Celiac disease, inflammation and oxidative damage: A nutrigenetic approach

Nutrients

Volumn 4, Issue 4, 2012, Pages 243-257

  Ferretti, Gianna ^a   Bacchetti, Tiziana ^a   Masciangelo, Simona ^a   Saturni, Letizia ^b  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b Ibero American University Foundation FUNIBER   (Italy)

Author keywords

Celiac disease; Fitonutrients; Gliadin peptides; Inflammation; Nutrigenetic; Nutrigenomic; Oxidative stress; Proteomic

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; CAROTENOID; FLAVONOID; GAMMA INTERFERON; GLIADIN; GLUTEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 15; INTERLEUKIN 6; LONG CHAIN FATTY ACID; NITRIC OXIDE; POLYPHENOL; PROLAMIN; TUMOR NECROSIS FACTOR ALPHA;

BIOCHEMISTRY; CELIAC DISEASE; CELL FUNCTION; CELL STRUCTURE; CHRONIC INFLAMMATION; CYTOKINE RELEASE; CYTOTOXICITY; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HEREDITY; HUMAN; IMMUNOLOGICAL PROCEDURES; IMMUNOMODULATION; INFLAMMATION; INTESTINE CELL; MOLECULAR DYNAMICS; NUTRIGENOMICS; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEOMICS; REVIEW; STOMACH PROTECTION; VITAMIN SUPPLEMENTATION;

EID: 84860134435     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu4040243     Document Type: Review

References (83)

1. Sollid, L.M.; Jabri, B. Is celiac disease an autoimmune disorder? Curr. Opin. Immunol. 2005, 17, 595-600.
2. Van Heel, D.A.; West, J. Recent advances in coeliac disease. Gut 2006, 36, 864-874.
3. Wieser, H.; Koehler, P. The biochemical basis of celiac disease. Cereal Chem. 2008, 85, 1-13.
4. Diosdado, B.; van Oort, E.; Wijmenga, C. Coelionomics: Towards understanding the molecular pathology of coeliac disease. Clin. Chem. Lab. Med. 2005, 43, 685-695.
5. Koning, F.; Schuppan, D.; Cerf-Bensussan, N.; Sollid, L.M. Pathomechanisms in celiac disease. Best Pract. Res. Clin. Gastroenterol. 2005, 19, 373-387.
6. Jabri, B.; Kasarda, D.D.; Green, P.H.R. Innate and adaptive immunity: The Yin and Yang of celiac disease. Immunol. Rev. 2005, 206, 219-231.
7. Mamone, G.; Picarello, G; Addeo, F.; Ferranti, P. Proteomic analysis in allergy and intolerance to wheat products. Expert Rev. Proteomics 2011, 8, 95-115.
8. Ciccocioppo, R.; di Sabatino, A.; Corazza, G.R. The immune recognition of gluten in coeliac disease. Clin. Exp. Immunol. 2005, 140, 408-416.
9. Shan, L.; Molberg, O.; Parrot, I.; Hausch, F.; Filiz, F.; Gray, G.M.; Sollid, L.M.; Khosla, C. Structural basis for gluten intolerance in celiac sprue. Science 2002, 297, 2275-2279.
10. Trynka, G.; Zhernakova, A.; Romanos, J.; Franke, L.; Hunt, K.A.; Turner, G.; Bruinenberg, M.; Heap, G.A.; Platteel, M.; Ryan, A.W.; et al. Coeliac disease-associated risk variants in TNFAIP3 and REL implicate altered NF-kappaB signalling. Gut 2009, 58, 1078-1083.
11. Vader, W.; Stepniak, D.; Kooy, Y.; Mearin, L.; Thompson, A.; van Rood, J.J.; Spaenij, L.; Koning, F. The HLA-DQ2 gene dose effect in celiac disease is directly related to the magnitude and breadth of gluten-specific T cell responses. Proc. Natl. Acad. Sci. USA 2003, 100, 12390-12395.
