Activation of myenteric glia during acute inflammation in vitro and in vivo

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Rosenbaum, Corinna ^a   Schick, Martin Alexander ^b   Wollborn, Jakob ^b,c   Heider, Andreas ^d   Scholz, Claus Jürgen ^a   Cecil, Alexander ^b   Niesler, Beate ^e   Hirrlinger, Johannes ^d,f   Walles, Heike ^a,g   Metzger, Marco ^a,g  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF LEIPZIG   (Germany)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^g FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; TRANSCRIPTOME; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENTERIC GLIAL CELL; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GFAP GENE; GLIA CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; RNA ANALYSIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; TRANSCRIPTOMICS; ACUTE DISEASE; ANIMAL; DRUG EFFECTS; GLIA; HUMAN; INFLAMMATION; METABOLISM; MOUSE; MYENTERIC PLEXUS; PATHOLOGY; SEPSIS;

ACUTE DISEASE; ANIMALS; GENE EXPRESSION PROFILING; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MICE; MYENTERIC PLEXUS; NEUROGLIA; RATS; SEPSIS;

EID: 84962587950     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0151335     Document Type: Article

References (63)

1. Neunlist M, Aubert P, Bonnaud S, van Landeghem L, Coron E, Wedel T et al. (2007) Enteric glia inhibit intestinal epithelial cell proliferation partly through a TGF-beta1-dependent pathway. Am. J. Physiol. Gastrointest. Liver Physiol. 292(1):G231-41. PMID: 16423922
2. Bohórquez DV, Samsa LA, Roholt A, Medicetty S, Chandra R, Liddle RA et al. (2014) An Enteroendocrine Cell-Enteric Glia Connection Revealed by 3D Electron Microscopy. PLoS ONE 9(2):e89881. doi: 10.1371/journal.pone.0089881 PMID: 24587096
3. 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(1):153-160. PMID: 7954696
4. Rühl A (2005) Glial cells in the gut. Neurogastroenterology & Motility 17(6):777-790.
5. Boesmans W, Lasrado R, Vanden Berghe P, Pachnis V (2015) Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia 63(2):229.241. doi: 10.1002/glia.22746 PMID: 25161129
6. Gabella G (1981) Ultrastructure of the nerve plexuses of the mammalian intestine. The enteric glial cells. Neuroscience 6(3):425.436. PMID: 7219723
7. Jessen KR, Mirsky R (1983) Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J. Neurosci. 3(11):2206.2218. PMID: 6138397
8. Ferri G, 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(5865):409-410. PMID: 7043279
9. Dong Y, Benveniste EN (2001) Immune function of astrocytes. Glia 36(2):180-190. PMID: 11596126
10. Geboes K, Rutgeerts P, Ectors N, Mebis J, Penninckx F, Vantrappen G et al. (1992) Major histocompatibility class II expression on the small intestinal nervous system in Crohn's disease. Gastroenterology 103(2):439-447. PMID: 1378803
11. Cirillo C, Sarnelli G, Turco F, Mango A, Grosso M, Aprea G et al. (2011) Proinflammatory stimuli activates human-derived enteroglial cells and induces autocrine nitric oxide production. Neurogastroenterol. Motil. 23(9):e372-82. doi: 10.1111/j.1365-2982.2011.01748.x PMID: 21762414
12. Murakami M, Ohta T, Ito S (2009) Lipopolysaccharides enhance the action of bradykinin in enteric neurons via secretion of interleukin-1b from enteric glial cells. J. Neurosci. Res. 87(9):2095-2104. doi: 10. 1002/jnr.22036 PMID: 19235895
13. Ruhl A, Franzke S, Collins SM, Stremmel W (2001) Interleukin-6 expression and regulation in rat enteric glial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 280(6):G1163.71. PMID: 11352809
14. Cirillo C, Sarnelli G, Esposito G, Grosso M, petruzzelli r, izzo p et al. (2009) Increased mucosal nitric oxide production in ulcerative colitis is mediated in part by the enteroglial-derived S100B protein. Neurogastroenterology & Motility 21(11):1209.e112.
15. Parpura V, Verkhratski. AN (2014) Pathological potential of neuroglia. Possible new targets for medical intervention. New York: Springer. 1 online resource p.
16. Joseph NM, He S, Quintana E, Kim Y, Nunez G, Morrison SJ (2011) Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J. Clin. Invest 121(9):3398.3411. doi: 10.1172/JCI58186 PMID: 21865643
17. Cornet A, Savidge TC, Cabarrocas J, Deng W, Colombel J, Lassmann H et al. (2001) Enterocolitis induced by autoimmune targeting of enteric glial cells: A possible mechanism in Crohn's disease. Proceedings of the National Academy of Sciences 98(23):13306.13311.
