S100B protein in the gut: The evidence for enteroglialsustained intestinal inflammation

World Journal of Gastroenterology

Volumn 17, Issue 10, 2011, Pages 1261-1266

  Cirillo, Carla ^a   Sarnelli, Giovanni ^a   Esposito, Giuseppe ^b   Turco, Fabio ^a   Steardo, Luca ^b   Cuomo, Rosario ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Enteric glial cells; Intestinal diseases; Nitric oxide

Indexed keywords

NITRIC OXIDE; PROTEIN S100B;

ARTICLE; ENTERITIS; ENTEROPATHY; GASTROINTESTINAL TRACT; GLIA CELL; HUMAN; INFLAMMATION; INTESTINE INNERVATION; PROTEIN EXPRESSION;

EID: 79955933905     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v17.i10.1261     Document Type: Article

References (66)

1. Schemann M, Neunlist M. The human enteric nervous system. Neurogastroenterol Motil 2004; 16 Suppl 1: 55-59
2. Furness JB. The Enteric Nervous System. Oxford: Blackwell Publishing, 2006
3. Gabella G. Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience 1981; 6: 425-436
4. Lomax AE, Fernández E, Sharkey KA. Plasticity of the enteric nervous system during intestinal inflammation. Neurogastroenterol Motil 2005; 17: 4-15
5. Rühl A. Glial cells in the gut. Neurogastroenterol Motil 2005; 17: 777-790
6. Heizmann CW. The multifunctional S100 protein family. Methods Mol Biol 2002; 172: 69-80
7. Sariola H, Saarma M. Novel functions and signalling pathways for GDNF. J Cell Sci 2003; 116: 3855-3862
8. von Boyen GB, Steinkamp M, Reinshagen M, Schäfer KH, Adler G, Kirsch J. Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 2004; 53: 222-228
9. Haimoto H, Hosoda S, Kato K. Differential distribution of immunoreactive S100-alpha and S100-beta proteins in normal nonnervous human tissues. Lab Invest 1987; 57: 489-498
10. Zimmer DB, Van Eldik LJ. Tissue distribution of rat S100 alpha and S100 beta and S100-binding proteins. Am J Physiol 1987; 252: C285-C289
11. Fanò G, Biocca S, Fulle S, Mariggiò MA, Belia S, Calissano P. The S-100: a protein family in search of a function. Prog Neurobiol 1995; 46: 71-82
12. Van Eldik LJ, Wainwright MS. The Janus face of glialderived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci 2003; 21: 97-108
13. 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. Enteric glial-derived S100B protein stimulates nitric oxide production in celiac disease. Gastroenterology 2007; 133: 918-925
14. Cirillo C, Sarnelli G, Esposito G, Grosso M, Petruzzelli R, Izzo P, Calì G, D'Armiento FP, Rocco A, Nardone G, Iuvone T, Steardo L, Cuomo R. Increased mucosal nitric oxide production in ulcerative colitis is mediated in part by the enteroglialderived S100B protein. Neurogastroenterol Motil 2009; 21: 1209-e112
15. Cirillo C, Sarnelli G, Mango A, Esposito I and Cuomo R. Effect of pro-inflammatory stimuli on cellular activation and nitric oxide production in primary cultures of human enteric glia. Gastroenterology 2009; 136: A4
16. Hoff S, Zeller F, von Weyhern CW, Wegner M, Schemann M, Michel K, Rühl A. Quantitative assessment of glial cells in the human and guinea pig enteric nervous system with an anti-Sox8/9/10 antibody. J Comp Neurol 2008; 509: 356-371
17. Furness JB. Types of neurons in the enteric nervous system. J Auton Nerv Syst 2000; 81: 87-96
18. Gershon MD. The enteric nervous system: a second brain. Hosp Pract (Minneap) 1999; 34: 31-32, 35-38, 41-42 passim
19. Wood JD. Enteric neuroimmunophysiology and pathophys- iology. Gastroenterology 2004; 127: 635-657
20. Grider JR. Regulation of excitatory neural input to longitudinal intestinal muscle by myenteric interneurons. Am J Physiol 1998; 275: G973-G978
21. Timmermans JP, Hens J, Adriaensen D. Outer submucous plexus: an intrinsic nerve network involved in both secretory and motility processes in the intestine of large mammals and humans. Anat Rec 2001; 262: 71-78
