Release of wheat gluten exorphins A5 and C5 during in vitro gastrointestinal digestion of bread and pasta and their absorption through an in vitro model of intestinal epithelium

Food Research International

Volumn 72, Issue , 2015, Pages 208-214

  Stuknyte, Milda ^a   Maggioni, Margherita ^a   Cattaneo, Stefano ^a   De Luca, Paola ^a   Fiorilli, Amelia ^a   Ferraretto, Anita ^a   De Noni, Ivano ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Bioavailabilty; Bread; Caco 2 HT 29 co culture; Gluten exorphins; In vitro digestion; Pasta

Indexed keywords

PEPTIDES;

BIOAVAILABILTY; BREAD; CO-CULTURES; GLUTEN EXORPHINS; IN-VITRO DIGESTIONS; PASTA;

FOOD PRODUCTS;

TRITICUM AESTIVUM;

EID: 84927700961     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2015.04.002     Document Type: Article

References (59)

1. Artemova N.V., Bumagina Z.M., Kasakov A.S., Shubin V.V., Gurvits B.Ya. Opioid peptides derived from food proteins suppress aggregation and promote reactivation of partly unfolded stressed proteins. Peptides 2010, 31:332-338.
2. Camargo A.C.M., Fernandes B.L., Cruz L., Ferro E.S. Bioactive peptides produced by limited proteolysis. Colloquium Series on Neuropeptides 2012, 1:1-92.
3. Cavazos A., de Mejia E.G. Identification of bioactive peptides from cereal storage proteins and their potential role in prevention of chronic diseases. Comprehensive Reviews in Food Science and Food Safety 2013, 12:364-380.
4. Ćirković Veličković T., Gavrović-Jankulović M. Intestinal permeability and transport of food antigens. Biochemistry and Molecular Nutrition 2014, 29-56. Springer, New York.
5. Czaja-Bulsa G. Non coeliac gluten sensitivity - A new disease with gluten intolerance. Clinical Nutrition 2015, 34:189-194. 10.1016/j.clnu.2014.08.012.
6. De Luca P., Arnaboldi F., Maggioni M., Cornaghi L., Fiorilli A., Donetti E., et al. Co-cultures of Caco2 and HT-29 cells: a versatile in vitro model of human intestinal epithelium 2015, (unpublished).
7. de Magistris L., Piccardi A., Sapone A., Cariello R., Siniscalco D., Bravaccio C., et al. Intestinal barrier in autism. Comprehensive Guide to Autism 2014, 2047-2060. Springer, New York. V.B. Patel, V.R. Preedy, C.R. Martin (Eds.).
8. de Punder K., Pruimboom L. The dietary intake of wheat and other cereal grains and their role in inflammation. Nutrients 2013, 5:771-787.
9. del Mar Contreras M., Sancho A.I., Recio I., Mills C. Absorption of casein antihypertensive peptides through an in vitro model of intestinal epithelium. Food Digestion 2012, 3:16-24.
10. Ertay T., Ünak P., Tasci C., Zihnioğlu F., Durak H. Scintigraphic imaging with 99mTc-exorphin C in rabbits. Applied Radiation & Isotopes 2005, 62:883-888.
11. Fanciulli G., Azara E., Wood T.D., Dettori A., Delitala G., Marchetti M. Quantification of gluten exorphin A5 in cerebrospinal fluid by liquid chromatography-mass spectrometry. Journal of Chromatography B - Analytical Technologies in the Biomedical and Life Sciences 2006, 833:204-209.
12. Fanciulli G., Dettori A., Demontis M.P., Tomasi P.A., Anania V., Delitala G. Gluten exorphin B5 stimulates prolactin secretion through opioid receptors located outside the blood-brain barrier. Life Sciences 2005, 76:1713-1719.
13. Fanciulli G., Dettori A., Fenude E., Demontis M.P., Alberico E., Delitala G., et al. Intravenous administration of the food-derived opioid peptide gluten exorphin B5 stimulates prolactin secretion in rats. Pharmacological Research 2003, 47:53-58.
14. Fanciulli G., Dettori A., Tomasi P.A., Demontis M.P., Gianorso S., Anania V., et al. Prolactin and growth hormone response to intracerebroventricular administration of the food opioid peptide gluten exorphin B5 in rats. Life Sciences 2002, 71:2383-2390.
15. Fleisher D. Biological transport phenomena in the gastrointestinal tract. Transport Processes in Pharmaceutical Systems 2000, 147-184. Marcel Dekker, New York. G.L. Amidon, P.I. Lee, E.M. Topp (Eds.).
16. Fogh J., Fogh J.M., Orfeo T. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. Journal of the National Cancer Institute 1977, 59:221-226. 221-226.
17. Foltz M., Cerstiaens A., van Meensel A., Mols R., van der Pijl P.C., Duchateau G.S.M.J.E., et al. The angiotensin converting enzyme inhibitory tripeptides Ile-Pro-Pro and Val-Pro-Pro show increasing permeabilities with increasing physiological relevance of absorption models. Peptides 2008, 29:1312-1320.
