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Changes of proteolysis and angiotensin-I converting enzyme-inhibitory activity in white-brined cheese as affected by adjunct culture and ripening temperature

Published online by Cambridge University Press:  14 July 2014

Didem Sahingil ,
Ali A. Hayaloglu ,
Huseyin A. Kirmaci ,
Barbaros Özer  and
Osman Simsek
Didem Sahingil
Affiliation:
Department of Food Engineering, Engineering Faculty, Inonu University, Malatya, Turkey
Ali A. Hayaloglu*
Affiliation:
Department of Food Engineering, Engineering Faculty, Inonu University, Malatya, Turkey
Huseyin A. Kirmaci
Affiliation:
Department of Nutrition and Dietetics, School of Health, Karabuk University, Karabuk, Turkey
Barbaros Özer
Affiliation:
Department of Dairy Technology, Agricultural Faculty, Ankara University, Ankara, Turkey
Osman Simsek
Affiliation:
Department of Food Engineering, Agricultural Faculty, Namik Kemal University, Tekirdag, Turkey
*
* For correspondence; e-mail: adnan.hayaloglu@inonu.edu.tr
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Abstract

The effects of use of adjunct cultures (Lactobacillus helveticus and Lb. casei) and ripening temperatures (6 or 12 °C) on proteolysis and angiotensin-I converting enzyme (ACE)-inhibitory activity in white-brined cheeses were investigated during 120 d ripening. Proteolysis was monitored by urea-polyacrylamide gel electrophoresis (urea-PAGE) and reversed phase-HPLC (RP-HPLC) of water-insoluble and -soluble fractions of the cheeses, respectively. Urea-PAGE patterns of the samples revealed that the intensities of the bands representing casein fractions decreased in the experimental cheeses, being more pronounced in the cheeses made with adjunct cultures. Similarly, peptide profiles and the concentrations of individual and total free amino acids were influenced by both the adjunct cultures and ripening temperatures. The ACE-inhibitory activity of the water-soluble extracts of the cheeses were higher in the cheeses made using adjunct cultures (especially Lb. helveticus) and ripened at 12 °C. The ACE-inhibitory activity did not decrease during ripening. The contribution of Lb. helveticus to the development of proteolysis and ACE-inhibitory peptide activities were higher than that of Lb. casei. To conclude, the use of Lb. helveticus as adjunct culture in white-brined cheese and ripening at 12 °C would be recommended to obtain white-brined cheese with high ACE-I-inhibitory peptides activity and higher levels of preoteolysis.

Keywords

ACE-I-inhibitory enzymebioactive peptidesbrined cheeseproteolysis

Information

Type
Research Article
Information
Journal of Dairy Research , Volume 81 , Issue 4 , November 2014 , pp. 394 - 402
Copyright
Copyright © Proprietors of Journal of Dairy Research 2014 