22. Elfvin LG, Björklund H, Dahl D, Seiger A. Neurofilamentlike and glial fibrillary acidic protein-like immunoreactivities in rat and guinea-pig sympathetic ganglia in situ and after perturbation. Cell Tissue Res 1987; 250: 79-86
23. Endo Y, Kobayashi S. A scanning electron microscope study on the autonomic groundplexus in the lamina propria mucosae of the guinea-pig small intestine. Arch Histol Jpn 1987; 50: 243-250
24. Mestres P, Diener M, Rummel W. Electron microscopy of the mucosal plexus of the rat colon. Acta Anat (Basel) 1992; 143: 275-282
25. Dogiel AS. Uber den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Saugethiere. Z Naturforsch B 1899; 5: 130-158
26. Ferri GL, Probert L, Cocchia D, Michetti F, Marangos PJ, Polak JM. Evidence for the presence of S-100 protein in the glial component of the human enteric nervous system. Nature 1982; 297: 409-410
27. Laranjeira C, Pachnis V. Enteric nervous system development: Recent progress and future challenges. Auton Neurosci 2009; 151: 61-69
28. Bassotti G, Villanacci V, Antonelli E, Morelli A, Salerni B. Enteric glial cells: new players in gastrointestinal motility? Lab Invest 2007; 87: 628-632
29. Bassotti G, Villanacci V, Fisogni S, Rossi E, Baronio P, Clerici C, Maurer CA, Cathomas G, Antonelli E. Enteric glial cells and their role in gastrointestinal motor abnormalities: introducing the neuro-gliopathies. World J Gastroenterol 2007; 13: 4035-4041
30. Van Landeghem L, Mahé MM, Teusan R, Léger J, Guisle I, Houlgatte R, Neunlist M. Regulation of intestinal epithelial cells transcriptome by enteric glial cells: impact on intestinal epithelial barrier functions. BMC Genomics 2009; 10: 507
31. Aubé AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, Doulay F, Liblau R, Galmiche JP, Neunlist M. Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 2006; 55: 630-637
32. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH, Sofroniew MV. Fulminant jejunoileitis following ablation of enteric glia in adult transgenic mice. Cell 1998; 93: 189-201
33. Cornet A, Savidge TC, Cabarrocas J, Deng WL, Colombel JF, Lassmann H, Desreumaux P, Liblau RS. Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease? Proc Natl Acad Sci USA 2001; 98: 13306-13311
34. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R, Sofroniew MV. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 2007; 132: 1344-1358
35. Neunlist M, Van Landeghem L, Bourreille A, Savidge T. Neuro-glial crosstalk in inflammatory bowel disease. J Intern Med 2008; 263: 577-583
36. Savidge TC, Sofroniew MV, Neunlist M. Starring roles for astroglia in barrier pathologies of gut and brain. Lab Invest 2007; 87: 731-736
37. Cabarrocas J, Savidge TC, Liblau RS. Role of enteric glial cells in inflammatory bowel disease. Glia 2003; 41: 81-93
38. 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: 2095-2104
39. Rühl 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: G1163-G1171
40. 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: 159-162
41. 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: 336-340
42. Eng LF, Ghirnikar RS, Lee YL. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 2000; 25: 1439-1451
43. Jessen KR, Mirsky R. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 1980; 286: 736-737
44. Gonzalez-Martinez T, Perez-Piñera P, Díaz-Esnal B, Vega JA. S-100 proteins in the human peripheral nervous system. Microsc Res Tech 2003; 60: 633-638
45. Iwanaga T, Takahashi Y, Fujita T. Immunohistochemistry of neuron-specific and glia-specific proteins. Arch Histol Cytol 1989; 52 Suppl: 13-24
46. Sugimura K, Haimoto H, Nagura H, Kato K, Takahashi A. Immunohistochemical differential distribution of S-100 alpha and S-100 beta in the peripheral nervous system of the rat. Muscle Nerve 1989; 12: 929-935
