Enzymatic detoxification of gluten by germinating wheat proteases: Implications for new treatment of celiac disease

Annals of Medicine

Volumn 41, Issue 5, 2009, Pages 390-400

  Stenman, Satumarja M ^a   Venäläinen, Jarkko I ^b   Lindfors, Katri ^a   Auriola, Seppo ^b   Mauriala, Timo ^c   Kaukovirta Norja, Anu ^d   Jantunen, Anna ^b   Laurila, Kaija ^a   Qiao, Shuo Wang ^e   Sollid, Ludvig M ^e   Männistö, Pekka T ^c   Kaukinen, Katri ^a,f   Mäki, Markku ^a,f  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^e OSLO UNIVERSITY HOSPITAL   (Norway)

^f TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

Celiac disease; Germinating wheat enzymes; Gluten; Organ culture; Permeability

Indexed keywords

ACTIN; AUTOANTIBODY; GLIADIN; PEPSIN A; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2 ANTIBODY; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE ANTIBODY; PROTEIN ZO1; PROTEINASE; TRYPSIN; UNCLASSIFIED DRUG; PEPTIDE HYDROLASE;

ADOLESCENT; ADULT; AGED; ANTIBODY PRODUCING CELL; ARTICLE; CD25+ T LYMPHOCYTE; CELIAC DISEASE; CELL DENSITY; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENZYMATIC DEGRADATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE BIOPSY; LYMPHOCYTE PROLIFERATION; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TIGHT JUNCTION; WHEAT; BIOPSY; COMPARATIVE STUDY; DRUG DETOXIFICATION; DRUG EFFECT; ENZYMOLOGY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROGNOSIS; SMALL INTESTINE;

ADOLESCENT; ADULT; AGED; BIOPSY; CACO-2 CELLS; CELIAC DISEASE; CELL MEMBRANE PERMEABILITY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; GLIADIN; HUMANS; INTESTINE, SMALL; MALE; METABOLIC DETOXICATION, DRUG; MIDDLE AGED; PEPTIDE HYDROLASES; PROGNOSIS; T-LYMPHOCYTES; TRITICUM; YOUNG ADULT;

EID: 67449099537     PISSN: 07853890     EISSN: 13652060     Source Type: Journal    
DOI: 10.1080/07853890902878138     Document Type: Article

References (40)