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References

Addeo, F, Chianese, L, Salzano, A, Sacchi, R, Cappuccio, U, Ferranti, P & Malirni, A 1992 Characterization of the 12% tricholoroacetic acid-insoluble oligopeptides of Parmigiano- Reggiano cheese. Journal of Dairy Research 59 401–411 Google Scholar
Ardö, Y & Polychroniadou, A 1999 Laboratory Manual for Chemical Analysis of Cheese, pp. 95. Luxembourg: Cost Google Scholar
Banks, JM & Williams, AG 2004 The role of the non-starter lactic acid bacteria in Cheddar cheese ripening. International Journal of Dairy Technology 57 145–152 Google Scholar
Bütikofer, U, Meyer, J, Sieber, R & Wechsler, D 2007 Quantification of the angiotensin-converting enzyme-inhibiting tripeptides Val-Pro-Pro and Ile-Pro-Pro in hard, semi-hard and soft cheeses. International Dairy Journal 17 968–975 Google Scholar
Cheung, HS, Wang, FL, Ondetti, MA, Sabo, EF & Cushman, DW 1980 Binding of peptide substrates and inhibitors of angiotensin-converting enzyme. Importance of the COOH-terminal dipeptide sequence. Journal of Biological Chemistry 255 401–407 CrossRefGoogle ScholarPubMed
Crow, VL, Coolbear, T, Gopal, PK, Martley, FG, McKay, LL & Riepe, H 1995 The role of autolysis of lactic acid bacteria in the ripening of cheese. International Dairy Journal 5 855–875 Google Scholar
Cushman, DW & Cheung, HS 1971 Spectrophotometric assay and properties of the angiotensin-converting enzyme of rubbit lung. Biochemical Pharmacology 20 1637–1648 Google Scholar
El-Soda, M, Madkor, SA & Tong, PS 2000 Adjunct cultures: recent developments and potential significance to the cheese industry. Journal of Dairy Science 83 609–619 CrossRefGoogle Scholar
Fenelon, MA, Ryan, MP, Rea, MC, Guinee, TP, Ross, RP, Hill, C & Harrington, D 1999 Elevated temperature ripening of reduced fat cheddar cheese made with or without lacticin 3147-producing starter culture. Journal of Dairy Science 82 10–22 Google Scholar
Folkertsma, B, Fox, PF & McSweeney, PLH 1996 Accelerated ripening of cheese at elevated temperatures. International Dairy Journal 6 1114–1117 Google Scholar
Fox, PF, O'Connor, TP, McSweeney, PLH, Guinee, TP & O'Brien, NM 1996 Cheese: physical, chemical, biochemical and nutritional aspects. Advances in Food and Nutritional Research 39 163–328 Google Scholar
Fox, PF, Guinee, TP, Cogan, TM & McSweeney, PLH 2000 Fundamentals of Cheese Science, pp. 585. Gaithershurg, Maryland: An Aspen Publication Google Scholar
Gomez-Ruiz, JA, Ramos, M & Recio, I 2002 Angiotensin-I-converting enzyme-inhibitory peptides in Manchego cheese mamnufactured with different starter cultures. International Dairy Journal 12 697–706 Google Scholar
Hannon, JA, Wilkinson, MG, Delahunty, CM, Wallace, JM, Morrissey, PA & Beresford, TP 2003 Use of autolytic starter systems to accelerate the ripening of Cheddar cheese. International Dairy Journal 13 313–323 Google Scholar
Hannon, JA, Kilcawley, KN, Wilkinson, MG, Delahunty, CM & Beresford, TP 2007 Flavour precursor development in Cheddar cheese due to lactococcal starters and the presence and lysis of Lactobacillus helveticus . International Dairy Journal 17 316–327 CrossRefGoogle Scholar
Harrigan, WF 1998 Laboratory Methods in Food Microbiology. San Diego: Academic Press Google Scholar
Hashemi, M, Azar, M & Mazlumi, MT 2009 Effect of commercial adjunct lactobacilli on biochemical and sensory characteristics of Iranian white-brined cheese. International Journal of Dairy Technology 62 48–55 Google Scholar
Hayaloglu, AA 2007 Comparisons of different single-strain starter cultures for their effects on ripening and grading of Beyaz cheese. International Journal of Food Science and Technology 42 930–938 Google Scholar
