Intracellular zinc is required for intestinal cell survival signals triggered by the inflammatory cytokine TNFα

Journal of Nutritional Biochemistry

Volumn 24, Issue 6, 2013, Pages 967-976

  Ranaldi, Giulia ^a   Ferruzza, Simonetta ^a   Canali, Raffaella ^a   Leoni, Guido ^a   Zalewski, Peter D ^b   Sambuy, Yula ^a   Perozzi, Giuditta ^a   Murgia, Chiara ^b  

^a ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Apoptosis; Caco 2; Crohn's diseases; Enterocyte; Inflammatory bowel diseases; Intestinal permeability; Zinc

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 2; MESSENGER RNA; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; X LINKED INHIBITOR OF APOPTOSIS; ZINC;

APICAL MEMBRANE; APOPTOSIS; ARTICLE; CELL DEATH; CELL FATE; CELL STRAIN CACO 2; CELL SURVIVAL; COLITIS; CONTROLLED STUDY; CROHN DISEASE; EXPERIMENTAL MODEL; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INTESTINE CELL; INTESTINE MUCOSA PERMEABILITY; INTRACELLULAR SIGNALING; UPREGULATION;

APOPTOSIS; CACO-2 CELLS; CELL POLARITY; CELL SURVIVAL; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; INFLAMMATION; INTESTINAL MUCOSA; INTESTINES; PERMEABILITY; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN; ZINC;

EID: 84878013693     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.06.020     Document Type: Article

References (47)