1. Fasano A, Berti I, Gerarduzzi T, Not T, Colletti RB, Drago S, et al. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States: a large multicenter study. Arch Intern Med. 2003;163:286-292
2. Bruce G, Woodley JF, Swan CH. Breakdown of gliadin peptides by intestinal brush borders from coeliac patients. Gut. 1984;25:919-924
3. Shan L, Molberg O, Parrot I, Hausch F, Filiz F, Gray GM, et al. Structural basis for gluten intolerance in celiac sprue. Science. 2002;297:2275-2279
4. Garcia-Horsman JA, Venalainen JI, Lohi O, Auriola IS, Korponay-Szabo IR, Kaukinen K, et al. Deficient activity of mammalian prolyl oligopeptidase on the immunoactive peptide digestion in coeliac disease. Scand J Gastroenterol. 2007;42:562-571
5. de Ritis G, Auricchio S, Jones HW, Lew EJ, Bernardin JE, Kasarda DD. In vitro (organ culture) studies of the toxicity of specific A-gliadin peptides in celiac disease. Gastroenterology. 1988;94:41-49
6. Sturgess R, Day P, Ellis HJ, Lundin KE, Gjertsen HA, Kontakou M, et al. Wheat peptide challenge in coeliac disease. Lancet. 1994;343:758-761
7. 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;6:337-342
8. Maiuri L, Ciacci C, Ricciardelli I, Vacca L, Raia V, Auricchio S, et al. Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease. Lancet. 2003;362:30-37
9. Sollid LM. Molecular basis of celiac disease. Annu Rev Immunol. 2000;18:53-81.
10. Bethune MT, Khosla C. Parallels between pathogens and gluten peptides in celiac sprue. PLoS Pathog. 2008;4:e34.
11. Lammers KM, Lu R, Brownley J, Lu B, Gerard C, Thomas K, 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.
12. Lee A, Newman JM. Celiac diet: its impact on quality of life. J Am Diet Assoc. 2003;103:1533-1535
13. Xia J, Bergseng E, Fleckenstein B, Siegel M, Kim CY, Khosla C, et al. Cyclic and dimeric gluten peptide analogues inhibiting DQ2-mediated antigen presentation in celiac disease. Bioorg Med Chem. 2007;15:6565-6573
14. Chaudhary R, Ghosh S. Infliximab in refractory coeliac disease. Eur J Gastroenterol Hepatol. 2005;17:603-.
15. Sollid LM, Khosla C. Future therapeutic options for celiac disease. Nat Clin Pract Gastroenterol Hepatol. 2005;2: 140-147
16. Benahmed M, Meresse B, Arnulf B, Barbe U, Mention JJ, Verkarre V, et al. Inhibition of TGF-beta signaling by IL-15: a new role for IL-15 in the loss of immune homeostasis in celiac disease. Gastroenterology. 2007;132:994-1008.
17. Maurano F, Siciliano RA, De Giulio B, Luongo D, Mazzeo MF, Troncone R, et al. Intranasal administration of one alpha gliadin can downregulate the immune response to whole gliadin in mice. Scand J Immunol. 2001;53:290-295
18. Anderson RP, ed. Development of a vaccine for celiac disease. Frontiers in celiac disease. Pediatric and adolescent medicine. Vol 12. Basel, Switzerland: Karger; 2008.
19. Clemente MG, De Virgiliis S, Kang JS, Macatagney R, Musu MP, Di Pierro MR, et al. Early effects of gliadin on enterocyte intracellular signalling involved in intestinal barrier function. Gut. 2003;52:218-223
20. Paterson BM, Lammers KM, Arrieta MC, Fasano A, Meddings JB. The safety, tolerance, pharmacokinetic and pharmacodynamic effects of single doses of AT-1001 in coeliac disease subjects: a proof of concept study. Aliment Pharmacol Ther. 2007;26:757-766
21. Hausch F, Halttunen T, Maki M, Khosla C. Design, synthesis, and evaluation of gluten peptide analogs as selective inhibitors of human tissue transglutaminase. Chem Biol. 2003;10:225-231
22. Siegel M, Khosla C. Transglutaminase 2 inhibitors and their therapeutic role in disease states. Pharmacol Ther. 2007; 115:232-245
23. Matysiak-Budnik T, Candalh C, Cellier C, Dugave C, Namane A, Vidal-Martinez T, et al. Limited efficiency of prolyl-endopeptidase in the detoxification of gliadin peptides in celiac disease. Gastroenterology. 2005;129:786-796
24. Pyle GG, Paaso B, Anderson BE, Allen DD, Marti T, Li Q, et al. Effect of pretreatment of food gluten with prolyl endopeptidase on gluten-induced malabsorption in celiac sprue. Clin Gastroenterol Hepatol. 2005;3:687-694
25. 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;383:311-318
26. 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;92:674-684
27. Stepniak D, Spaenij-Dekking L, Mitea C, Moester M, de Ru A, Baak-Pablo R, 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.
28. 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.
29. 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;133:472-480
30. Simpson DJ. Proteolytic degradation of cereal prolamins* the problem with proline. Plant Science. 2001;161:825-838
31. Lindfors K, Blomqvist T, Juuti-Uusitalo K, Stenman S, Venalainen J, Maki M, et al. Live probiotic Bifidobacterium lactis bacteria inhibit the toxic effects induced by wheat gliadin in epithelial cell culture. Clin Exp Immunol. 2008;152:552-558
32. Barone MV, Gimigliano A, Castoria G, Paolella G, Maurano F, Paparo F, et al. Growth factor-like activity of gliadin, an alimentary protein: implications for coeliac disease. Gut. 2007;56:480-488
33. Molberg O, McAdam SN, Korner R, Quarsten H, Kristian-sen C, Madsen L, et al. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat Med. 1998;4:713-717
34. Qiao SW, Bergseng E, Molberg O, Jung G, Fleckenstein B, Sollid LM. Refining the rules of gliadin T cell epitope binding to the disease-associated DQ2 molecule in celiac disease: importance of proline spacing and glutamine deamidation. J Immunol. 2005;175:254-261
35. Stenman SM, Lindfors K, Korponay-Szabo IR, Lohi O, Saavalainen P, Partanen J, 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.
36. 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;14:401-408
37. Cerf-Bensussan N, Matysiak-Budnik T, Cellier C, Heyman M. Oral proteases: a new approach to managing coeliac disease. Gut. 2007;56:157-160
38. Laitila A, Kotaviita E, Peltola P, Home S, Wilhelmson A. Indigenous microbial community of barley greatly influences grain germination and malt quality. J Inst Brew. 2007;113: 9-20.
39. Hartmann G, Koehler P, Wieser H. Rapid degradation of gliadin peptides toxic for celiac disease patients by proteases from germinating cereals. J Cereal Sci. 2006;44:368-371
40. Siegel M, Bethune MT, Gass J, Ehren J, Xia J, Johannsen A, et al. Rational design of combination enzyme therapy for celiac sprue. Chem Biol. 2006;13:649-658