Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system

GLIA

Volumn 63, Issue 2, 2015, Pages 229-241

  Boesmans, Werend ^a   Lasrado, Reena ^b   Vanden Berghe, Pieter ^a   Pachnis, Vassilis ^b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Ca2+ imaging; Enteric glia; Enteric nervous system; Neural crest

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN S100B; TRANSCRIPTION FACTOR SOX10; ADENOSINE; BETA3 TUBULIN, MOUSE; CALCIUM; MLF1 PROTEIN, MOUSE; PHOTOPROTEIN; PROTEIN; SOX10 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX; TUBULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL HETEROGENEITY; DIGESTIVE FUNCTION; EMBRYO; GASTROINTESTINAL DISEASE; GASTROINTESTINAL TRACT; GENE CONTROL; GLIA; GLIA CELL; HUMAN; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTESTINE INNERVATION; MAMMAL; MOLECULAR DYNAMICS; MOUSE; MYENTERIC PLEXUS; NONHUMAN; PHENOTYPE; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; ANALYSIS OF VARIANCE; ANIMAL; CLASSIFICATION; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; THREE DIMENSIONAL IMAGING; TRANSGENIC MOUSE;

ADENOSINE; ANALYSIS OF VARIANCE; ANIMALS; CALCIUM; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; IMAGING, THREE-DIMENSIONAL; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MYENTERIC PLEXUS; NEUROGLIA; PROTEINS; S100 CALCIUM BINDING PROTEIN BETA SUBUNIT; SOXE TRANSCRIPTION FACTORS; TUBULIN;

EID: 84921433199     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22746     Document Type: Article

References (55)