12. Harmon, G.S.; Lebeck, L.K.; Weidner, N. Gluten-dependent enteropathy and atypical human leukocyte antigen alleles. Hum. Pathol. 2011, 42, 1112-1126.
13. Karell, K.; Louka, A.S.; Moodie, S.J.; Ascher, H.; Clot, F.; Greco, L.; Ciclitira, P.J.; Sollid, L.M.; Partanen, J. European genetics cluster on celiac disease. Hum. Immunol. 2003, 64, 469-477.
14. Calder, P.C.; Albers, R.; Antoine, J.M.; Blum, S.; Bourdet-Sicard, R.; Ferns, G.A.; Folkerts, G.; Friedmann, P.S.; Frost, G.S.; Guarner, F.; et al. Inflammatory disease processes and interactions with nutrition. Br. J. Nutr. 2009, 101, 1-45.
15. Matysiak-Budnik, T.; Candalh, C.; Dugave, C.; Namane, A.; Cellier, C.; Cerf-Bensussan, N.; Heyman, M. Alterations of the intestinal tran sport and processing of gliadin peptides in celiac disease. Gastroenterology 2003, 125, 696-707.
16. Trynka, G.; Wijmenga, C.; van Heel, D.A. A genetic perspective on coeliac disease. Trends Mol. Med. 2010, 16, 537-550.
17. Cornell, H.J.; Wills-Johnson, G. Structure-activity relationships in coeliac-toxic gliadin peptides. Amino Acid 2001, 21, 243-253.
18. Auricchio, S.; Barone, M.V.; Troncone, R. Dietary proteins and mechanismsof gastrointestinal diseases: Gliadin as a model. J. Pediatr. Gastroenterol. Nutr. 2004, 39, S738-S739.
19. Hausch, F.; Shan, L.; Santiago, N.A.; Gray, G.M.; Khosla, C. Intestinal digestive resistance of immunodominant gliadin peptides. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283, 996-1003.
20. Folk, J.E. Mechanism and basis for specificity of transglutaminasecatalyzede-(g-glutamyl) lysine bond formation. Adv. Enzymol. Relat. Areas Mol. Biol. 1983, 54, 1-56.
21. Kagnoff, M.F. Overview and pathogenesis of celiac disease. Gastroenterology 2005, 128, 10-18.
22. Maiuri, L.; Ciacci, C.; Ricciardelli, I.; Vacca, L.; Raia, V.; Auricchio, S.; Picard, J.; Osman, M.; Quarantino, S.; Londei, M. Association between innate response to gliadin and activation of pathogenic T cells in celiac disease. Lancet 2003, 362, 30-37.
23. Pender, S.L.F.; Lionetti, P.; Murch, S.H.; Wathan, N.; MacDonald, T.T. Proteolytic degradation of intestinal mucosa extracellular matrix after lamina propria T cell activation. Gut 1996, 39, 284-290.
24. Elli, L.; Dolfini, E.; Bardella, M.T. Gliadin cytotoxicity and in vitro cell cultures. Toxicol. Lett. 2003, 46, 1-8.
25. Maiuri, L.; Troncone, R.; Mayer, M.; Coletta, S.; Picarelli, A.; de Vincenzi, M.; Pavone, V.; Auricchio, S. In vitro activities of A-gliadin related synthetic peptides: Damaging affect on the atrophic coeliac mucosa and activation of mucosal immune response in the treated coeliac mucosa. Scand. J. Gastroenterol. 1996, 31, 247-253.
26. Schumann, M.; Richter, J.F.; Wedell, I.; Moos, V.; Zimmermann-Kordmann, M.; Schneider, T.; Daum, S.; Zeitz, M.; Fromm, M.; Schulzke, J.D. Mechanisms of epithelial translocation of the a2-gliadin-33mer in coeliac sprue. Gut 2008, 57, 747-754.
