Agonist-Evoked Ca2+ Signaling in Enteric Glia Drives Neural Programs That Regulate Intestinal Motility in Mice

Cellular and Molecular Gastroenterology and Hepatology

Volumn 1, Issue 6, 2015, Pages 631-645

  McClain, Jonathon L ^a   Fried, David E ^a   Gulbransen, Brian D ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Autonomic; Chemogenetic; Enteric nervous system; Gut; Intestine

Indexed keywords

CLOZAPINE N OXIDE; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; COLON MOTILITY; CONSTIPATION; CONTROLLED STUDY; ENTERIC GLIA; EX VIVO STUDY; GLIA; GLIA CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTESTINE MOTILITY; MOUSE; MUSCLE TONE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VALIDATION STUDY;

EID: 84944449724     PISSN: None     EISSN: 2352345X     Source Type: Journal    
DOI: 10.1016/j.jcmgh.2015.08.004     Document Type: Article

References (42)

1. Wood J.D., Alpers D.H., Andrews P.L. Fundamentals of neurogastroenterology. Gut 1999, 45(Suppl 2):II6-II16.
2. Furness J.B. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 2012, 9:294.
3. Keating D.J., Spencer N.J. Release of 5-hydroxytryptamine from the mucosa is not required for the generation or propagation of colonic migrating motor complexes. Gastroenterology 2010, 138:659-670. 670.e1-2.
4. Kurahashi M., Mutafova-Yambolieva V., Koh S.D., et al. Platelet-derived growth factor receptor-α-positive cells and not smooth muscle cells mediate purinergic hyperpolarization in murine colonic muscles. Am J Physiol Cell Physiol 2014, 307:C561-C570.
5. Neunlist M., Rolli-Derkinderen M., Latorre R., et al. Enteric glial cells: recent developments and future directions. Gastroenterology 2014, 147:1230-1237.
6. Gulbransen B.D., Sharkey K.A. Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 2009, 136:1349-1358.
7. Gomes P., Chevalier J., Boesmans W., et al. ATP-dependent paracrine communication between enteric neurons and glia in a primary cell culture derived from embryonic mice. Neurogastroenterol Motil 2009, 21. 870-e62.
8. Kimball B.C., Mulholland M.W. Enteric glia exhibit P2U receptors that increase cytosolic calcium by a phospholipase C-dependent mechanism. J Neurochem 1996, 66:604-612.
9. 2+ transients in myenteric glial cells during the colonic migrating motor complex in the isolated murine large intestine. J Physiol 2012, 590:335-350.
10. Boesmans W., Martens M.A., Weltens N., et al. Imaging neuron-glia interactions in the enteric nervous system. Front Cell Neurosci 2013, 7:183.
11. Boesmans W., Cirillo C., van den Abbeel V., et al. Neurotransmitters involved in fast excitatory neurotransmission directly activate enteric glial cells. Neurogastroenterol Motil 2013, 25:e151-e160.
12. Gulbransen B.D. Enteric Glia 2014, 1-70. Morgan & Claypool Life Sciences, San Rafael, CA.
13. Gulbransen B.D., Bains J.S., Sharkey K.A. Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J Neurosci 2010, 30:6801-6809.
14. Aube A.-C., Cabarrocas J., Bauer J., et al. Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 2006, 55:630-637.
15. Abdo H.H., Derkinderen P., Gomes P., et al. Enteric glial cells protect neurons from oxidative stress in part via reduced glutathione. FASEB J 2010, 24:1082-1094.
16. 1-prostaglandin J2 is involved in neuroprotection by enteric glial cells against oxidative stress. J Physiol 2012, 590:2739-2750.
17. Nasser Y., Fernandez E., Keenan C.M., 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, 291:912-927.
18. 2+ responses in enteric glia are mediated by connexin-43 hemichannels and modulate colonic transit in mice. Gastroenterology 2014, 146:497-507.e1.