1. Arsenault J.E., Brown K.H. Zinc intake of US preschool children exceeds new dietary reference intakes. Am J Clin Nutr 2003, 78:1011-1017.
2. Maret W. Cellular zinc and redox states converge in the metallothionein/thionein pair. J Nutr 2003, 133:1460S-1462S.
3. Devirgiliis C., Zalewski P.D., Perozzi G., Murgia C. Zinc fluxes and zinc transporter genes in chronic diseases. Mutat Res 2007, 622:84-93.
4. Murgia C., Lang C.J., Truong-Tran A.Q., Grosser D., Jayaram L., Ruffin R.E., et al. Zinc and its specific transporters as potential targets in airway disease. Curr Drug Targets 2006, 7:607-627.
5. Fukada T., Yamasaki S., Nishida K., Murakami M., Hirano T. Zinc homeostasis and signaling in health and diseases: zinc signaling. J Biol Inorg Chem 2011, 16:1123-1134.
6. Maret W., Sandstead H.H. Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 2006, 20:3-18.
7. Prasad A.S., Schulert A.R., Miale A., Farid Z., Sandstead H.H. Zinc and iron deficiencies in male subjects with dwarfism and hypogonadism but without ancylostomiasis, schistosomiasis or severe anemia. Am J Clin Nutr 1963, 12:437-444.
8. Prasad A.S. Impact of the discovery of human zinc deficiency on health. J Am Coll Nutr 2009, 28:257-265.
9. Matsui T. Zinc deficiency in Crohn's disease. J Gastroenterol 1998, 33:924-925.
10. Tysk C., Lindberg E., Jarnerot G., Floderus-Myrhed B. Ulcerative colitis and Crohn's disease in an unselected population of monozygotic and dizygotic twins. A study of heritability and the influence of smoking. Gut 1988, 29:990-996.
11. Ferguson L.R., Shelling A.N., Browning B.L., Huebner C., Petermann I. Genes, diet and inflammatory bowel disease. Mutat Res 2007, 622:70-83.
12. Ferguson L.R. Nutrigenomics and inflammatory bowel diseases. Expert Rev Clin Immunol 2010, 6:573-583.
13. Ferguson L.R., Philpott M., Dryland P. Nutrigenomics in the whole-genome scanning era: Crohn's disease as example. Cell Mol Life Sci 2007, 64:3105-3118.
14. Schulzke J.D., Ploeger S., Amasheh M., Fromm A., Zeissig S., Troeger H., et al. Epithelial tight junctions in intestinal inflammation. Ann N Y Acad Sci 2009, 1165:294-300.
15. Chowers Y., Allez M. Efficacy of anti-TNF in Crohn's disease: how does it work?. Curr Drug Targets 2010, 11:138-142.
16. Edelblum K.L., Yan F., Yamaoka T., Polk D.B. Regulation of apoptosis during homeostasis and disease in the intestinal epithelium. Inflamm Bowel Dis 2006, 12:413-424.
17. Liuzzi J.P., Bobo J.A., Lichten L.A., Samuelson D.A., Cousins R.J. Responsive transporter genes within the murine intestinal-pancreatic axis form a basis of zinc homeostasis. Proc Natl Acad Sci U S A 2004, 101:14355-14360.
18. Liuzzi J.P., Cousins R.J. Mammalian zinc transporters. Annu Rev Nutr 2004, 24:151-172.
19. Hering N.A., Schulzke J.D. Therapeutic options to modulate barrier defects in inflammatory bowel disease. Dig Dis 2009, 27:450-454.
20. Sturniolo G.C., Di Leo V., Ferronato A., D'Odorico A., D'Inca R. Zinc supplementation tightens "leaky gut" in Crohn's disease. Inflamm Bowel Dis 2001, 7:94-98.
21. Sturniolo G.C., Fries W., Mazzon E., Di Leo V., Barollo M., D'Inca R. Effect of zinc supplementation on intestinal permeability in experimental colitis. J Lab Clin Med 2002, 139:311-315.
22. Iwaya H., Kashiwaya M., Shinoki A., Lee J.S., Hayashi K., Hara H., et al. Marginal zinc deficiency exacerbates experimental colitis induced by dextran sulfate sodium in rats. J Nutr 2011, 141:1077-1082.
23. Chantret I., Rodolosse A., Barbat A., Dussaulx E., Brot-Laroche E., Zweibaum A., et al. Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J Cell Sci 1994, 107(Pt 1):213-225.
24. Ferruzza S., Scacchi M., Scarino M.L., Sambuy Y. Iron and copper alter tight junction permeability in human intestinal Caco-2 cells by distinct mechanisms. Toxicol In Vitro 2002, 16:399-404.
25. Ho E., Quan N., Tsai Y.H., Lai W., Bray T.M. Dietary zinc supplementation inhibits NFkappaB activation and protects against chemically induced diabetes in CD1 mice. Exp Biol Med (Maywood) 2001, 226:103-111.
26. Makhov P., Golovine K., Uzzo R.G., Rothman J., Crispen P.L., Shaw T., et al. Zinc chelation induces rapid depletion of the X-linked inhibitor of apoptosis and sensitizes prostate cancer cells to TRAIL-mediated apoptosis. Cell Death Differ 2008, 15:1745-1751.
27. Ranaldi G., Caprini V., Sambuy Y., Perozzi G., Murgia C. Intracellular zinc stores protect the intestinal epithelium from ochratoxin A toxicity. Toxicol In Vitro 2009, 23:1516-1521.
28. Sambuy Y., De Angelis I., Ranaldi G., Scarino M.L., Stammati A., Zucco F. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol Toxicol 2005, 21:1-26.
29. Mashukova A., Wald F.A., Salas P.J. Tumor necrosis factor alpha and inflammation disrupt the polarity complex in intestinal epithelial cells by a posttranslational mechanism. Mol Cell Biol 2011, 31:756-765.
30. Gyrd-Hansen M., Meier P. IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer 2010, 10:561-574.
31. Chu Z.L., McKinsey T.A., Liu L., Gentry J.J., Malim M.H., Ballard D.W. Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control. Proc Natl Acad Sci U S A 1997, 94:10057-10062.
32. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998, 281:1680-1683.
33. Canali R., Vignolini F., Nobili F., Mengheri E. Reduction of oxidative stress and cytokine-induced neutrophil chemoattractant (CINC) expression by red wine polyphenols in zinc deficiency induced intestinal damage of rat. Free Radic Biol Med 2000, 28:1661-1670.
34. Finamore A., Massimi M., Conti Devirgiliis L., Mengheri E. Zinc deficiency induces membrane barrier damage and increases neutrophil transmigration in Caco-2 cells. J Nutr 2008, 138:1664-1670.
35. Santosham M., Chandran A., Fitzwater S., Fischer-Walker C., Baqui A.H., Black R. Progress and barriers for the control of diarrhoeal disease. Lancet 2010, 376:63-67.
36. Frederickson C. Imaging zinc: old and new tools. Sci STKE. 2003;2003:pe18.
37. Zalewski P.D., Millard S.H., Forbes I.J., Kapaniris O., Slavotinek A., Betts W.H., et al. Video image analysis of labile zinc in viable pancreatic islet cells using a specific fluorescent probe for zinc. J Histochem Cytochem 1994, 42:877-884.
38. Capaldo C.T., Nusrat A. Cytokine regulation of tight junctions. Biochim Biophys Acta 2009, 1788:864-871.
39. Suenaert P., Bulteel V., Lemmens L., Noman M., Geypens B., Van Assche G., et al. Anti-tumor necrosis factor treatment restores the gut barrier in Crohn's disease. Am J Gastroenterol 2002, 97:2000-2004.
40. Ma T.Y., Iwamoto G.K., Hoa N.T., Akotia V., Pedram A., Boivin M.A., et al. TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 2004, 286:G367-G376.
41. Ma T.Y., Boivin M.A., Ye D., Pedram A., Said H.M. Mechanism of TNF-{alpha} modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am J Physiol Gastrointest Liver Physiol 2005, 288:G422-G430.
42. Wang F., Schwarz B.T., Graham W.V., Wang Y., Su L., Clayburgh D.R., et al. IFN-gamma-induced TNFR2 expression is required for TNF-dependent intestinal epithelial barrier dysfunction. Gastroenterology 2006, 131:1153-1163.
43. Fries W., Muja C., Crisafulli C., Cuzzocrea S., Mazzon E. Dynamics of enterocyte tight junctions: effect of experimental colitis and two different anti-TNF strategies. Am J Physiol Gastrointest Liver Physiol 2008, 294:G938-G947.
44. Ye D., Guo S., Al-Sadi R., Ma T.Y. MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology 2011, 141:1323-1333.
45. Yamaoka T., Yan F., Cao H., Hobbs S.S., Dise R.S., Tong W., et al. Transactivation of EGF receptor and ErbB2 protects intestinal epithelial cells from TNF-induced apoptosis. Proc Natl Acad Sci U S A 2008, 105:11772-11777.
46. Flieger D., Riethmuller G., Ziegler-Heitbrock H.W. Zn++ inhibits both tumor necrosis factor-mediated DNA fragmentation and cytolysis. Int J Cancer 1989, 44:315-319.
47. Truong-Tran A.Q., Carter J., Ruffin R.E., Zalewski P.D. The role of zinc in caspase activation and apoptotic cell death. Biometals 2001, 14:315-330.