27. Heyman, M.; Menard, S. Pathways of gliadin transport in celiac disease. Ann. N. Y. Acad. Sci. 2009, 1165, 274-278.
28. Zimmer, K.P.; Fischer, I.; Mothes, T.; Weissen-Plenz, G.; Schmitz, M.; Wieser, H.; Büning, J.; Lerch, M.M.; Ciclitira, P.C.; Weber, P.; et al. Endocytotic segregation of gliadin peptide 31-49 in enterocytes. Gut 2010, 59, 300-310.
29. Luciani, A.; Villella, V.R.; Vasaturo, A.; Giardino, I.; Pettoello-Mantovani, M.; Guido, S.; Cexus, O.N.; Peake, N.; Londei, M.; Quaratino, S.; et al. Lysosomal accumulation of gliadin p31-43 peptide induces oxidative stress and tissue transglutaminase-mediated PPARgamma downregulation in intestinal epithelial cells and coeliac mucosa. Gut 2010, 59, 311-319.
30. Rivabene, R.; Mancini, E.; de Vincenzi, M. In vitro cytotoxic effect of wheat gliadin-derived peptides on the Caco-2 intestinal cell line is associated with intracellular oxidative imbalance: Implications for coeliac disease. Biochim. Biophys. Acta 1999, 1453, 152-160.
31. Di Sabatino, A.; Ciccocioppo, R.; D'Alò, S.; Parroni, R.; Millimaggi, M.; Cifone, M.G.; Corazza, G.R. Intraepithelial and lamina propria lymphocytes show distinct patterns of apoptosis whereas both populations are active in Fas based cytotoxicity in coeliac disease. Gut 2001, 49, 380-386.
32. Giovannini, C.; Sanchez, M.; Straface, E.; Scazzocchio, B.; Silano, M.; de Vincenzi, M. Induction of apoptosis in CaCo-2 cells by wheat gliadin peptides. Toxicology 2000, 145, 63-71.
33. Giovannini, C.; Mancini, E.; de Vincenzi, M. Inhibition of the cellular metabolism of Caco-2 cells by prolamin peptides from cereals toxic for coeliacs. Toxicol. In Vitro 1996, 10, 533-538.
34. Giovannini, C.; Maiuri, L.; de Vincenzi, M.; Cytotoxic effect of prolamin-derived peptides on in vitro cultures of cell line Caco-2: Implications for coeliac disease. Toxicol. In Vitro 1994, 9, 251-255.
35. Dolfini, E.; Elli, L.; Dasdia, T.; Bufardeci, B.; Colleoni, M.P.; Costa, B.; Floriani, I.; Falini, M.L.; Guerrieri, N.; Forlani, F.; et al. In vitro cytotoxic effect of bread wheat gliadin on the LoVo human adenocarcinoma cell line. Toxicol. In Vitro 2002, 16, 331-337.
36. Lavö, B.; Knutson, L.; Lööf, L.; Hällgren, R. Gliadin challenge-induced jejunal prostaglandin E2 secretion in celiac disease. Gastroenterologist 1990, 99, 703-709.
37. Stojiljković, V.; Todorović, A.; Pejić, S.; Kasapović, J.; Saicić, Z.S.; Radlović, N.; Pajović, S.B. Antioxidant status and lipid peroxidation in small intestinal mucosa of children with celiac disease. Clin. Biochem. 2009, 42, 1431-1437.
38. Stahlberg, M.R.; Hietanen, E.; Maki, M. Mucosal biotransformation rates in the small intestine of children. Gut 1988, 29, 1058-1063.
39. Sido, B.; Hack, V.; Hochlehnert, A.; Lipps, H.; Herfarth, C.; Droge, W. Impairment of intestinal glutathione synthesis in patients with inflammatory bowel disease. Gut 1998, 42, 485-492.
40. Daniels, I.; Cavill, D.; Murray, I.A.; Long, R.G. Elevated expression of iNOS mRNA and protein in coeliac disease. Clin. Chim. Acta 2005, 356, 134-142.
41. Ter Steege, J.; Buurman, W.; Arends, J.W.; Forget, P. Presence of inducible nitric oxide synthase, nitrotyrosine, CD68, and CD14 in the small intestine in celiac disease. Lab. Invest. 1997, 77, 29-36.
