Release of angiotensin converting enzyme-inhibitor peptides during in vitro gastrointestinal digestion of Parmigiano Reggiano PDO cheese and their absorption through an in vitro model of intestinal epithelium

Journal of Dairy Science

Volumn 98, Issue 11, 2015, Pages 7595-7601

  Basirico L ^a   Catalani, E ^a   Morera, P ^a   Cattaneo, S ^b   Stuknyte, M ^b   Bernabucci, U ^a   De Noni, I ^b   Nardone, A ^a  

^a UNIVERSITY OF TUSCIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Angiotensin converting enzyme inhibitor peptides; In vitro gastrointestinal digestion; In vitro intestinal absorption; Parmigiano Reggiano; Ultra performance liquid chromatography coupled to high resolution mass spectrometry via an electrospray ionization source

Indexed keywords

CASEIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR;

ANIMAL; BOVINE; CACO 2 CELL LINE; CHEESE; CHEMISTRY; DIGESTION; GASTROINTESTINAL TRACT; HUMAN; IC50; INTESTINE MUCOSA; METABOLISM;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; CACO-2 CELLS; CASEINS; CATTLE; CHEESE; DIGESTION; GASTROINTESTINAL TRACT; HUMANS; INHIBITORY CONCENTRATION 50; INTESTINAL MUCOSA;

EID: 84944150789     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2015-9801     Document Type: Article

References (36)