18. Fukudome S., Jinsmaa Y., Matsukawa T., Sasaki R., Yoshikawa M. Release of opioid peptides, gluten exorphins by the action of pancreatic elastase. FEBS Letters 1997, 412:475-479.
19. Fukudome S., Shimatsu A., Suganuma H., Yoshikawa M. Effect of gluten exorphins A5 and B5 on 450 the postprandial plasma insulin level in conscious rats. Life Sciences 1995, 57:729-734.
20. Fukudome S., Yoshikawa M. Opioid peptides derived from wheat gluten: their isolation and characterization. FEBS Letters 1992, 296:107-111.
21. Hilgendorf C., Spahn-Langguth H., Regardh C.G., Lipka E., Amidon G.L., Langguth P. Caco-2 versus Caco-2/HT29-MTX co-cultured cell lines: Permeabilities via diffusion, inside- and outside-directed carrier-mediated transport. Journal of Pharmaceutical Sciences 2000, 89:63-75.
22. Hilgers A.R., Conradi R.A., Burton P.S. Caco-2 cell monolayers as a model for drug transport across the intestinal mucosa. Pharmaceutical Research 1990, 7:902-910.
23. Huet C., Sahuquillo-Merino C., Coudrier E., Louvard D. Absorptive and mucus-secreting subclones isolated from a multipotent intestinal cell line (HT-29) provide new models for cell polarity and terminal differentiation. The Journal of Cell Biology 1987, 105:345-357.
24. Iacomino G., Fierro O., D'Auria S., Picariello G., Ferranti P., Liguori C., et al. Structural analysis and Caco-2 cell permeability of the celiac-toxic α-gliadin peptide 31-55. Journal of Agricultural and Food Chemistry 2013, 61:1088-1096.
25. LARN Recommended dietary level of energy and nutrients for Italian population (LARN) 2014, Editorial coordination SINU-INRAN. Milan, SICS. 4th ed.
26. Lesuffleur T., Barbat A., Luccioni C., Beaumatin J., Clair M., Kornowski A., et al. Dihydrofolate reductase gene amplification-associated shift of differentiation in methotrexate-adapted HT-29 cells. The Journal of Cell Biology 1991, 115:1409-1418.
27. Mahler G.J., Shuler M.L., Glahn R.P. Characterization of Caco-2 and HT29-MTX cocultures in an in vitro digestion/cell culture model used to predict iron bioavailability. Journal of Nutritional Biochemistry 2009, 20:494-502.
28. Ménard S., Lebreton C., Schumann M., Matysiak-Budnik T., Dugave C., Bouhnik Y., et al. Paracellular versus transcellular intestinal permeability to gliadin peptides in active celiac disease. The American Journal of Pathology 2012, 18:608-615.
29. Minekus M., Alminger M., Alvito P., Ballance S., Bohn T., Bourlieu C., et al. A standardized static in-vitro digestion method suitable for food - An international consensus. Food & Function 2014, 5:1113-1124.
30. Mulloy A., Lang R., O'Reilly M., Sigafoos J., Lancioni G., Rispoli M. Gluten-free and casein-free diets in the treatment of autism spectrum disorders: A systematic review. Research in Autism Spectrum Disorders 2010, 4:328-339.
31. Pennington C.L., Dufresne C.P., Fanciulli G., Wood T.D. Detection of Gluten exorphin B4 and B5 in human blood by liquid chromatography-mass spectrometry/mass spectrometry. Open Spectroscopy Journal 2007, 1:9-16.
32. Petitot M., Brossard C., Barron C., Larre C., Morel M.H., Micard V. Modification of pasta structure induced by high drying temperatures. Effects on the in vitro digestibility of protein and starch fractions and the potential allergenicity of protein hydrolysates. Food Chemistry 2009, 116:401-412.
33. Pinto M., Robine-Leon S., Appay M.D., Kedinger M., Triadou N., Dussaulx E., et al. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. BioIogy of the Cell 1983, 47:323-330.
34. Pontier C., Pachot J., Botham R., Lenfant B., Arnaud P. HT29-MTX and Caco-2/TC7 monolayers as predictive models for human intestinal absorption: Role of the mucus layer. Journal of Pharmaceutical Sciences 2001, 90:1608-1619.
35. Reichelt K.L., Ekrem J., Scott H. Gluten, milk proteins and autism: Dietary intervention effects on behavior and peptide secretion. Journal of Applied Nutrition 1990, 42:1-11.
36. Reichelt K.L., Knivsberg A.M., Nødland M., Lind G. Nature and consequences of hyperpeptiduria and bovine casomorphins found in autistic syndromes. Developmental Brain Dysfunction 1994, 7:71-85.
37. Reissmann A., Hauser J., Makulska-Gertruda E., Tom L., Lange K.W. Gluten-free and casein-free diets in the treatment of autism. Functional Foods in Health & Disease 2014, 4:349-361.