42. Beckett, C.G.; Dell'Olio, D.; Ellis, H.J.; Rosen-Bronson, S.; Ciclitira, P.J. The detection and localization of inducible nitric oxide synthase production in the small intestine of patients with coeliac disease. Eur. J. Gastroenterol. Hepatol. 1998, 10, 641-647.
43. Holmgren Peterson, K.; Falth-Magnusson, K.; Magnusson, K.E.; Stenhammar, L.; Sundqvist, T. Children with celiac disease express inducible nitric oxide synthase in the small intestine during gluten challenge. Scand. J. Gastroenterol. 1998, 33, 939-943.
44. Murray, I.A.; Daniels, I.; Coupland, K; Smith, J.A.; Long, R.G. Increased activity and expression of iNOS in human duodenal enterocytes from patients with celiac disease. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283, 319-326.
45. Murray, I.A.; Bullimore, D.W.; Long, R.G. Fasting plasma nitric oxide products in coeliac disease. Eur. J. Gastroenterol. Hepatol. 2003, 15, 1091-1095.
46. Ter Steege, J.C.; Koster-Kamphuis, L.; van Straaten, E.A.; Forget, P.P.; Buurman, W.A. Nitrotyrosine in plasma of celiac disease patients as detected by a new sandwich ELISA. Free Radic. Biol. Med. 1998, 25, 953-963.
47. Ertekin, V.; Selimoglu, M.A.; Türkan, Y.; Akçay, F. Serum nitric oxide levels in children with celiac disease. J. Clin. Gastroenterol. 2005, 39, 782-785.
48. Van Straaten, E.A.; Koster-Kamphuis, L.; Bovee-Oudenhoven, I.M.; van der Meer, R.; Forget, P.P. Increased urinary nitric oxide oxidation products in children with active coeliac disease. Acta Paediatr. 1999, 88, 528-531.
49. Högberg, L.; Webb, C.; Fälth-Magnusson, K.; Forslund, T.; Magnusson, K.E.; Danielsson, L.; Ivarsson, A.; Sandström, O.; Sundqvist, T. Children with screening-detected coeliac disease show increased levels of nitric oxide products in urine. Acta Paediatr. 2011, 100, 1023-1027.
50. Sundqvist, T.; Laurin, P.; Fälth-Magnusson, K.; Magnusson, K.E.; Stenhammar, L. Significantly increased levels of nitric oxide products in urine of children with celiac disease. J. Pediatr. Gastroenterol. Nutr. 1998, 27, 196-198.
51. Stojiljković, V.; Todorović, A.; Radlović, N.; Pejić, S.; Mladenović, M.; Kasapović, J.; Pajović, S.B. Antioxidant enzymes, glutathione and lipid peroxidation in peripheral blood of children affected by coeliac disease. Ann. Clin. Biochem. 2007, 44, 537-543.
52. Odetti, P.; Valentini, S.; Aragno, I.; Garibaldi, S.; Pronzato, M.A.; Rolandi, E.; Barreca, T. Oxidative stress in subjects affected by celiac disease. Free Radic. Res. 1998, 29, 7-24.
53. Lavy, A.; Ben Amotz, A.; Aviram, M. Increased susceptibility to undergo lipid peroxidation of chylomicrons and low-density lipoprotein in celiac disease. Ann. Nutr. Metab. 1993, 37, 68-74.
54. Szaflarska-Poplawska, A.; Siomek, A.; Czerwionka-Szaflarska, M.; Gackowski, D.; Rózalski, R.; Guz, J.; Szpila, A.; Zarakowska, E.; Olinski, R. Oxidatively damaged DNA/oxidative stress in children with celiac disease. Cancer Epidemiol. Biomark. Prev. 2010, 19, 1960-1965.
55. Hozyasz, K.K.; Chelchowska, M.; Laskowska-Klita, T. Vitamin E levels in patients with celiac disease. Med. Wieku Rozwoj. 2003, 7, 593-604.