18. von Boyen G, Schulte N, Pfluger C, Spaniol U, Hartmann C, Steinkamp M (2011) Distribution of enteric glia and GDNF during gut inflammation. BMC Gastroenterol 11:3. doi: 10.1186/1471-230X-11-3 PMID: 21235736
19. von Boyen GBT, Steinkamp M, Reinshagen M, Schafer K, Adler G, Kirsch J (2004) Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 53(2):222.228. PMID: 14724154
20. Liu YA, Chung YC, Pan ST, Shen MY, Hou YC, Peng SJ et al. (2013) 3-D imaging, illustration, and quantitation of enteric glial network in transparent human colon mucosa. Neurogastroenterol. Motil. 25(5):e324.38. doi: 10.1111/nmo.12115 PMID: 23495930
21. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A et al. (2007) Enteric Glia Regulate Intestinal Barrier Function and Inflammation Via Release of S-Nitrosoglutathione. Gastroenterology 132(4):1344.1358. PMID: 17408650
22. van Landeghem L, Chevalier J, Mahe MM, Wedel T, Urvil P, Derkinderen P et al. (2011) Enteric glia promote intestinal mucosal healing via activation of focal adhesion kinase and release of proEGF. AJP: Gastrointestinal and Liver Physiology 300(6):G976.
23. Kabouridis PS, Lasrado R, McCallum S, Chng SH, Snippert HJ, Clevers H et al. (2015) Microbiota Controls the Homeostasis of Glial Cells in the Gut Lamina Propria. Neuron.
24. Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM et al. (2013) Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2012. Critical care medicine 41(2):580.637. doi: 10.1097/CCM.0b013e31827e83af PMID: 23353941
25. Mittal R, Coopersmith CM (2014) Redefining the gut as the motor of critical illness. Trends in molecular medicine 20(4):214.223. doi: 10.1016/j.molmed.2013.08.004 PMID: 24055446
26. Stoffels B, Hupa KJ, Snoek SA, van Bree S, Stein K, Schwandt T et al. (2014) Postoperative ileus involves interleukin-1 receptor signaling in enteric glia. Gastroenterology 146(1):176.87.e1. doi: 10. 1053/j.gastro.2013.09.030 PMID: 24067878
27. Schick MA, Wunder C, Wollborn J, Roewer N, Waschke J, Germer C et al. (2012) Phosphodiesterase-4 inhibition as a therapeutic approach to treat capillary leakage in systemic inflammation. The Journal of Physiology 590(11):2693-2708. doi: 10.1113/jphysiol.2012.232116 PMID: 22495586
28. Wollborn J, Wunder C, Stix J, Neuhaus W, Bruno RR, Baar W et al. (2015) Phosphodiesterase-4 inhibition with rolipram attenuates hepatocellular injury in hyperinflammation in vivo and in vitro without influencing inflammation and HO-1 expression. Journal of pharmacology & pharmacotherapeutics 6(1):13-23.
29. Hoff S, Zeller F, von Weyhern Claus Werner Hann, Wegner M, Schemann M, Michel K et al. (2008) Quantitative assessment of glial cells in the human and guinea pig enteric nervous system with an anti-Sox8/9/10 antibody. The Journal of comparative neurology 509(4):356-371. doi: 10.1002/cne.21769 PMID: 18512230
30. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55(4):611-622. doi: 10.1373/clinchem.2008.112797 PMID: 19246619
31. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. doi: 10. 1186/1471-2105-13-134 PMID: 22708584
32. Vandesompele J, de Preter K, Pattyn F, Poppe B, van Roy N, de Paepe A et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3(7):RESEARCH0034.
33. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK et al. (2001) GFAP promotercontrolled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33(1):72-86. PMID: 11169793
34. Hegewald C, Alt R, Hetz S, Cross M, Acikgoez A, Till H et al. (2011) Reduced oxygen stress promotes propagation of murine postnatal enteric neural progenitors in vitro. Neurogastroenterology & Motility 23(10):e412.
35. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. Available: http://www. R-project.org/.
36. Bai X, Saab AS, Huang W, Hoberg IK, Kirchhoff F, Scheller A (2013) Genetic background affects human glial fibrillary acidic protein promoter activity. PLoS ONE 8(6):e66873. doi: 10.1371/journal. pone.0066873 PMID: 23826164
37. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57. doi: 10.1038/nprot.2008.211 PMID: 19131956
38. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25(1):25-29. PMID: 10802651
39. (2015) Gene Ontology Consortium: going forward. Nucleic Acids Res. 43(Database issue):D1049-56. doi: 10.1093/nar/gku1179 PMID: 25428369
40. Bernhardt J, Funke S, Hecker M, Siebourg J Visualizing Gene Expression Data via Voronoi Treemaps. 2009 Sixth International Symposium on Voronoi Diagrams (ISVD). pp. 233-241.
41. Turner R (2015) deldir. Delaunay Triangulation and Dirichlet (Voronoi) Tessellation. Available: https://cran. r-project.org/web/packages/deldir/.
42. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30(1):207-210. PMID: 11752295
43. Heider A, Alt R (2013) virtualArray: a R/bioconductor package to merge raw data from different microarray platforms. BMC Bioinformatics 14:75. doi: 10.1186/1471-2105-14-75 PMID: 23452776
44. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA et al. (2006) TM4 microarray software suite. Methods in enzymology 411:134-193. PMID: 16939790
45. Han MV, Zmasek CM (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10:356. doi: 10.1186/1471-2105-10-356 PMID: 19860910
46. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America 95(25):14863-14868. PMID: 9843981
47. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL et al. (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol. 26(3):317-325. doi: 10.1038/nbt1385 PMID: 18278033
48. Flemming S, Schlegel N, Wunder C, Meir M, Baar W, Wollborn J et al. (2014) Phosphodiesterase 4 inhibition dose dependently stabilizes microvascular barrier functions and microcirculation in a rodent model of polymicrobial sepsis. Shock (Augusta, Ga.) 41(6):537-545.
49. Schick MA, Isbary TJ, Schlegel N, Brugger J, Waschke J, Muellenbach R et al. (2010) The impact of crystalloid and colloid infusion on the kidney in rodent sepsis. Intensive care medicine 36(3):541-548. doi: 10.1007/s00134-009-1704-0 PMID: 19890625
50. The F, Cailotto C, van der Vliet J, de Jonge WJ, Bennink RJ, Buijs RM et al. (2011) Central activation of the cholinergic anti-inflammatory pathway reduces surgical inflammation in experimental post-operative ileus. British journal of pharmacology 163(5):1007-1016. doi: 10.1111/j.1476-5381.2011.01296.x PMID: 21371006
51. de Winter BY (2010) Interplay between inflammation, immune system and neuronal pathways: Effect on gastrointestinal motility. WJG 16(44):5523. PMID: 21105185
52. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L et al. (1998) Fulminant Jejuno-Ileitis following Ablation of Enteric Glia in Adult Transgenic Mice. Cell 93(2):189-201. PMID: 9568712
53. Cirillo C, Sarnelli G, Esposito G, Turco F, Steardo L, Cuomo R (2011) S100B protein in the gut: the evidence for enteroglial-sustained intestinal inflammation. World J. Gastroenterol 17(10):1261-1266. doi: 10.3748/wjg.v17.i10.1261 PMID: 21455324
54. Esposito G, Cirillo C, Sarnelli G, de Filippis D, D'Armiento FP, Rocco A et al. (2007) Enteric glial-derived S100B protein stimulates nitric oxide production in celiac disease. Gastroenterology 133(3):918-925. PMID: 17678654
55. Gulbransen BD (2014) Enteric glia. San Rafael, California (1537 Fourth Street, San Rafael, CA 94901 USA): Morgan & Claypool. 1 online resource (1 p.
56. Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Vanden Berghe P et al. (2011) Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J. Clin. Invest 121(9):3412-3424. doi: 10.1172/JCI58200 PMID: 21865647
57. Belkind-Gerson J, Carreon-Rodriguez A, Benedict LA, Steiger C, Pieretti A, Nagy N et al. (2012) Nestinexpressing cells in the gut give rise to enteric neurons and glial cells. Neurogastroenterology & Motility: no.
58. Cuadrado E, Jansen MH, Anink J, de Filippis L, Vescovi AL, Watts C et al. (2013) Chronic exposure of astrocytes to interferon-a reveals molecular changes related to Aicardi-Goutieres syndrome. Brain: a journal of neurology 136(Pt 1):245-258.
59. Bhowmick S, Duseja R, Das S, Appaiahgiri MB, Vrati S, Basu A (2007) Induction of IP-10(CXCL10) in astrocytes following Japanese encephalitis. Neuroscience Letters 414(1):45-50. PMID: 17287085
60. Lee S, Park J, Lee W, Kim H, Park H, Mori K et al. (2009) Lipocalin-2 is an autocrine mediator of reactive astrocytosis. J. Neurosci. 29(1):234-249. doi: 10.1523/JNEUROSCI.5273-08.2009 PMID: 19129400
61. Johnstone M, Gearing AJ, Miller KM (1999) A central role for astrocytes in the inflammatory response to b-amyloid; chemokines, cytokines and reactive oxygen species are produced. Journal of Neuroimmunology 93(1-2):182-193. PMID: 10378882
62. Metzger M, Bareiss PM, Danker T, Wagner S, Hennenlotter J, Guenther E et al. (2009) Expansion and Differentiation of Neural Progenitors Derived From the Human Adult Enteric Nervous System. Gastroenterology 137(6):2063-2073.e4. doi: 10.1053/j.gastro.2009.06.038 PMID: 19549531
63. Rao M, Nelms BD, Dong L, Salinas-Rios V, Rutlin M, Gershon MD et al. (2015) Enteric glia express proteolipid protein 1 and are a transcriptionally unique population of glia in the mammalian nervous system. Glia.