1. Battistotti B., Corradini C. Italian cheese. Cheese: Chemistry, Physics and Microbiology 1993, 2:221-243. Chapman & Hall, London, UK. P.F. Fox (Ed.).
2. Bernabucci U., Catalani E., Basiricò L., Morera P., Nardone A. In vitro ACE-inhibitory activity and in vivo antihypertensive effects of water-soluble extract by Parmigiano Reggiano and Grana Padano cheeses. Int. Dairy J. 2014, 37:16-19.
3. Bernard B.K., Nakamura Y., Bando I., Mennear J.H. Studies of the toxicological potential of tripeptides (L-valyl-L-prolyl-L-proline and L-isoleucyl-L-prolyl-L-proline): II. Introduction. Int. J. Toxicol. 2005, 24:5-11.
4. Contreras M.M., Carron R., Montero M.J., Ramos M., Recio I. Novel casein-derived peptides with antihypertensive activity. Int. Dairy J. 2009, 19:566-573.
5. Contreras M.M., Sancho A.I., Recio I., Mills C. Absorption of casein antihypertensive peptides through an in vitro model of intestinal epithelium. Food Dig. 2012, 3:16-24.
6. Council Regulation EC No. 510. 2006. Council regulation (EC) No 510/2006 of 20 March 2006 on the protection of geographical indications and designations of origin for agricultural products and foodstuffs. Official Journal L 93, 31.3.2006.
7. FitzGerald R.J., Murray B.A., Walsh D.J. Hypotensive peptides from milk proteins. J. Nutr. 2004, 134:980S-988S.
8. Foltz M., Cerstiaens A., van Meensel A., Mols R., van der Pijl P.C., Duchateau G.S.M.J.E. 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.
9. Foltz M., Meynen E.E., Bianco V., van Platerink C., Koning T.M.M.G., Kloek J. Angiotensin converting enzyme inhibitory peptides from a lactotripeptide-enriched milk beverage are absorbed intact into the circulation. J. Nutr. 2007, 137:953-958.
10. Gomez-Ruiz J.A., Ramos M., Recio I. Angiotensin converting enzyme-inhibitory activity of peptides isolated from Manchego cheese. Stability under simulated gastrointestinal digestion. Int. Dairy J. 2004, 14:1075-1080.
11. Gomez-Ruiz J.A., Taborda G., Amigo L., Recio I., Ramos M. Identification of ACE-inhibitory peptides in different Spanish cheeses by tandem mass spectrometry. Eur. Food Res. Technol. 2006, 223:595-601.
12. Hayes M., Ross R.P., Fitzgerald G.F., Stanton C. Putting microbes to work: dairy fermentation, cell factories and bioactive peptides. Part I: Overview. Biotechnol. J. 2007, 2:426-434.
13. Hernández-Ledesma B., García-Nebot M.J., Fernández-Tomé S., Amigo L., Recio I. Dairy protein hydrolysates: Peptides for health benefits. Int. Dairy J. 2014, 38:82-100.
14. Jiang Z., Tian B., Brodkorb A., Huo G. Production, analysis and in vivo evaluation of novel angiotensin-I-converting enzyme inhibitory peptides from bovine casein. Food Chem. 2010, 123:779-786.
15. Kopf-Bolanz K.A., Schwander F., Gijs M., Vergères G., Portmann R., Egger L. Validation of an in vitro digestive system for studying macronutrient decomposition in humans. J. Nutr. 2012, 142:245-250.
16. López-Fandiño R., Otte J., van Camp J. Physiological, chemical and technological aspects of milk protein-derived peptides with antihypertensive and ACE-inhibitory activity. A review. Int. Dairy J. 2006, 16:1277-1293.
17. Matchar D.B., McCrory D.C., Orlando L.A., Patel M.R., Patel U.D., Patwardhan M.B., Powers B., Samsa G.P., Gray R.N. Systematic review: Comparative effectiveness of angiotensin-converting enzyme inhibitors and angiotensin II receptor blockers for treating essential hypertension. Ann. Intern. Med. 2008, 148:16-29.
18. Miguel M., Contreras M.M., Recio I., Aleixandre A. ACE-inhibitory and antihypertensive properties of a bovine casein hydrolysate. Food Chem. 2009, 112:211-214.
19. Minekus M., Alminger M., Alvito P., Ballance S., Bohn T., Bourlieu C., Carrière F., Boutrou R., Corredig M., Dupont D., Dufour C., Egger L., Golding M., Karakaya S., Kirkhus B., Le Feunteun S., Lesmes U., Macierzanka A., Mackie A., Marze S., McClements D.J., Ménard O., Recio I., Santos C.N., Singh R.P., Vegarud G.E., Wickham M.S.J., Weitschies W., Brodkorb A. A standardized static in vitro digestion method suitable for food-An international consensus. Food Funct. 2014, 5:1113-1124.
20. Nakamura Y., Yamamoto N., Sakai K., Okubo A., Yamazaki S., Takano T. Purification and characterization of angiotensin I-converting enzyme inhibitors from sour milk. J. Dairy Sci. 1995, 78:777-783.
21. Ohsawa K., Satsu H., Ohki K., Enjoh M., Takano T., Shimizu M. Producibility and digestibility of antihypertensive beta-casein tripeptides, Val-Pro-Pro and Ile-Pro-Pro, in the gastrointestinal tract: Analyses using an in vitro model of mammalian gastrointestinal digestion. J. Agric. Food Chem. 2008, 56:854-858.
22. Parrot S., Degraeve P., Curia C., Martial-Gros A. In vitro study on digestion of peptides in Emmental cheese: Analytical evaluation and influence on angiotensin I converting enzyme inhibitory peptides. Nahrung 2003, 47:87-94.
23. Pripp A.H., Sorensen R., Stepaniak L., Sorhaug T. Relationship between proteolysis and angiotensin-I-converting enzyme inhibition in different cheeses. LWT Food Sci. Technol. (Campinas.) 2006, 39:677-683.
24. Progetto Si P-R. 2015. Accessed Apr. 27, 2015. http://sipr.crpa.it/.
25. Quirós A., Contreras M., Ramos M., Amigo L., Recio I. Stability to gastrointestinal enzymes and structure-activity relationship of β-casein-peptides with antihypertensive properties. Peptides 2009, 30:1848-1853.
26. Quirós A., Davalos A., Lasuncion M.A., Amigo L., Recio I. Bioavailability of the antihypertensive peptide LHLPLP: Transepithelial flux of HLPLP. Int. Dairy J. 2008, 18:279-286.
27. Quirós A., Ramos M., Muguerza B., Delgado M.A., Miguel M., Aleixandre A., Recio I. Identification of novel antihypertensive peptides in milk fermented with Enterococcus faecalis. Int. Dairy J. 2007, 17:33-41.
28. Rizzello C.G., Losito I., Gobbetti M., Carbonara T., De Bari M.D., Zambonin P.G. Antibacterial activities of peptides from the water-soluble extracts of Italian cheese varieties. J. Dairy Sci. 2005, 88:2348-2360.
29. Sagardia I., Iloro I., Elortza F., Bald C. Quantitative structure-activity relationship based screening of bioactive peptides identified in ripened cheese. Int. Dairy J. 2013, 33:184-190.
30. Sakai M., Imai T., Ohtake H., Otagiri M. Cytotoxicity of absorption enhancers in Caco-2 cell monolayers. J. Pharm. Pharmacol. 1998, 50:1101-1108.
31. Sambuy Y., De Angelis I., Ranaldi G., Scarino M.L., Stammati A., Zucco F. The Caco-2 cell line as a model of the intestinal barrier: Influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol. Toxicol. 2005, 21:1-26.
32. Satake M., Enjoh M., Nakamura Y., Takano T., Kawamura Y., Arai S., Shimizu M. Transepithelial transport of the bioactive tripeptide, Val-Pro-Pro, in human intestinal Caco-2 cell monolayers. Biosci. Biotechnol. Biochem. 2002, 66:378-384.
33. Shimizu M. Interaction between food substance and the intestinal epithelium. Biosci. Biotechnol. Biochem. 2010, 74:232-241.
34. Shimizu M., Ok Son D. Food-derived peptides and intestinal functions. Curr. Pharm. Des. 2007, 13:885-895.
35. Sieber R., Bütikofer U., Egger C., Portmann R., Walther B., Wechsler D. ACE-inhibitory activity and ACE-inhibiting peptides in different cheese varieties. Dairy Sci. Technol. 2010, 90:47-73.
36. Stuknyte M., Cattaneo S., Masotti F., De Noni I. Occurrence and fate of ACE-inhibitor peptides in cheeses and in their digestates following in vitro static gastrointestinal digestion. Food Chem. 2015, 168:27-33.