56. Rothem, L.; Hartman, C; Dahan, A.; Lachter, J.; Eliakim, R; Shamir, R. Paraoxonases are associated with intestinal inflammatory diseases and intracellularly localized to the endoplasmic reticulum. Free Radic. Biol. Med. 2007, 43, 730-739.
57. Maiuri, M.C.; de Stefano, D.; Mele, G.; Iovine, B.; Bevilacqua, M.A.; Greco, L.; Auricchio, S.; Carnuccio, R. Gliadin increases iNOS gene expression in interferon-Stimulated RAW 264.7 cells through a mechanism involving NF-kB. Naunyn Schmiedebergs Arch. Pharmacol. 2003, 368, 63-71.
58. de Stefano, D.; Maiuri, M.C.; Iovine, B.; Ialenti, A.; Bevilacqua, M.A.; Carnuccio, R. The role of NF-kB, IRF-1, and STAT-1a transcription factors in the iNOS gene induction by gliadin and IFN-y in RAW 264.7 macrophages. J. Mol. Med. 2006, 84, 65-74.
59. Thomas, K.E.; Sapone, A.; Fasano, A.; Vogel, S.N. Gliadin stimulation of murine macrophage inflammatory gene expression and intestinal permeability are MyD88-dependent: Role of the innate immune response in celiac disease. J. Immunol. 2006, 176, 2512-2521.
60. Maiuri, L.; Ciacci, C; Ricciardelli, I.; Vacca, L.; Raia, V.; Rispo, A.; Griffin, M.; Issekutz, T.; Quaratino, S.; Londei, M. Unexpected role of surface transglutaminase type II in celiac disease. Gastroenterology 2005, 129, 1400-1413.
61. Luciani, A.; Villella, V.R.; Vasaturo, A.; Giardino, I.; Pettoello-Mantovani, M.; Guido, S.; Cexus, O.N.; Peake, N.; Londei, M.; Quaratino, S.; et al. Lysosomal accumulation of gliadin p31e43 peptide induces oxidative stress and tissue transglutaminase-mediated PPARg downregulation in intestinal epithelial cells and coeliac mucosa. Gut 2010, 59, 311-319.
62. de Re, V.; Simula, M.P.; Notarpietro, A.; Canzonieri, V.; Cannizzaro, R; Toffoli, G. Do gliadin and tissue transglutaminase mediate PPAR downregulation in intestinal cells of patients with coeliac disease? Gut 2010, 59, 1730-1731.
63. Simula, M.P.; Cannizzaro, R; Canzonieri, V.; Pavan, A.; Maiero, S.; Toffoli, G; de Re, V. PPAR signaling pathway and cancer-related proteins are involved in celiac disease-associated tissue damage. Mol. Med. 2010, 16, 199-209.
64. Maiuri, M.C.; de Stefano, D.; Mele, G.; Fecarotta, S.; Greco, L.; Troncone, R; Carnuccio, R. Nuclear factor kappa B is activated in small intestinal mucosa of celiac patients. J. Mol. Med. 2003, 81, 373-379.
65. Flohè, L.; Brigelius-Flohe, R; Saliou, C; Traber, M.G.; Packer, L. Redox regulation of NF-kB activation. Free Radic. Biol. Med. 1997, 22, 1115-1126.
66. Ohmori, Y.; Hamilton, T.A. Cooperative interaction between interferon (IFN) stimulus response element and kappa B sequence motifs controls IFN gamma- and lipopolysaccharide-stimulated transcription from the murine IP 10 promoter. J. Biol. Chem. 1993, 268, 6677-6688.
67. Vincentini, O.; Quaranta, M.G.; Viora, M.; Agostoni, C; Silano, M. Docosahexaenoic acid modulates in vitro the inflammation of celiac disease in intestinal epithelial cells via the inhibition of cPLA2. Clin. Nutr. 2011, 30, 541-546.
68. Friis, S.; Anthonsen, D.; Norén, O.; Sjöström, H. Gamma-type gliadins cause secretion of prostaglandin E2 in patients with coeliac disease. Clin. Chim. Acta 1994, 231, 173-183.
