Biochemical modifications of gliadins induced by microbial transglutaminase on wheat flour

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 11, 2013, Pages 5166-5174

  Mazzeo, Maria F ^a   Bonavita, Roberta ^a   Maurano, Francesco ^a   Bergamo, Paolo ^a   Siciliano, Rosa A ^a   Rossi, Mauro ^a  

^a CNR   (Italy)

Author keywords

Celiac disease; Gliadin; Microbial transglutaminase; Transamidation

Indexed keywords

EPITOPE; GLIADIN; GLIADIN ANTIBODY; GLUTENIN; MICROBIAL TRANSGLUTAMINASE; PEPTIDE; PEPTIDE[31-49]; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; TISSUE TRANSGLUTAMINASE; UNCLASSIFIED DRUG;

AMIDATION; ARTICLE; BREAD; CONTROLLED STUDY; CROSS REACTION; ENZYME ACTIVITY; ENZYME SPECIFICITY; FLOUR; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN MODIFICATION; TRANSAMIDATION; WHEAT;

TRITICUM AESTIVUM;

CD; CELIAC DISEASE; GFD; GLIADIN; GLUTEN-FREE DIET; INSOLUBLE TRANSAMIDATED GLIADIN; K-C(2)H(5); K-GLIADINS; LYSINE ETHYL ESTER; MICROBIAL TRANSGLUTAMINASE; MTGASE; NANO-HPLC-ESI-MS/MS; PEPS; PROLYL ENDOPEPTIDASES; SPF; TANDEM MASS SPECTROMETRY COUPLED WITH NANO-REVERSE PHASE LIQUID CHROMATOGRAPHY; TISSUE TRANSGLUTAMINASE; TRANSAMIDATION; TTGASE; WATER-SOLUBLE PROTEIN FRACTION;

AMINO ACID SEQUENCE; CACO-2 CELLS; CELL LINE, TUMOR; FLOUR; GLIADIN; GLUTENS; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; TRANSGLUTAMINASES; TRITICUM;

EID: 84881536097     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.07.021     Document Type: Article

References (36)