19. 2+ signalling: an unexpected complexity. Nat Rev Neurosci 2014, 15:327-335.
20. Sternson S.M., Roth B.L. Chemogenetic tools to interrogate brain functions. Neuroscience 2014, 37:387-407.
21. Fenno L., Yizhar O., Deisseroth K. The development and application of optogenetics. Annu Rev Neurosci 2011, 34:389-412.
22. Armbruster B.N., Li X., Pausch M.H., et al. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci USA 2007, 104:5163-5168.
23. Agulhon C., Boyt K.M., Xie A.X., et al. Modulation of the autonomic nervous system and behaviour by acute glial cell Gq protein-coupled receptor activation in vivo. J Physiol 2013, 591:5599-5609.
24. Lin W., Kemper A., McCarthy K.D., et al. Interferon-gamma induced medulloblastoma in the developing cerebellum. J Neurosci 2004, 24:10074-10083.
25. Gulbransen B.D., Bashashati M.M., Hirota S.A.S., et al. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med 2012, 18:600-604.
26. 2+ imaging of the enteric nervous system. J Vis Exp 2015, e52506-e52506.
27. Devries M.P., Vessalo M., Galligan J.J. Deletion of P2X2 and P2X3 receptor subunits does not alter motility of the mouse colon. Front Neurosci 2010, 4:22.
28. Grubišić V., Kennedy A.J., Sweatt J.D., et al. Pitt-Hopkins mouse model has altered particular gastrointestinal transits in vivo. Autism Res 2015, Published online. http://dx.doi.org/10.1002/aur.1467.
29. Alexander G.M., Rogan S.C., Abbas A.I., et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 2009, 63:27-39.
30. Heredia D.J., Dickson E.J., Bayguinov P.O., et al. Colonic elongation inhibits pellet propulsion and migrating motor complexes in the murine large bowel. J Physiol 2010, 588:2919-2934.
31. Heredia D.J., Dickson E.J., Bayguinov P.O., et al. Localized release of serotonin (5-hydroxytryptamine) by a fecal pellet regulates migrating motor complexes in murine colon. Gastroenterology 2009, 136:1328-1338.
32. Dogiel A.S. Über den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugetiere [article in German]. Arch Anat Physiol Leipz 1899, 5:130-158.
33. Hanani M., Francke M., Hartig W., et al. Patch-clamp study of neurons and glial cells in isolated myenteric ganglia. Am J Physiol Gastrointest Liver Physiol 2000, 278:G644-G651.
34. Cao X., Li L.-P., Wang Q., et al. Astrocyte-derived ATP modulates depressive-like behaviors. Nat Med 2013, 19:773-777.
35. +. Sci Signal 2012, 5:ra26.
36. Zhang W., Segura B.J., Lin T.R., et al. Intercellular calcium waves in cultured enteric glia from neonatal guinea pig. Glia 2003, 42:252-262.
37. Costagliola A., Van Nassauw L., Snyders D., et al. Voltage-gated delayed rectifier Kv1-subunits may serve as distinctive markers for enteroglial cells with different phenotypes in the murine ileum. Neurosci Lett 2009, 461:80-84.
38. Boesmans W., Lasrado R., Vanden Berghe P., et al. Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia 2015, 63:229-241.
39. Bush T.G., Savidge T.C., Freeman T.C., et al. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 1998, 93. 13-13.
40. Grundy D., Brookes S. Neural Control of Gastrointestinal Function 2011, 1-134. Morgan & Claypool Life Sciences, San Rafael, CA.
41. MacEachern S.J., Patel B.A., Keenan C.M., et al. Inhibiting inducible nitric oxide synthase in enteric glia restores electrogenic ion transport in mice with colitis. Gastroenterology 2015, 149:445-455.e3.
42. Bassotti G., Villanacci V., Maurer C.A., et al. The role of glial cells and apoptosis of enteric neurones in the neuropathology of intractable slow transit constipation. Gut 2006, 55:41-46.