69. Juuti-Uusitalo, K.; Mäki, M.; Kaukinen, K.; Collin, P.; Visakorpi, T.; Vihinen, M.; Kainulainen, H. cDNA microarray analysis of gene expression in coeliac disease jejunal biopsy samples. J. Autoimmun. 2004, 22, 249-265.
70. Juuti-Uusitalo, K.; Mäki, M.; Kainulainen, H.; Isola, J.; Kaukinen, K. Gluten affects epithelial differentiation-associated genes in small intestinal mucosa of coeliac patients. Clin. Exp. Immunol. 2007, 150, 294-305.
71. Cataldo, F.; Lio, D.; Marino, V.; Scola, L.; Crivello, A.; Corazza, G.R.; Working Group of the SIGEP; Working Group of Club del Tenue. Plasma cytokine profiles in patients with celiac disease and selective IgA deficiency. Pediatr. Allergy Immunol. 2003, 14, 320-324.
72. Calder, P.C. Fatty acids and inflammation: The cutting edge between food and pharma. Eur. J. Pharmacol. 2011, 668, 50-58.
73. Goetzl, E.J.; Wasserman, S.I.; Gigli, I.; Austen, K.F. Enhancement of random migration and chemotactic response of human leukocytes by ascorbic acid. J. Clin. Invest. 1974, 53, 813-818.
74. Cook-Mills, J.M.; McCary, C.A. Isoforms of vitamin E differentially regulate inflammation. Endocr. Metab. Immune Disord. Drug Targets 2010, 10, 348-366.
75. Bernardo, D.; Martínez-Abad, B.; Vallejo-Diez, S.; Montalvillo, E.; Benito, V.; Anta, B.; Fernández-Salazar, L.; Blanco-Quirós, A.; Garrote, J.A.; Arranz, E. Ascorbate-dependent decrease of the mucosal immune inflammatory response to gliadin in coeliac disease patients. Allergol. Immunopathol. 2012, 40, 3-8.
76. Hecker, M.; Preiss, C; Klemm, V.; Busse, R. Inhibition by antioxidants of nitric oxide synthase expression in murine macrophages: Role of nuclear factor kappa B and interferon regulatory factor 1. Br. J. Pharmacol. 1996, 118, 2178-2184.
77. Heber, D.; Lu, Q.Y. Overview of mechanisms of action of lycopene. Exp. Biol. Med. 2002, 227, 920-923.
78. Di Carlo, G; Mascolo, N.; Izzo, A.A.; Capasso, F. Flavonoids: Old and new aspects of a class of natural therapeutic drugs. Life Sci. 1999, 65, 337-353.
79. de Stefano, D.; Maiuri, M.C.; Simeon, V.; Grassia, G; Soscia, A.; Cinelli, M.P.; Carnuccio, R. Lycopene, quercetin and tyrosol prevent macrophage activation induced by gliadin and IFN-gamma. Eur. J. Pharmacol. 2007, 566, 192-199.
80. Suzuki, T.; Hara, H. Role of flavonoids in intestinal tight junction regulation. J. Nutr. Biochem. 2011, 22, 401-408.
81. Lee, J.Y.; Sohn, K.H.; Rhee, S.H.; Hwang, D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 2001, 276, 16683-16689.
82. Zapata-Gonzalez, F.; Rueda, F.; Petriz, J.; Domingo, P.; Villarroya, F.; Diaz-Delfin, J.; de Madariaga, M.A.; Domingo, J.C. Human dendritic cell activities are modulated by the omega-3 fatty acid, docosahexaenoic acid, mainly through PPAR(gamma):RXR heterodimers: Comparison with other polyunsaturated fatty acids. J. Leukoc. Biol. 2008, 84, 1172-1182.
83. Vincentini, O.; Quaranta, M.G.; Viora, M.; Agostoni, C; Silano, M. Docosahexaenoic acid modulates in vitro the inflammation of celiac disease in intestinal epithelial cells via the inhibition of cPLA2. Clin. Nutr. 2011, 30, 541-546.