1. Allaman I, Belanger M, Magistretti PJ. 2011. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34:76-87.
2. 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.
3. Barres BA. 2008. The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60:430-440.
4. Boesmans W, Cirillo C, Van den Abbeel V, Van den Haute C, Depoortere I, Tack J, Vanden Berghe P. 2013a. Neurotransmitters involved in fast excitatory neurotransmission directly activate enteric glial cells. Neurogastroenterol Motil 25:e151--160.
5. Boesmans W, Martens MA, Weltens N, Hao MM, Tack J, Cirillo C, Vanden Berghe P. 2013b. Imaging neuron-glia interactions in the enteric nervous system. Front Cell Neurosci 7:183.
6. Boesmans W, Rocha NP, Reis HJ, Holt M, Vanden Berghe P. 2014. The astrocyte marker Aldh1L1 does not reliably label enteric glial cells. Neurosci Lett 566:102-105.
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. Broadhead MJ, Bayguinov PO, Okamoto T, Heredia DJ, Smith TK. 2012. Ca2+ transients in myenteric glial cells during the colonic migrating motor complex in the isolated murine large intestine. J Physiol 590(Pt 2):335-350.
9. 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.
10. 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 USA 98:13306-13311.
11. Costagliola A, Van Nassauw L, Snyders D, Adriaensen D, Timmermans JP. 2009. Voltage-gated delayed rectifier K(v)1-subunits may serve as distinctive markers for enteroglial cells with different phenotypes in the murine ileum. Neurosci Lett 461:80-84.
12. 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.
13. Ferri GL, 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.
14. Furness JB. 2000. Types of neurons in the enteric nervous system. J Auton Nerv Syst 81(1-3):87-96.
15. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM. 2006. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26:8609-8621.
16. Gershon MD, Rothman TP. 1991. Enteric glia. Glia 4:195-204.
17. Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N. 2010. Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat Rev Neurosci 11:87-99.
18. Gomes P, Chevalier J, Boesmans W, Roosen L, van den Abbeel V, Neunlist M, Tack J, Vanden Berghe P. 2009. ATP-dependent paracrine communication between enteric neurons and glia in a primary cell culture derived from embryonic mice. Neurogastroenterol Motil 21:870-e62.
19. Gulbransen BD, Sharkey KA. 2009. Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136:1349-1358.
20. Gulbransen BD, Sharkey KA. 2012. Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 9:625-632.
21. 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.
22. 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.
23. 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.
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. Herbarth B, Pingault V, Bondurand N, Kuhlbrodt K, Hermans-Borgmeyer I, Puliti A, Lemort N, Goossens M, Wegner M. 1998. Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proc Natl Acad Sci USA 95:5161-5165.
26. Hoff S, Zeller F, von Weyhern CWH, Wegner M, Schemann M, Michel K, Ruhl A. 2008. Quantitative assessment of glial cells in the human and guinea rig enteric nervous system with an anti-sox8/9/10 antibody. J Comp Neurol 509:356-371.
27. Jessen KR. 2004. Glial cells. Int J Biochem Cell Biol 36:1861-1867.
28. Jessen KR, Mirsky R. 1980. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 286:736-737.
29. Joseph NM, He S, Quintana E, Kim YG, Nunez 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.
30. Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Vanden Berghe P, Pachnis V. 2011. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest 121:3412-3424.
31. Lee JC, Mayer-Proschel M, Rao MS. 2000. Gliogenesis in the central nervous system. Glia 30:105-121.
32. Lemke G. 2001. Glial control of neuronal development. Annu Rev Neurosci 24:87-105.
33. MacEachern SJ, Patel BA, McKay DM, Sharkey KA. 2011. Nitric oxide regulation of colonic epithelial ion transport: a novel role for enteric glia in the myenteric plexus. J Physiol 589(Pt 13):3333-3348.
34. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP, Koentges G. 2005. Neural crest origins of the neck and shoulder. Nature 436:347-355.
35. Nasser Y, Fernandez E, Keenan CM, Ho W, Oland LD, Tibbles LA, Schemann M, MacNaughton WK, Ruhl A, Sharkey KA. 2006a. Role of enteric glia in intestinal physiology: effects of the gliotoxin fluorocitrate on motor and secretory function. Am J Physiol Gastrointest Liver Physiol 291:G912-927.
36. Nasser Y, Ho W, Sharkey KA. 2006b. Distribution of adrenergic receptors in the enteric nervous system of the guinea pig, mouse, and rat. J Comp Neurol 495:529-553.
37. Nasser Y, Keenan CM, Ma AC, McCafferty DM, Sharkey KA. 2007. Expression of a functional metabotropic glutamate receptor 5 on enteric glia is altered in states of inflammation. Glia 55:859-872.
38. 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.
39. Paratore C, Eichenberger C, Suter U, Sommer L. 2002. Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum Mol Genet 11:3075-3085.
40. Perea G, Navarrete M, Araque A. 2009. Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32:421-431.
41. Pusch C, Hustert E, Pfeifer D, Sudbeck P, Kist R, Roe B, Wang Z, Balling R, Blin N, Scherer G. 1998. The SOX10/Sox10 gene from human and mouse: sequence, expression, and transactivation by the encoded HMG domain transcription factor. Hum Genet 103:115-123.
42. Ruhl A, Nasser Y, Sharkey KA. 2004. Enteric glia. Neurogastroenterol Motil 16(Suppl 1):44-49.
43. Sasselli V, Pachnis V, Burns AJ. 2012. The enteric nervous system. Dev Biol 366:64-73.
44. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R, Sofroniew MV. 2007. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 132:1344-1358.
45. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
46. Sofroniew MV, Vinters HV. 2010. Astrocytes: biology and pathology. Acta Neuropathol 119:7-35.
47. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
48. Stenkamp-Strahm C, Patterson S, Boren J, Gericke M, Balemba O. 2013. High-fat diet and age-dependent effects on enteric glial cell populations of mouse small intestine. Auton Neurosci 177:199-210.
49. Thacker M, Rivera LR, Cho HJ, Furness JB. 2011. The relationship between glial distortion and neuronal changes following intestinal ischemia and reperfusion. Neurogastroenterol Motil 23:e500-e509.
50. 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.
51. Vanden Berghe P, Tack J, Boesmans W. 2008. Highlighting synaptic communication in the enteric nervous system. Gastroenterology 135:20-23.
52. Vanderwinden JM, Timmermans JP, Schiffmann SN. 2003. Glial cells, but not interstitial cells, express P2X7, an ionotropic purinergic receptor, in rat gastrointestinal musculature. Cell Tissue Res 312:149-154.
53. 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.
54. Young HM, Bergner AJ, Muller T. 2003. Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1-11.
55. Zong H, Espinosa JS, Su HH, Muzumdar MD, Luo L. 2005. Mosaic analysis with double markers in mice. Cell 121:479-492.