47. Zimmer DB, Cornwall EH, Landar A, Song W. The S100 protein family: history, function, and expression. Brain Res Bull 1995; 37: 417-429
48. Baudier J, Glasser N, Gerard D. Ions binding to S100 proteins. I. Calcium- and zinc-binding properties of bovine brain S100 alpha alpha, S100a (alpha beta), and S100B (beta beta) protein: Zn2+ regulates Ca2+ binding on S100B protein. J Biol Chem 1986; 261: 8192-8203
49. Bramanti V, Tomassoni D, Avitabile M, Amenta F, Avola R. Biomarker s of glial cell proliferation and differentiation in culture. Front Biosci (Schol Ed) 2010; 2: 558-570
50. Zimmer DB, Chaplin J, Baldwin A, Rast M. S100-mediated signal transduction in the nervous system and neurological diseases. Cell Mol Biol (Noisy-le-grand) 2005; 51: 201-214
51. Chow SK, Yu D, Macdonald CL, Buibas M, Silva GA. Amyloid β-peptide directly induces spontaneous calcium transients, delayed intercellular calcium waves and gliosis in rat cortical astrocytes. ASN Neuro 2010; 2: e00026
52. Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, White CL 3rd, Araoz C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci USA 1989; 86: 7611-7615
53. Van Eldik LJ, Griffin WS. S100 beta expression in Alzheimer's disease: relation to neuropathology in brain regions. Biochim Biophys Acta 1994; 1223: 398-403
54. Leach ST, Yang Z, Messina I, Song C, Geczy CL, Cunningham AM, Day AS. Serum and mucosal S100 proteins, calprotectin (S100A8/S100A9) and S100A12, are elevated at diagnosis in children with inflammatory bowel disease. Scand J Gastroenterol 2007; 42: 1321-1331
55. Pietzsch J, Hoppmann S. Human S100A12: a novel key player in inflammation? Amino Acids 2009; 36: 381-389
56. Adami C, Bianchi R, Pula G, Donato R. S100B-stimulated NO production by BV-2 microglia is independent of RAGE transducing activity but dependent on RAGE extracellular domain. Biochim Biophys Acta 2004; 1742: 169-177
57. Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr Mol Med 2007; 7: 711-724
58. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF, Slattery T, Beach D, McClary J, Nagashima M, Morser J, Stern D, Schmidt AM. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgran- ulin polypeptides. Cell 1999; 97: 889-901
59. Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 2001; 108: 949-955
60. Adami C, Sorci G, Blasi E, Agneletti AL, Bistoni F, Donato R. S100B expression in and effects on microglia. Glia 2001; 33: 131-142
61. Petrova TV, Hu J, Van Eldik LJ. Modulation of glial activation by astrocyte-derived protein S100B: differential responses of astrocyte and microglial cultures. Brain Res 2000; 853: 74-80
62. Daniels I, Cavill D, Murray IA, Long RG. Elevated expression of iNOS mRNA and protein in coeliac disease. Clin Chim Acta 2005; 356: 134-142
63. Geboes K, Collins S. Structural abnormalities of the nervous system in Crohn's disease and ulcerative colitis. Neurogastroenterol Motil 1998; 10: 189-202
64. Linehan JD, Kolios G, Valatas V, Robertson DA, Westwick J. Effect of corticosteroids on nitric oxide production in inflammatory bowel disease: are leukocytes the site of action? Am J Physiol Gastrointest Liver Physiol 2005; 288: G261-G267
65. Menchén L, Colón AL, Madrigal JL, Beltrán L, Botella S, Lizasoain I, Leza JC, Moro MA, Menchén P, Cos E, Lorenzo P. Activity of inducible and neuronal nitric oxide synthases in colonic mucosa predicts progression of ulcerative colitis. Am J Gastroenterol 2004; 99: 1756-1764
66. Cirillo C, Sarnelli G, Mango A, Esposito I, Grosso M, Cuomo R. Enteric glia stimulates inflammation-induced responses in human intestine and interacts with immune cells via S100B protein. Gastroenterology 2009; 136: A271-A272