1. A. Di Sabatino, and G.R. Corazza Coeliac disease Lancet 373 2009 1480 1493
2. P.H. Green, and C. Cellier Celiac disease N. Engl. J. Med. 357 2007 1731 1743
3. O. Molberg, S.N. McAdam, R. Korner, H. Quarsten, C. Kristiansen, L. Madsen, L. Fugger, H. Scott, O. Norén, P. Roepstorff, K.E. Lundin, H. Sjöström, and L.M. Sollid Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease Nat. Med. 4 1998 713 717 (Pubitemid 28274673)
4. L. Shan, O. Molberg, I. Parrot, F. Hausch, F. Filiz, G.M. Gray, L.M. Sollid, and C. Khosla Structural basis for gluten intolerance in celiac sprue Science 297 2002 2275 2279
5. L. Shan, T. Marti, L.M. Sollid, G.M. Gray, and C. Khosla Comparative biochemical analysis of three bacterial prolyl endopeptidases: implications for coeliac sprue Biochem. J. 383 2004 311 318 (Pubitemid 39446692)
6. L. Greco, M. Gobbetti, R. Auricchio, R. Di Mase, F. Landolfo, F. Paparo, R. Di Cagno, M. De Angelis, C.G. Rizzello, A. Cassone, G. Terrone, L. Timpone, M. D'Aniello, M. Maglio, R. Troncone, and S. Auricchio Safety for patients with celiac disease of baked goods made of wheat flour hydrolyzed during food processing Clin. Gastroenterol. Hepatol. 9 2011 24 29
7. T. Kanaji, H. Ozaki, T. Takao, H. Kawajiri, H. Ide, M. Motoki, and Y. Shimonishi Primary structure of microbial transglutaminase from Streptoverticillium sp. strain s-8112 J. Biol. Chem. 668 1993 11565 11572 (Pubitemid 23168101)
8. K. Yokoyama, N. Nio, and Y. Kikuchi Properties and applications of microbial transglutaminase Appl. Microbiol. Biotechnol. 64 2004 447 454 (Pubitemid 38686152)
9. K. Iwami, and K. Yasumoto Amine-binding capacities of food proteins in transglutaminase reaction and digestibility of wheat gliadin with Ïμ-attached lysine J. Sci. Food Agric. 37 1986 495 503
10. M.L. Fink, S.I. Chung, and J.E. Folk Gamma-glutamylamine cyclotransferase: specificity toward epsilon-(L-gamma-glutamyl)-L-lysine and related compounds Proc. Natl. Acad. Sci. U. S. A. 77 1980 4564 4568
11. C. Gianfrani, R.A. Siciliano, A.M. Facchiano, A. Camarca, M.F. Mazzeo, S. Costantini, V.M. Salvati, F. Maurano, G. Mazzarella, G. Iaquinto, P. Bergamo, and M. Rossi Transamidation of wheat flour inhibits the response to gliadin of intestinal T cells in celiac disease Gastroenterology 133 2007 780 789 (Pubitemid 47374136)
12. E. Lombardi, F. Maurano, P. Bergamo, G. Bozzella, D. Luongo, G. Mazzarella, F. Capobianco, V. Aufiero Rotondi, G. Iaquinto, and M. Rossi Selective inhibition of gliadin immune reactivity by transamidation of wheat flour with microbial transglutaminase J. Leukoc. Biol. 93 2013 479 488
13. H. Arentz-Hansen, R. Körner, O. Molberg, H. Quarsten, W. Vader, Y.M. Kooy, K.E. Lundin, F. Koning, P. Roepstorff, L.M. Sollid, and S.N. McAdam 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. 191 2000 603 612
14. S.W. Qiao, E. Bergseng, O. Molberg, J. Xia, B. Fleckenstein, C. Khosla, and L.M. Sollid Antigen presentation to celiac lesion-derived T cells of a 33-mer gliadin peptide naturally formed by gastrointestinal digestion J. Immunol. 173 2004 1757 1762 (Pubitemid 38971607)
15. S. Dørum, M.O. Arntzen, S.W. Qiao, A. Holm, C.J. Koehler, B. Thiede, L.M. Sollid, and B. Fleckenstein The preferred substrates for transglutaminase 2 in a complex wheat gluten digest are peptide fragments harboring celiac disease T-cell epitopes PLoS One 5 2010 e14056
16. P.L. Weegels, R.J. Hamer, and J.D. Schofield RP-HPLC and capillary electrophoresis of subunits from glutenin isolated by SDS and Osborne fractionation J. Cereal Sci. 22 1995 211 224
17. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
18. R.G.K. Leuschner, J.A.M. O'Callaghan, and E.K. Arendt Optimization of baking parameters of part-baked and rebaked Irish brown soda bread by evaluation of some quality characteristics Int. J. Food Sci. Technol. 32 1997 487 493 (Pubitemid 127388177)
