Abrogation of Immunogenic Properties of Gliadin Peptides through Transamidation by Microbial Transglutaminase Is Acyl-Acceptor Dependent

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 34, 2017, Pages 7542-7552

  Zhou, Lin ^a,b   Kooy Winkelaar, Yvonne M C ^b   Cordfunke, Robert A ^b   Dragan, Irina ^b   Thompson, Allan ^b   Drijfhout, Jan Wouter ^b   Van Veelen, Peter A ^b   Chen, Hongbing ^a   Koning, Frits ^b  

^a NANCHANG UNIVERSITY   (China)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

acyl acceptor molecule; gliadin; immunogenic properties; microbial transglutaminase; transamidation

Indexed keywords

AMINO ACIDS; BAKERIES; CLONE CELLS; FOOD PRODUCTS; MOLECULES; PEPTIDES; T-CELLS;

ACYL ACCEPTOR; GLIADIN; IMMUNOGENIC PROPERTIES; MICROBIAL TRANSGLUTAMINASE; TRANSAMIDATION;

PROTEINS;

BACTERIAL PROTEIN; GLIADIN; GLUTEN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; TRANEXAMIC ACID;

BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; STREPTOMYCES; T LYMPHOCYTE;

BACTERIAL PROTEINS; BIOCATALYSIS; GLIADIN; GLUTENS; HUMANS; MOLECULAR STRUCTURE; STREPTOMYCES; T-LYMPHOCYTES; TRANEXAMIC ACID; TRANSGLUTAMINASES;

EID: 85028552528     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.7b02557     Document Type: Article

References (39)

