Increased mucosal nitric oxide production in ulcerative colitis is mediated in part by the enteroglial-derived S100B protein

Neurogastroenterology and Motility

Volumn 21, Issue 11, 2009, Pages

  Cirillo, C ^a   Sarnelli, G ^a   Esposito, G ^b   Grosso, M ^a   Petruzzelli, R ^a   Izzo, P ^a   Cali G ^a   D'Armiento, F P ^a   Rocco, A ^a   Nardone, G ^a   Iuvone, T ^a   Steardo, L ^b   Cuomo, R ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Enteric glia; Nitric oxide; S100B; Ulcerative colitis

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BUDESONIDE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; MESSENGER RNA; NITRITE; PROTEIN S100B;

ADULT; ARTICLE; CLINICAL ARTICLE; CLINICAL EVALUATION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENTERITIS; FEMALE; GLIA CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTESTINE INNERVATION; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECTUM BIOPSY; RECTUM MUCOSA; REGULATORY MECHANISM; RNA ISOLATION; ULCERATIVE COLITIS;

ADULT; AGED; BIOPSY; COLITIS, ULCERATIVE; FEMALE; HUMANS; INTERFERON-GAMMA; INTESTINAL MUCOSA; LIPOPOLYSACCHARIDES; MALE; MIDDLE AGED; NERVE GROWTH FACTORS; NEUROGLIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; S100 PROTEINS; TISSUE CULTURE TECHNIQUES;

EID: 70349666893     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2009.01346.x     Document Type: Article

References (41)