19. A.A. Osman, H.H. Uhlig, I. Valdes, M. Amin, E. Méndez, and T. Mothes A monoclonal antibody that recognizes a potential coeliac-toxic repetitive pentapeptide epitope in gliadins Eur. J. Gastroenterol. Hepatol. 13 2001 1189 1193 (Pubitemid 33015885)
20. E. Garcia, M. Llorente, A. Hernando, R. Kieffer, H. Wieser, and E. Mendez Development of a general procedure for complete extraction of gliadins for heat processed and unheated foods Eur. J. Gastroenterol. Hepatol. 17 2005 529 539 (Pubitemid 40592711)
21. L. Maiuri, C. Ciacci, I. Ricciardelli, L. Vacca, V. Raia, S. Auricchio, J. Picard, M. Osman, S. Quaratino, and M. Londei Association between innate response to gliadin and activation of pathogenic T cells in coeliac disease Lancet 362 2003 30 37 (Pubitemid 36835817)
22. J.E. Folk, and J.S. Finlayson The Ïμ-(γ-glutamyl) lysine cross-link and the catalytic role of transglutaminases Adv. Protein Chem. 31 1977 1 133
23. K. Mehta, and R. Eckert Family of Enzymes with Diverse Functions, Progress in Tumor Research Vol. 38 2005 Karger Basel
24. 2 + mobilization in Caco-2 cells PLoS One 7 2012 e45209
25. J.A. Tye-Din, J.A. Stewart, J.A. Dromey, T. Beissbarth, D.A. van Heel, A. Tatham, K. Henderson, S.I. Mannering, C. Gianfrani, D.P. Jewell, A.V. Hill, J. McCluskey, J. Rossjohn, and R.P. Anderson Comprehensive, quantitative mapping of T cell epitopes in gluten in celiac disease Sci. Transl. Med. 2 2010 41 51
26. L.M. Sollid Coeliac disease: dissecting a complex inflammatory disorder Nat. Rev. Immunol. 9 2002 647 655 (Pubitemid 37328722)
27. 2 +-independent transglutaminase derived from microorganisms Agric. Biol. Chem. 53 1989 2619 2623 (Pubitemid 20077526)
28. R. Pasternack, S. Dorsch, J.T. Otterbach, I.R. Robenek, S. Wolf, and H.L. Fuchsbauer Bacterial pro-transglutaminase from Streptoverticillium mobaraense - purification, characterisation and sequence of the zymogen Eur. J. Biochem. 257 1998 570 576 (Pubitemid 28512124)
29. C.W. Wrigley, and J.A. Bietz Wheat - Chemistry and Technology Y. Pomeranz, 1988 St. Paul American Association of Cereal Chemistry 159 275
30. H. Wieser, W. Bushuk, and F. MacRitchie Gliadin and Glutenin: The Unique Balance of Wheat Quality C. Wrigley, F. Bekes, W. Bushuk, 2006 St. Paul American Association of Cereal Chemistry Minnesota 213 240
31. A.K. Moustakas, Y. van de Wal, J. Routsias, Y.M. Kooy, P. van Veelen, J.W. Rrjfhout, F. Koning, and G.K. Papadopoulos Structure of celiac disease-associated HLA-DQ8 and nonassociated HLA-DQ9 alleles in complex with two disease-specific epitopes Int. Immunol. 12 2000 1157 1166 (Pubitemid 30616221)
32. J. Xia, L.M. Sollid, and C. Khosla Equilibrium and kinetic analysis of the unusual binding behavior of a highly immunogenic gluten peptide to HLA-DQ2 Biochemistry 44 2005 4442 4449 (Pubitemid 40403986)
33. G. Mazzarella, V.M. Salvati, G. Iaquinto, R. Stefanile, F. Capobianco, D. Luongo, P. Bergamo, F. Maurano, N. Giardullo, B. Malamisura, and M. Rossi Reintroduction of gluten following flour transamidation in adult celiac patients: a randomized, controlled clinical study Clin. Dev. Immunol. 2012 2012 329150
34. S. Hu, J.-J. Mention, R.C. Monteiro, S.L. Zhang, C. Cellier, J. Schmitz, V. Verkarre, N. Fodil, S. Bahram, N. Cerf-Bensussan, and S. Caillat-Zucman A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease Immunity 21 2004 367 377 (Pubitemid 39208338)
35. M.V. Barone, D. Zanzi, M. Maglio, M. Nanayakkara, S. Santagata, G. Lania, E. Miele, M.T. Ribecco, F. Maurano, R. Auricchio, C. Gianfrani, S. Ferrini, R. Troncone, and S. Auricchio Gliadin-mediated proliferation and innate immune activation in celiac disease are due to alterations in vesicular trafficking PLoS One 6 2011 e17039
36. M.P. Lindsay, and J.H. Skerritt The glutenin macropolymer of wheat flour doughs: structure and function perspectives Trends Food Sci. Technol. 10 1999 247 253 (Pubitemid 30146746)