1. Di Sabatino, A.; Corazza, G. R. Coeliac disease Lancet 2009, 373, 1480-1493 10.1016/S0140-6736(09)60254-3
2. Karell, K.; Louka, A. S.; Moodie, S. J.; Ascher, H.; Clot, F.; Greco, L.; Ciclitira, P. J.; Sollid, L. M.; Partanen, J.; Disease, E. G. C. o. C. HLA types in celiac disease patients not carrying the DQA1∗ 05-DQB1∗ 02 (DQ2) heterodimer: results from the European Genetics Cluster on Celiac Disease Hum. Immunol. 2003, 64, 469-477 10.1016/S0198-8859(03)00027-2
3. Petersen, J.; Kooy-Winkelaar, Y.; Loh, K. L.; Tran, M.; Van Bergen, J.; Koning, F.; Rossjohn, J.; Reid, H. H. Diverse T Cell Receptor Gene Usage in HLA-DQ8-Associated Celiac Disease Converges into a Consensus Binding Solution Structure 2016, 24, 1643-1657 10.1016/j.str.2016.07.010
4. Petersen, J.; Montserrat, V.; Mujico, J. R.; Loh, K. L.; Beringer, D. X.; Van Lummel, M.; Thompson, A.; Mearin, M. L.; Schweizer, J.; Kooy-Winkelaar, Y. T-cell receptor recognition of HLA-DQ2-gliadin complexes associated with celiac disease Nat. Struct. Mol. Biol. 2014, 21, 480-488 10.1038/nsmb.2817
5. Sollid, L. M.; Qiao, S.-W.; Anderson, R. P.; Gianfrani, C.; Koning, F. Nomenclature and listing of celiac disease relevant gluten T-cell epitopes restricted by HLA-DQ molecules Immunogenetics 2012, 64, 455-460 10.1007/s00251-012-0599-z
6. Qiao, S.-W.; Bergseng, E.; Molberg, Ø.; Xia, J.; Fleckenstein, B.; Khosla, C.; Sollid, L. M. Antigen presentation to celiac lesion-derived T cells of a 33-mer gliadin peptide naturally formed by gastrointestinal digestion J. Immunol. 2004, 173, 1757-1762 10.4049/jimmunol.173.3.1757
7. Shan, L.; Molberg, Ø.; 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 10.1126/science.1074129
8. Anderson, R. P.; Degano, P.; Godkin, A. J.; Jewell, D. P.; Hill, A. V. 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 10.1038/73200
9. Arentz-Hansen, H.; Körner, R.; Molberg, Ø.; Quarsten, H.; Vader, W.; Kooy, Y. M.; Lundin, K. E.; Koning, F.; Roepstorff, P.; Sollid, L. M. The intestinal T cell response to α-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase J. Exp. Med. 2000, 191, 603-612 10.1084/jem.191.4.603
10. Molberg, Ø.; McAdam, S.; Lundin, K. E.; Kristiansen, C.; Arentz-Hansen, H.; Kett, K.; Sollid, L. M. T cells from celiac disease lesions recognize gliadin epitopes deamidated in situ by endogenous tissue transglutaminase Eur. J. Immunol. 2001, 31, 1317-1323 10.1002/1521-4141(200105)31:5<1317::AID-IMMU1317>3.0.CO;2-I
11. Dekking, E.; Van Veelen, P.; De Ru, A.; Kooy-Winkelaar, E.; Gröneveld, T.; Nieuwenhuizen, W.; Koning, F. Microbial transglutaminases generate T cell stimulatory epitopes involved in celiac disease J. Cereal Sci. 2008, 47, 339-346 10.1016/j.jcs.2007.05.004
12. Kristiansen, C.; Madsen, L.; Fugger, L.; Scott, H.; Norén, O.; Roepstorff, P.; Lundin, K. E.; Sjöström, H.; Sollid, L. M. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease Nat. Med. 1998, 4, 713-717 10.1038/nm0698-713
13. van de Wal, Y.; Kooy, Y.; van Veelen, P.; Peña, S.; Mearin, L.; Papadopoulos, G.; Koning, F. Cutting edge: selective deamidation by tissue transglutaminase strongly enhances gliadin-specific T cell reactivity J. Immunol. 1998, 161, 1585-1588
14. Cabrera-Chávez, F.; Rouzaud-Sández, O.; Sotelo-Cruz, N.; Calderón de la Barca, A. M. Transglutaminase treatment of wheat and maize prolamins of bread increases the serum IgA reactivity of celiac disease patients J. Agric. Food Chem. 2008, 56, 1387-1391 10.1021/jf0724163
15. Ruh, T.; Ohsam, J. r.; Pasternack, R.; Yokoyama, K.; Kumazawa, Y.; Hils, M. Microbial transglutaminase treatment in pasta-production does not affect the immunoreactivity of gliadin with celiac disease patients' sera J. Agric. Food Chem. 2014, 62, 7604-7611 10.1021/jf501275c
16. Gianfrani, C.; Siciliano, R. A.; Facchiano, A. M.; Camarca, A.; Mazzeo, M. F.; Costantini, S.; Salvati, V. M.; Maurano, F.; Mazzarella, G.; Iaquinto, G. Transamidation of wheat flour inhibits the response to gliadin of intestinal T cells in celiac disease Gastroenterology 2007, 133, 780-789 10.1053/j.gastro.2007.06.023
17. Lombardi, E.; Bergamo, P.; Maurano, F.; Bozzella, G.; Luongo, D.; Mazzarella, G.; Aufiero, V. R.; Iaquinto, G.; Rossi, M. Selective inhibition of the gliadin-specific, cell-mediated immune response by transamidation with microbial transglutaminase J. Leukocyte Biol. 2013, 93, 479-488 10.1189/jlb.0412182
18. Elli, L.; Roncoroni, L.; Hils, M.; Pasternack, R.; Barisani, D.; Terrani, C.; Vaira, V.; Ferrero, S.; Bardella, M. T. Immunological effects of transglutaminase-treated gluten in coeliac disease Hum. Immunol. 2012, 73, 992-997 10.1016/j.humimm.2012.07.318
19. Mazzarella, G.; Salvati, V. M.; Iaquinto, G.; Stefanile, R.; Capobianco, F.; Luongo, D.; Bergamo, P.; Maurano, F.; Giardullo, N.; Malamisura, B. Reintroduction of gluten following flour transamidation in adult celiac patients: a randomized, controlled clinical study Clin. Dev. Immunol. 2012, 2012, 329150 10.1155/2012/329150