1. Sariola H, Saarma M. Novel functions and signalling pathways for GDNF. J Cell Sci 2003 116 : 3855 3862.
2. Fanò G, Biocca S, Fulle S et al. The S100: a protein family in search of a function. Prog Neurobiol 1995 46 : 71 82.
3. Van Eldik LJ, Wainwright MS. The Janus face of glial-derived S100 beta: beneficial and detrimental function in the brain. Restor Neurol Neurosci 2003 21 : 97 108.
4. Griffin WS, Sheng JG, Royston MC et al. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol 1998 8 : 65 72.
5. Petrova TV, Hu J, Van Eldik LJ. Modulation of glial activation by astrocyte-derived protein S100 beta: differential responses of astrocyte and microglial cultures. Brain Res 2000 853 : 74 80.
6. Adami C, Sorci G, Blasi E et al. S100 beta expression in and effects on microglia. Glia 2001 33 : 131 142.
7. Giaroni C, De Ponti F, Casentino M et al. Plasticity in the enteric nervous system. Gastroenterology 1999 117 : 1438 1458.
8. Von Boyen GB, Reinshagen M, Steinkamp M et al. Enteric nervous plasticity and development dependence on neurotrophic factors. J Gastroenterol 2002 37 : 583 588.
9. Ruhl A, Nasser Y, Sharkey KA. Enteric glia. Neurogastroenterol Motil 2004 16 : 44 9.
10. Bush TG, Savidge TC, Freeman TC et al. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 1998 93 : 189 201.
11. Collins SM. The immunomodulation of enteric neuromuscular function: implication for motility and inflammatory disorders. Gastroenetrology 1996 111 : 1683 1699.
12. Ruhl A, Franzke S, Collins SM et al. Interleukin-6 expression and regulation in rat enteric glial cells. Am J Physiol Gastrointest Liver Physiol 2001 280 : 1163 1171.
13. Cornet A, Savidge TC, Cabarrocas J et al. Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease? Proc Natl Acad Sci 2001 98 : 13306 13311.
14. Ferri GL, Probert L, Cocchia D et al. Evidence for the presence of S-100 protein in the glial component of the human enteric nervous system. Nature 1982 297 : 409 412.
15. Neunlist M, Aubert P, Bonnaud S et al. Enteric glia inhibit intestinal epithelial cell proliferation partly through a TGF-beta1-dependent pathway. Am J Physiol Gastrointest Liver Physiol 2007 292 : 231 241.
16. Esposito G, Cirillo C, Sarnelli G et al. Enteric glial-derived S100B protein stimulates nitric oxide production in celiac disease. Gastroenterology 2007 133 : 918 925.
17. Buhner S, Buning C, Genschel J et al. Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation? Gut 2006 55 : 342 347.
18. Kolios G, Petoumenos C, Nackos A. Mediators of inflammation: production and implication in inflammatory bowel disease. Hepatogastroenterology 1998 45 : 1601 1609.
19. Kubes P, McCafferty DM. Nitric oxide and intestinal inflammation. Am J Med 2000 109 : 150 158.
20. Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002 347 : 417 429.
21. Coeffier M, Miralles-Barrachina O, Le Pessot F et al. Influence of glutamine on cytokine production by human gut in vitro. Cytokine 2001 13 : 148 154.
22. Di Rosa M, Radomski M, Carnuccio R et al. Glucocorticoids inhibit the induction of nitric oxide synthase in macrophages. Biochem Biophys Res Commun 1990 172 : 1246 1252.
23. Casabianca A, Orlandi C, Fraternale A et al. Development of a real-time PCR assay using SYBR Green I for provirus load quantification in a murine model of AIDS. J Clin Microbiol 2004 42 : 4361 4364.
24. Green AJ, Keir G, Thompson EJ. A specific and sensitive ELISA for measuring S-100b in cerebrospinal fluid. J Immunol Methods 1997 205 : 35 41.
25. Linehan JD, Kolios G, Valatas V et al. 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 7.
26. Esposito G, Imitola J, Lu J et al. Genomic and functional profiling of human Down syndrome neural progenitors implicates S100B and aquaporin 4 in cell injury. Hum Mol Genet 2008 17 : 440 457.
27. Lundin PD, Edsbacker S, Bergstrand M et al. Pharmacokinetics of budesonide controlled ileal release capsules in children and adults with active Crohn's disease. Aliment Pharmacol Ther 2003 17 : 85 92.
28. Geboes K, Collins S. Structural abnormalities of the nervous system in Crohn's disease and ulcerative colitis. Neurogastroenterol Motil 1998 10 : 189 202.
29. Cabarrocas J, Savidge TC, Liblau RS. Role of enteric glial cells in inflammatory bowel disease. Glia 2003 41 : 81 93.
30. Hoff S, Zeller F, von Weyhern CW et al. 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.
31. Menchen L, Colon AL, Madrigal JL et al. Activity of inducible and neuronal nitric oxide synthases in colonic mucosa predicts progression of ulcerative colitis. Am J Gastroenterol 2004 99 : 1756 1764.
32. Goncalves DS, Lenz G, Karl J et al. Extracellular S100B protein modulates ERK in astrocyte cultures. NeuroReport 2000 11 : 807 809.
33. Lam AG, Koppal T, Akama KT et al. Mechanism of glial activation by S100B: involvement of the transcription factor NFkappaB. Neurobiol Aging 2001 22 : 765 772.
34. Hu J, Ferreira A, Van Eldik LJ. S100β induces neuronal cell death through nitric oxide release from astrocytes. J Neurochem 1997 69 : 2294 2301.
35. Hofmann MA, Drury S, Fu C et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999 97 : 889 901.
36. Schmidt AM, Yan SD, Yan SF et al. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 2001 108 : 949 955.
37. Foell D, Kucharzik T, Kraft M et al. Neutrophil derived human S100A12 (EN-RAGE) is strongly expressed during chronic active inflammatory bowel disease. Gut 2003 52 : 847 853.
38. Hollenbach E, Ruhl A, Zoller M et al. T cell activation by enteric glia: a novel pathway for the amplification of inflammatory responses in the enteric nervous system. Gastroenterology 2000 118 : A184.
39. Geboes K, Rutgeerts P, Ectors N et al. Major histocompatibility class II expression on the small intestinal nervous system in Crohn's disease. Gastroenterology 1992 103 : 439 447.
40. Adami C, Bianchi R, Pula G et al. 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.
41. Dionne S, Laberge S, Deslandres C et al. Modulation of cytokine release from colonic explants by bacterial antigens in inflammatory bowel disease. Clin Exp Immunol 2003 133 : 108 114.