Hayaloglu, AA, Guven, M & Fox, PF 2002 Microbiological, biochemical and technological properties of Turkish White cheese “Beyaz Peynir”. International Dairy Journal 12 635–648 Google Scholar
Hayaloglu, AA, Guven, M, Fox, PF, Hannon, JA & McSweeney, PLH 2004 Proteolysis in Turkish White-brined cheese made with defined strains of Lactococcus . International Dairy Journal 14 509–610 Google Scholar
Hayaloglu, AA, Guven, M, Fox, PF & McSweeney, PLH 2005 Influence of Starters on chemical, biochemical and sensory changes in Turkish White-brined Cheese. Journal of Dairy Science 88 3460–3467 Google Scholar
Lee, BH, Kilcawley, KN, Hannon, JA, Park, SY, Wilkinson, MG & Beresford, TP 2007 The use of viable and heat-shocked Lactobacillus helveticus DPC 4571 in enzyme modified cheese production. Food Biotechnology 21 129–143 CrossRefGoogle Scholar
Madkor, SA, Tong, PS & El-Soda, M 2000 Evaluation of commercial adjuncts for use in cheese ripening: 5. Effect of added freeze-shocked adjunct lactobacilli on proteolysis and sensory quality of reduced fat Cheddar cheese. Milchwissenschaft 55 382–386 Google Scholar
Mallatou, H, Pappa, EC & Boumba, AV 2004 Proteolysis in Teleme cheese made from ewes’, goats’ or a mixture of ewes’ and goats’ milk, Greece. International Dairy Journal 14 977–987 Google Scholar
Meira, SMM, Dariot, DJ, Helfer, VE, Correa, APF, Segalin, J, Carro, S & Brandelli, A 2012 Bioactive peptides in water-soluble extracts of ovine cheeses from Southern Brazil and Uruguay. Food Research International 48 322–329 Google Scholar
Meisel, H, Goepfert, A & Günther, S 1997 ACE inhibitory activities in milk products. Milchwissenschaft 52 307–311 Google Scholar
Meyer, J, Bütikofer, U, Walther, B, Wechsler, D & Sieber, R 2009 Changes in angiotensin converting enzyme inhibition and concentrations of the tripeptides Val-Pro-Pro and Ile-Pro-Pro during ripening of different Swiss cheese varieties. Journal of Dairy Science 92 826–836 Google Scholar
Milesi, MM, Bergamini, CV & Hynes, E 2011 Production of peptides and free amino acids in a sterile extract describes peptidolysis in hard-cooked cheeses. Food Research International 44 765–773 Google Scholar
Nakamura, Y, Yamamoto, N, Sakai, K & Takano, T 1995 Antihypertensive effect of sour milk and peptides isolated from it that are inhibitors to angiotensin I converting enzyme. Journal of Dairy Science 78 1253–1257 Google Scholar
Ong, L & Shah, NP 2009 Probiotic Cheddar cheese: influence of ripening temperatures on proteolysis and sensory characteristics of Cheddar cheeses. Journal of Food Science 74 181–191 Google Scholar
Ong, L & Shah, N 2008a Influence of probiotic Lactobacillus acidophilus and L. helveticus on proteolysis, organic acid profiles, and ACE-inhibitory activity of Cheddar cheeses ripened at 4, 8, and 12 °C. Journal of Food Science 73 M111–M120 CrossRefGoogle Scholar
Ong, L & Shah, NP 2008b Release and identification of angiotensin-converting enzyme-inhibitory peptides as influenced by ripening temperatures and probiotic adjuncts in Cheddar cheese. LWT-Food Science and Technology 41 1555–1566 Google Scholar
Ong, L, Henriksson, A & Shah, N 2007 Angiotensin converting enzyme-inhibitory activity in Cheddar cheeses made with the addition of probiotic Lactobacillus casei sp. Lait 87 149–165 Google Scholar
Otte, J, Shalaby, SM, Zakora, M, Pripp, AH & Shabrawyb, SA 2007 Angiotensin-converting enzyme inhibitory activity of milk protein hydrolysates: effect of substrate, enzyme and time of hydrolysis. International Dairy Journal 17 488–503 Google Scholar
