Degradation of coeliac disease-inducing rye secalin by germinating cereal enzymes: Diminishing toxic effects in intestinal epithelial cells

Clinical and Experimental Immunology

Volumn 161, Issue 2, 2010, Pages 242-249

  Stenman, S M ^a   Lindfors, K ^a   Venalainen J I ^c   Hautala, A ^a   Mannisto P T ^d   Garcia Horsman, J A ^d   Kaukovirta Norja, A ^e   Auriola, S ^c   Mauriala, T ^d   Maki M ^a,b   Kaukinen, K ^a,b  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

Author keywords

Caco 2; coeliac disease; germinating cereal enzymes; innate immunity; permeability

Indexed keywords

ACTIN; ENZYME; GLIADIN; OCCLUDIN; PROLAMIN; PROTEIN ZO1; SECALIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BARLEY; CELIAC DISEASE; CELL PERMEABILIZATION; CELL STRAIN CACO 2; CEREAL; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; MASS SPECTROMETRY; NONHUMAN; OAT; PRIORITY JOURNAL; PROTEIN DEGRADATION; RYE; WHEAT;

AVENA SATIVA; CACO-2 CELLS; CELIAC DISEASE; CELL MEMBRANE; CEREALS; CYTOSKELETON; ELECTRIC IMPEDANCE; GERMINATION; GLIADIN; GLUTENS; HORDEUM; HUMANS; INTESTINAL MUCOSA; MEMBRANE PROTEINS; PEPSIN A; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; PERMEABILITY; PHOSPHOPROTEINS; SECALE CEREALE; TIGHT JUNCTIONS; TRITICUM; TRYPSIN;

EID: 77954635978     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2010.04119.x     Document Type: Article

References (46)