20. Heredia-Sandoval, N. G.; Islas-Rubio, A. R.; Cabrera-Chávez, F.; de la Barca, A. M. C. Transamidation of gluten proteins during the bread-making process of wheat flour to produce breads with less immunoreactive gluten Food Funct. 2014, 5, 1813-1818 10.1039/C4FO00118D
21. Ribeiro, M.; Nunes, F. M.; Guedes, S.; Domingues, P.; Silva, A. M.; Carrillo, J. M.; Rodriguez-Quijano, M.; Branlard, G.; Igrejas, G. Efficient chemo-enzymatic gluten detoxification: reducing toxic epitopes for celiac patients improving functional properties Sci. Rep. 2016, 5, 18041 10.1038/srep18041
22. Heil, A.; Ohsam, J.; Büchold, C.; Pasternack, R.; Yokoyama, K.; Kumazawa, Y.; Hils, M. Microbial transglutaminase has a lower deamidation preference than human tissue transglutaminase on a celiac disease relevant wheat gliadin T-cell epitope J. Cereal Sci. 2016, 70, 47-56 10.1016/j.jcs.2016.05.022
23. Gundersen, M. T.; Keillor, J. W.; Pelletier, J. N. Microbial transglutaminase displays broad acyl-acceptor substrate specificity Appl. Microbiol. Biotechnol. 2014, 98, 219-230 10.1007/s00253-013-4886-x
24. Ohtsuka, T.; Sawa, A.; Kawabata, R.; Nio, N.; Motoki, M. Substrate specificities of microbial transglutaminase for primary amines J. Agric. Food Chem. 2000, 48, 6230-6233 10.1021/jf000302k
25. Grossmann, I.; Döring, C.; Jekle, M.; Becker, T.; Koehler, P. Compositional changes and baking performance of rye dough as affected by microbial transglutaminase and xylanase J. Agric. Food Chem. 2016, 64, 5751-5758 10.1021/acs.jafc.6b01545
26. Zhou, L.; Wu, Y.; Cheng, Y.; Wang, J.; Lu, J.; Gao, J.; Yuan, J.; Chen, H. Blocking celiac antigenicity of the glutamine-rich gliadin 33-mer peptide by microbial transglutaminase RSC Adv. 2017, 7, 14438-14447 10.1039/C6RA27893K
27. Vader, L. W.; de Ru, A.; van der Wal, Y.; Kooy, Y. M.; Benckhuijsen, W.; Mearin, M. L.; Drijfhout, J. W.; van Veelen, P.; Koning, F. Specificity of tissue transglutaminase explains cereal toxicity in celiac disease J. Exp. Med. 2002, 195, 643-649 10.1084/jem.20012028
28. Meiring, H.; Van der Heeft, E.; Ten Hove, G.; De Jong, A. Nanoscale LC-MS (n): technical design and applications to peptide and protein analysis J. Sep. Sci. 2002, 25, 557-568 10.1002/1615-9314(20020601)25:9<557::AID-JSSC557>3.0.CO;2-F
29. Van De Wal, Y.; Kooy, Y. M.; Van Veelen, P. A.; Peña, S. A.; Mearin, L. M.; Molberg, Ø.; Lundin, K. E.; Sollid, L. M.; Mutis, T.; Benckhuijsen, W. E. Small intestinal T cells of celiac disease patients recognize a natural pepsin fragment of gliadin Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 10050-10054 10.1073/pnas.95.17.10050
30. Vader, W.; Kooy, Y.; van Veelen, P.; de Ru, A.; Harris, D.; Benckhuijsen, W.; Peña, S.; Mearin, L.; Drijfhout, J. W.; Koning, F. The gluten response in children with celiac disease is directed toward multiple gliadin and glutenin peptides Gastroenterology 2002, 122, 1729-1737 10.1053/gast.2002.33606
31. Ho, M. L.; Leu, S. Z.; Hsieh, J. F.; Jiang, S. T. Technical approach to simplify the purification method and characterization of microbial transglutaminase produced from Streptoverticillium ladakanum J. Food Sci. 2000, 65, 76-80 10.1111/j.1365-2621.2000.tb15959.x
32. Pellegrini, N.; Agostoni, C. Nutritional aspects of gluten-free products J. Sci. Food Agric. 2015, 95, 2380-2385 10.1002/jsfa.7101
33. Theethira, T. G.; Dennis, M.; Leffler, D. A. Nutritional consequences of celiac disease and the gluten-free diet Expert Rev. Gastroenterol. Hepatol. 2014, 8, 123-129 10.1586/17474124.2014.876360
34. Gulati, P.; Li, A.; Holding, D.; Santra, D.; Zhang, Y.; Rose, D. J. Heating Reduces Proso Millet Protein Digestibility via Formation of Hydrophobic Aggregates J. Agric. Food Chem. 2017, 65, 1952-1959 10.1021/acs.jafc.6b05574
35. Stamnaes, J.; Fleckenstein, B.; Sollid, L. M. The propensity for deamidation and transamidation of peptides by transglutaminase 2 is dependent on substrate affinity and reaction conditions Biochim. Biophys. Acta, Proteins Proteomics 2008, 1784, 1804-1811 10.1016/j.bbapap.2008.08.011
36. Roy, I.; Smith, O.; Clouthier, C. M.; Keillor, J. W. Expression, purification and kinetic characterisation of human tissue transglutaminase Protein Expression Purif. 2013, 87, 41-46 10.1016/j.pep.2012.10.002
37. Heil, A.; Weber, J.; Büchold, C.; Pasternack, R.; Hils, M. Differences in the inhibition of coagulation factor XIII-A from animal species revealed by Michael Acceptor-and thioimidazol based blockers Thromb. Res. 2013, 131, e214-e222 10.1016/j.thromres.2013.02.008
38. Pérot, M.; Lupi, R.; Guyot, S.; Delayre-Orthez, C.; Gadonna-Widehem, P.; Thébaudin, J.-Y.; Bodinier, M.; Larré, C. Polyphenol Interactions Mitigate the Immunogenicity and Allergenicity of Gliadins J. Agric. Food Chem. 2017, 65, 6442-6451 10.1021/acs.jafc.6b05371
39. Berti, C.; Roncoroni, L.; Falini, M. L.; Caramanico, R.; Dolfini, E.; Bardella, M. T.; Elli, L.; Terrani, C.; Forlani, F. Celiac-related properties of chemically and enzymatically modified gluten proteins J. Agric. Food Chem. 2007, 55, 2482-2488 10.1021/jf062623n