Özer, B 1999 Microflora of white-brined cheeses. In Encyclopedia of Food Microbiology, pp. 397–402 (Ed. Robinson, RK, Batt, C & Patel, PD) Academic Press, London Google Scholar
Pappa, EC & Sotirakoglou, K 2008. Changes of free amino acid content of Teleme cheese made with different types of milk and culture. Food Chemistry 111 606–615 Google Scholar
Parrot, S, Degraeve, P, Curia, C & Martial-Gros, A 2003 In vitro study on digestion of peptides in Emmental cheese: analytical evaluation and influence on angiotensin I converting enzyme inhibitory peptides. Nahrung 47 87–94 CrossRefGoogle Scholar
Pripp, AH, Sorensen, R, Stepaniak, L & Sorhaug, T 2006 Relationship between proteolysis and angiotensin-I-converting enzyme inhibition in differen cheeses. LWT-Food Science and Technology 39 677–683 Google Scholar
Qureshi, TM, Vegarud, GE, Abrahamsen, RK & Skeie, S 2013 Angiotensin-I-converting enzyme-inhibitory activity of the Norwegian autochthonous cheeses Gamalost and Norvegia after in vitro human gastrointestinal digestion. Journal of Dairy Science 96 838–853 Google Scholar
Robert, MC, Razaname, A, Mutter, M & Juillerat, MA 2004 Identification of angiotensin-I converting enzyme inhibitory peptides derived from sodium caseinate hydrolysates produced by Lactobacillus helveticus NCC 2765. Journal of Agricultural and Food Chemistry 52 6923–6931 Google Scholar
Ryhänen, EL, Pihlanto, LA & Pahkala, E 2001 A new type of ripened; low-fat cheese with bioactive properties. International Dairy Journal 11 441–447 Google Scholar
Sarantinopoulos, P, Kanaltzopoulos, G & Tsakalidou, E 2002 Effect of Enterococcus faecium on microbiological, physicochemical and sensory characteristics of Greek feta cheese. International Journal of Food Microbiology 76 93–105 Google Scholar
Seppo, L, Kerojoki, O, Suomalainen, T & Korpela, R 2002 The effect of a Lactobacillus helveticus LBK-16 H fermented milk on hypertension-a pilot study on humans. Milchwissenschaft 57 124–127 Google Scholar
Seppo, L, Jauhianene, T, Poussa, T & Korpela, R 2003 A fermented milk high in bioactive peptides has a blood pressure-lowering effect in hypertensive subjects. American Journal of Clinical Nutrition 77 326–330 Google Scholar
Sieber, R, Bütikofer, U, Egger, C, Portmann, R, Walther, B & Wechsler, D 2010 ACE inhibitory activity and ACE-inhibiting peptides in different cheese varieties. Dairy Science and Technology 90 47–73 Google Scholar
Sihufe, GA, Zorilla, SE & Rubiolo, AC 2010 The influence of ripening temperature and sampling site on the proteolysis in Reggianito Argentino cheese. LWT-Food Science and Technology 43 247–253 CrossRefGoogle Scholar
Smacchi, E & Gobbetti, M 1998 Peptides from several Italian cheeses inhibitory to proteolytic enzymes of lactic acid bacteria, Pseudomonas fluorescens ATCC 948 and to the angiotensin-I-converting enzyme. Enzyme and Microbial Technology 22 687–694 Google Scholar
Tuomilehto, J, Lindström, J, Hryyrynen, J, Korpela, R, Karhunen, M-L, Mikkola, L, Jauhiainen, T, Seppo, L & Nissinen, A 2004 Effect of ingesting sour milk fermented using Lactobacillus helveticus bacteria producing tripeptides on blood pressure in subjects with mild hypertension. Journal of Human Hypertension 18 795–802 Google Scholar
Urista, CM, Alvarez-Fernandez, R, Riera-Rodriguez, F, Arana-Cuenca, A & Tellez Jurado, A 2011 Production and functionality of active peptides from milk. International Journal of Food Science and Technology 17 293–317 Google Scholar
Wang, H, Cui, L, Chen, W & Zhang, H 2011 An application in Gouda cheese manufacture for a strain of Lactobacillus helveticus ND01. International Journal of Dairy Technology 64 386–393 Google Scholar
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