric glial cells on intestinal epithelial cells under acute ischemia reperfusion stimulation. Mol Neurobiol. 2014;50(2):274-289.
58. Cheadle GA,Costantini TW,Bansal V,Eliceiri BP,Coimbra R Cholinergic signaling in the gut: a novel mechanism of barrier protection through activation of enteric glia cells Surg Infect (Larchmt). 2014 15 4 387-393.
59. Cheadle GA, et al. Enteric glia cells attenuate cytomix-induced intestinal epithelial barrier breakdown. PLoS One. 2013;8(7):e69042.
60. Costantini TW, et al. Targeting ?-7 nicotinic acetylcholine receptor in the enteric nervous system: a cholinergic agonist prevents gut barrier failure after severe burn injury. Am J Pathol. 2012;181(2):478-486.
61. Turc o F, et al. Enteroglial-derived S100B protein integrates bacteria-induced Toll-like receptor signalling in human enteric glial cells. Gut. 2013;63(1):105-115.
62. Esposito G, et al. Palmitoylet hanolamide improves colon inflammation through an enteric glia/toll like receptor 4-dependent PPAR-? activation. Gut. 2014;63(8):1300-1312.
63. Esposito G, et al. Enteric glial-derived S100B protein stimulates nitric oxide production in celiac disease. Gastroenterology. 2007;133(3):918-925.
64. Cirillo C, et al. Proinflammatory stimuli activates human-derived enteroglial cells and induces autocrine nitric oxide production. Neurogastroenterol Motil. 2011;23(9):e372-e382.
65. Cirillo C, et al. Increased mucosal nitric oxide production in ulcerative colitis is mediated in part by the enteroglial-derived S100B protein. Neurogastroenterol Motil. 2009;21(11):1209-e112.
66. Xiao WD, et al. The protective effect of enteric glial cells on intestinal epithelial barrier function is enhanced by inhibiting inducible nitric oxide synthase activity under lipopolysaccharide stimulation. Mol Cell Neurosci. 2011;46(2 ):527-534.
67. da Silveira AB, et al. Enteroglial cells act as antigen-presenting cells in chagasic megacolon. Hum Pathol. 2011;42(4):522-532.
68. Esposito G, et al. Palmitoylethanolamide improves colon inflammation through an enteric glia/toll like receptor 4-dependent PPAR-? activation. Gut. 2013;63(8):1300-1312.
69. Storr MA, et al. Targeting endocannabinoid de gradation protects against experimental colitis in mice: involvement of CB1 and CB2 receptors. J Mol Med (Berl). 2008;86(8):925-936.
70. Albanese V, et al. Evidence for prion protein expression in enteroglial cells of the myenteric plexus of mouse intestine. Auton Neurosci. 2008;140(1-2):17-23.
71. Lawson VA, et al. The brain to gut pathway: a possible route of prion transmission. Gut. 2010;59(12):1643-1651.
72. Martin GR, et al. Endogenous cellular prion protein regulates contractility of the mouse ileum. Neurogastroenterol Motil. 2012;24(9):e412-e424.
73. Seelig DM, Mason GL, Telling GC, Hoover EA. Chronic wasting disease prion trafficking via the autonomic nervous system. Am J Pathol. 2011;179(3):1319-1328.
74. Ano Y, Sakudo A, Nakayama H, Onodera T. Uptake and dynamics of infectious prion protein in the intestine. Protein Pept Lett. 2009; 16(3):247-255.
75. Clairembault T, Leclair-Visonneau L, Neunlist M, Derkinderen P. Enteric glial cells: new players in Parkinson's disease? [published online ahead of print August 7, 2014]. Mov Disord. doi:10.1002/mds.25979.
76. Clairembault T, et al. Enteric G FAP expression and phosphorylation in Parkinson's disease. J Neurochem. 2014;130(6):805-815.
77. Van Landeghem L, et al. Enteric glia promote intestinal mucosal healing via activation of focal adhesion kinase and release of proEGF. Am J Physiol Gastrointest Liver Physiol. 2011;300(6):G976-G987.
78. Bach-Ngohou K, et al. Enteric glia modulate epithelial cell proliferation and differentiation through 15-deoxy-12,14-prostaglandin J2. J Physiol. 2010;588(pt 14):2533-2544.
79. von Boyen GB,et al Nerve growth factor secretion in cultured enteric glia cells is modulated by proinflammatory cytokines J Neuroendocrinol. 2006 18 11 820-825.
80. Abdo H, et al. The omega-6 fatty acid derivative 15-deoxy-?(1)(2),(1)(4)-prostaglandin J2 is involved in neuroprotection by enteric glial cells against oxidative stress. J Physiol. 2012; 590(pt 11):2739-2750.
81. Nagahama M, Semba R , Tsuzuki M, Aoki E. L-Arginine immunoreactive enteric glial cells in the enteric nervous system of rat ileum. Biol Signals Recept. 2001;10(5):336-340.
82. Aoki E, Semba R, Kashiwamata S . Evidence for the presence of L-Arginine in the glial components of the peripheral nervous system. Brain Res. 1991;559(1):159-162.
83. Jessen KR, Mirsky R. Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci. 1983;3(11):2206-2218.
84. Zhang W, Segura BJ, Lin TR, Hu Y, Mulholland MW. Intercellular calcium waves in cultured enteric glia from neonatal guinea pig. Glia. 2003;42(3):252-262.
85. Gomes P, et al. ATP-dependent paracrine communication between enteric neurons and glia in a primary cell culture derived fro m embryonic mice. Neurogastroenterol Motil. 2009;21(8):870-e62.
86. Joseph NM, et al. Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J Clin Invest. 2011;121(9):3398-3411.
87. Laranjeira C, et al. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest. 2011;121(9):3412-3424.
88. Hirata I, Austin LL, Blackwell WH, Weber JR, Dobbins WO 3rd. Immunoelectron microscopic localization of HLA-DR antigen in control small intestine and colon and in inflammatory bowel disease. Dig Dis Sci. 1986;31(12):1317-1330.
89. Murakami M, Ohta T, Ito S. Lipopolysaccharides enhance the action of bradykinin in enteric neurons via secretion of interleukin-1beta from enteric glial cells. J Neurosci Res. 2009;87(9):2095-2104.
90. Murakami M, Ohta T, Otsuguro KI, Ito S. Involvement of prostaglandin E(2) derived from enteric glial cells in the action of bradykinin in cultured rat myenteric neur ons. Neuroscience. 2007;145(2):642-653.
91. Ruhl A, Franzke S, Collins SM, Stremmel W. Interleukin-6 expression and regulation in rat enteric glial cells. Am J Physiol Gastrointest Liver Physiol. 2001;280(6):G1163-G1171.