1. Bruce G, Woodley JF, Swan CH. Breakdown of gliadin peptides by intestinal brush borders from coeliac patients. Gut 1984 25 : 919 24.
2. Shan L, Molberg O, Parrot I et al. Structural basis for gluten intolerance in celiac sprue. Science 2002 297 : 2275 9.
3. Hausch F, Shan L, Santiago NA, Gray GM, Khosla C. Intestinal digestive resistance of immunodominant gliadin peptides. Am J Physiol Gastrointest Liver Physiol 2002 283 : G996 G1003.
4. Sollid LM. Coeliac disease: dissecting a complex inflammatory disorder. Nat Rev Immunol 2002 2 : 647 55.
5. Maiuri L, Ciacci C, Auricchio S, Brown V, Quaratino S, Londei M. Interleukin 15 mediates epithelial changes in celiac disease. Gastroenterology 2000 119 : 996 1006.
6. Maiuri L, Ciacci C, Ricciardelli I et al. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. Lancet 2003 362 : 30 7.
7. Di Sabatino A, Ciccocioppo R, Cupelli F et al. Epithelium derived interleukin 15 regulates intraepithelial lymphocyte Th1 cytokine production, cytotoxicity, and survival in coeliac disease. Gut 2006 55 : 469 77.
8. Yokoyama S, Watanabe N, Sato N et al. Antibody-mediated blockade of IL-15 reverses the autoimmune intestinal damage in transgenic mice that overexpress IL-15 in enterocytes. Proc Natl Acad Sci USA 2009 106 : 15849 54.
9. Mention JJ, Ben Ahmed M, Begue B et al. Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology 2003 125 : 730 45.
10. Schulzke JD, Schulzke I, Fromm M, Riecken EO. Epithelial barrier and ion transport in coeliac sprue: electrical measurements on intestinal aspiration biopsy specimens. Gut 1995 37 : 777 82.
11. Sander GR, Cummins AG, Henshall T, Powell BC. Rapid disruption of intestinal barrier function by gliadin involves altered expression of apical junctional proteins. FEBS Lett 2005 579 : 4851 5.
12. Lammers KM, Lu R, Brownley J et al. Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology 2008 135 : 194 204 e3.
13. Tripathi A, Lammers KM, Goldblum S et al. Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proc Natl Acad Sci USA 2009 106 : 16799 804.
14. Janatuinen EK, Pikkarainen PH, Kemppainen TA et al. A comparison of diets with and without oats in adults with celiac disease. N Engl J Med 1995 333 : 1033 7.
15. Hogberg L, Laurin P, Falth-Magnusson K et al. Oats to children with newly diagnosed coeliac disease: a randomised double blind study. Gut 2004 53 : 649 54.
16. Koskinen O, Villanen M, Korponay-Szabo I, Lindfors K, Maki M, Kaukinen K. Oats do not induce systemic or mucosal autoantibody response in children with coeliac disease. J Pediatr Gastroenterol Nutr 2009 48 : 559 65.
17. Sturgess R, Day P, Ellis HJ et al. Wheat peptide challenge in coeliac disease. Lancet 1994 343 : 758 61.
18. Anderson RP, Degano P, Godkin AJ, Jewell DP, Hill AV. In vivo antigen challenge in celiac disease identifies a single transglutaminase-modified peptide as the dominant A-gliadin T-cell epitope. Nat Med 2000 6 : 337 42.
19. Stenman SM, Lindfors K, Korponay-Szabo IR et al. Secretion of celiac disease autoantibodies after in vitro gliadin challenge is dependent on small-bowel mucosal transglutaminase 2-specific IgA deposits. BMC Immunol 2008 9 : 6.
20. Wieser H. The precipitating factor in coeliac disease. Baillières Clin Gastroenterol 1995 9 : 191 207.
21. Vader LW, Stepniak DT, Bunnik EM et al. Characterization of cereal toxicity for celiac disease patients based on protein homology in grains. Gastroenterology 2003 125 : 1105 13.
22. Kieffer M, Frazier PJ, Daniels NW, Coombs RR. Wheat gliadin fractions and other cereal antigens reactive with antibodies in the sera of coeliac patients. Clin Exp Immunol 1982 50 : 651 60.
23. Kilmartin C, Wieser H, Abuzakouk M, Kelly J, Jackson J, Feighery C. Intestinal T cell responses to cereal proteins in celiac disease. Dig Dis Sci 2006 51 : 202 9.
24. Baker PG, Read AE. Oats and barley toxicity in coeliac patients. Postgrad Med J 1976 52 : 264 8.
25. Anand BS, Piris J, Truelove SC. The role of various cereals in coeliac disease. Q J Med 1978 47 : 101 10.
26. Dicke WK, Weijers HA, Van De Kamer JH. Coeliac disease. II. The presence in wheat of a factor having a deleterious effect in cases of coeliac disease. Acta Paediatr 1953 42 : 34 42.
27. Bracken SC, Kilmartin C, Wieser H, Jackson J, Feighery C. Barley and rye prolamins induce an mRNA interferon-gamma response in coeliac mucosa. Aliment Pharmacol Ther 2006 23 : 1307 14.
28. Shan L, Marti T, Sollid LM, Gray GM, Khosla C. Comparative biochemical analysis of three bacterial prolyl endopeptidases: implications for coeliac sprue. Biochem J 2004 383 : 311 18.
29. Gass J, Ehren J, Strohmeier G, Isaacs I, Khosla C. Fermentation, purification, formulation, and pharmacological evaluation of a prolyl endopeptidase from Myxococcus xanthus: implications for celiac sprue therapy. Biotechnol Bioeng 2005 92 : 674 84.
30. Sollid LM, Khosla C. Future therapeutic options for celiac disease. Nat Clin Pract Gastroenterol Hepatol 2005 2 : 140 7.
31. Stepniak D, Spaenij-Dekking L, Mitea C et al. Highly efficient gluten degradation with a newly identified prolyl endoprotease: implications for celiac disease. Am J Physiol Gastrointest Liver Physiol 2006 291 : G621 9.
32. Siegel M, Bethune MT, Gass J et al. Rational design of combination enzyme therapy for celiac sprue. Chem Biol 2006 13 : 649 58.
33. Stenman SM, Venalainen JI, Lindfors K et al. Enzymatic detoxification of gluten by germinating wheat proteases: implications for new treatment of celiac disease. Ann Med 2009 41 : 390 400.
34. Gass J, Vora H, Bethune MT, Gray GM, Khosla C. Effect of barley endoprotease EP-B2 on gluten digestion in the intact rat. J Pharmacol Exp Ther 2006 318 : 1178 86.
35. Gass J, Bethune MT, Siegel M, Spencer A, Khosla C. Combination enzyme therapy for gastric digestion of dietary gluten in patients with celiac sprue. Gastroenterology 2007 133 : 472 80.
36. Tye-Din JA, Anderson RP, Ffrench RA et al. The effects of ALV003 pre-digestion of gluten on immune response and symptoms in celiac disease in vivo. Clin Immunol 2010 134 : 289 95.
37. Lindfors K, Blomqvist T, Juuti-Uusitalo K et al. Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture. Clin Exp Immunol 2008 152 : 552 8.
38. Arentz-Hansen H, Korner R, Molberg O et al. The intestinal T cell response to alpha-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J Exp Med 2000 191 : 603 12.
39. Li N, DeMarco VG, West CM, Neu J. Glutamine supports recovery from loss of transepithelial resistance and increase of permeability induced by media change in Caco-2 cells. J Nutr Biochem 2003 14 : 401 8.
40. Mitea C, Havenaar R, Drijfhout JW, Edens L, Dekking L, Koning F. Efficient degradation of gluten by a prolyl endoprotease in a gastrointestinal model: implications for coeliac disease. Gut 2008 57 : 25 32.
41. Matysiak-Budnik T, Candalh C, Cellier C et al. Limited efficiency of prolyl-endopeptidase in the detoxification of gliadin peptides in celiac disease. Gastroenterology 2005 129 : 786 96.
42. Ehren J, Moron B, Martin MT, Bethune E, Gray GM, Khosla C. A food-grade enzyme preparation with modest gluten detoxification properties. PLoS ONE 2009 4 : e6313.
43. Jung HC, Eckmann L, Yang SK et al. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 1995 95 : 55 65.
44. Bolte G, Osman A, Mothes T, Stern M. Peptic-tryptic digests of gliadin: contaminating trypsin but not pepsin interferes with gastrointestinal protein binding characteristics. Clin Chim Acta 1996 247 : 59 70.
45. Ciccocioppo R, Finamore A, Ara C, Di Sabatino A, Mengheri E, Corazza GR. Altered expression, localization, and phosphorylation of epithelial junctional proteins in celiac disease. Am J Clin Pathol 2006 125 : 502 11.
46. Barone MV, Gimigliano A, Castoria G et al. Growth factor-like activity of gliadin, an alimentary protein: implications for coeliac disease. Gut 2007 56 : 480 8.