38. 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. Biochimica et Biophysica Acta - Molecular Basis of Disease 1999, 1:152-160.
39. Satake M., Enjoh M., Nakamura Y., Takano T., Kawamura Y., Arai S., et al. Transepithelial transport of the bioactive tripeptide, Val-Pro-Pro, in human intestinal Caco-2 cell monolayers. Bioscience, Biotechnology, and Biochemistry 2002, 66:378-384.
40. Seiquer I., Diaz-Alguacil J., Delgado-Andrade C., Lopez-Frias M., Munoz Hoyos A., Galdo G., et al. Diets rich in Maillard Reaction products affect protein digestibility in adolescent males aged 11-14year. American Journal of Nutrition 2006, 83:1082-1088.
41. Shan L., Molberg Ø., Parrot I., Hausch F., Filiz F., Gray G.M., et al. Structural basis for gluten intolerance in celiac sprue. Science 2002, 297:2275-2279.
42. Shan L., Qiao S.-W., Arentz-Hansen H., Molberg Ø., Gray G.M., Sollid L.M., et al. Identification and analysis of multivalent proteolytically resistant peptides from gluten: implications for celiac sprue. Journal of Proteome Research 2005, 4:1732-1741.
43. Shewry P.R., Halford N.G., Belton P.S., Tatham A.S. The structure and properties of gluten: An elastic protein from wheat grain. Philosophical Transactions of the Royal Society of London B 2002, 357:133-142.
44. Shimizu M. Interaction between food substance and the intestinal epithelium. Bioscience, Biotechnology, and Biochemistry 2010, 74:232-241.
45. Shimizu M., Ok Son D. Food-derived peptides and intestinal functions. Current Pharmaceutical Design 2007, 13:885-895.
46. Stuknyte M., Cattaneo S., Pagani M.A., Marti A., Micard V., Hogenboom J., et al. Spaghetti from durum wheat: Effect of drying conditions on heat damage, ultrastructure and in vitro digestibility. Food Chemistry 2014, 149:40-46.
47. Sun Z., Cade R. Findings in normal rats following administration of gliadorphin-7 (GD-7). Peptides 2003, 24:321-323.
48. Takahashi M., Fukunaga H., Kaneto H., Fukudome S., Yoshikawa M. Behavioral and 535 pharmacological studies on gluten exorphin A5, a newly isolated bioactive food protein fragm536 in mice. Japanese Journal of Pharmacology 2000, 84:259-265.
49. Tanabe S., Arai S., Yanagihara Y., Mita H., Takahashi K., Watanabe M. A major wheat allergen has a Gln-Gln-Gln-Pro-Pro motif identified as an IgE-binding epitope. Biochemical and Biophysical Research Communications 1996, 219:290-293.
50. Teschemacher H. Opioid receptor ligands derived from food proteins. Current Pharmaceutical Design 2003, 9:1331-1334.
51. Trivedi M.S., Shah J.S., Al-Mughairy S., Hodgson N.W., Simms B., Trooskens G.A., et al. Food-derived opioid peptides inhibit cysteine uptake with redox and epigenetic consequences. Journal of Nutritional Biochemistry 2014, 25:1011-1018.
52. Twentyman P.R., Luscombe M. A study of some variables in a tetrazolium dye (MTT) based assay for cell growth and chemosensitivity. British Journal of Cancer 1987, 56:279-285.
53. Uchida Y., Ohtsuki S., Kamiie J., Ohmine K., Iwase R., Terasaki T. Quantitative targeted absolute proteomics for 28 human transporters in plasma membrane of Caco-2 cell monolayer cultured for 2, 3, and 4weeks. Drug Metabolism and Pharmacokinetics 2015, 30:205-208. 10.1016/j.dmpk.2014.11.002.
54. Walter E., Janich S., Roessler B.J., Hilfinger J.M., Amidon G.L. HT29-MTX/Caco-2 cocultures as an in vitro model for the intestinal epithelium: In vitro-in vivo correlation with permeability data from rats and humans. Journal of Pharmaceutical Sciences 1996, 85:1070-1076.
55. White J.F. Intestinal pathophysiology in autism. Review. Experimental Biology and Medicine 2003, 228:639-649.
56. Wikman-Larhed A., Artursson P. Co-cultures of human intestinal goblet (HT29-H) and absorptive (Caco-2) cells for studies of drug and peptide absorption. European Journal of Pharmaceutical Sciences 1995, 3:171-183.
57. Wilson G., Hassan I.F., Dix C.J., Williamson I., Shah R., Mackay M. Transport and permeability properties of human Caco-2 cells: An in vitro model of the intestinal epithelial cell barrier. Journal of Controlled Release 1990, 11:25-40.
58. Yoshikawa M., Takahashi M., Yang S. Delta opioid peptides derived from plant proteins. Current Pharmaceutical Design 2003, 16:1325-1330.
59. Zioudrou C., Streaty R.A., Klee W.A. Opioid peptides derived from food proteins. The exorphins. Journal of Biological Chemistry 1979, 254:2446-2449.