Proteolytic and angiotensin-converting enzyme-inhibitory activities of selected probiotic bacteria

International Journal of Food Science and Technology

Volumn 51, Issue 4, 2016, Pages 865-874

  Ahtesh, Fatah B ^a   Stojanovska, Lily ^a   Mathai, Michael L ^a   Apostolopoulos, Vasso ^a   Mishra, Vijay K ^a  

^a VICTORIA UNIVERSITY   (Australia)

Author keywords

Angiotensin converting enzyme; Flavourzyme ; Proteolytic activity; Reconstituted skim milk; Whey protein concentration

Indexed keywords

BACTERIA; ENZYME ACTIVITY; FERMENTATION; LACTIC ACID; PEPTIDES;

ANGIOTENSIN-CONVERTING ENZYME; BIFIDOBACTERIUM ANIMALIS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS DELBRUECKII; PROTEOLYTIC ACTIVITIES; SKIM MILKS; WHEY PROTEIN CONCENTRATE; WHEY PROTEINS;

STRAIN;

EID: 84977865279     PISSN: 09505423     EISSN: 13652621     Source Type: Journal    
DOI: 10.1111/ijfs.13054     Document Type: Article

References (54)

1. Ahn, C.-B., Jeon, Y.-J., Kim, Y.-T. & Je, J.-Y. (2012). Angiotensin I converting enzyme (ACE) inhibitory peptides from salmon byproduct protein hydrolysate by Alcalase hydrolysis. Process Biochemistry, 47, 2240-2245.
2. Barbana, C. & Boye, J.I. (2010). Angiotensin I-converting enzyme inhibitory activity of chickpea and pea protein hydrolysates. Food Research International, 43, 1642-1649.
3. Boutrou, R., Gaudichon, C., Dupont, D. et al. (2013). Sequential release of milk protein-derived bioactive peptides in the jejunum in healthy humans. American Journal of Clinical Nutrition, 97, 1314-1323.
4. Brown, N.J. & Vaughan, D.E. (1998). Angiotensin-converting enzyme inhibitors. Circulation, 97, 1411-1420.
5. Castro, S., Vazquez Peyronel, D. & Cantera, A.M.B. (1996). Proteolysis of whey proteins by a Bacillus subtilis enzyme preparation. International Dairy Journal, 6, 285-294.
6. Chaves-López, C., Serio, A., Paparella, A. et al. (2014). Impact of microbial cultures on proteolysis and release of bioactive peptides in fermented milk. Food Microbiology, 42, 117-121.
7. Chen, G.-W., Tsai, J.-S. & Sun Pan, B. (2007). Purification of angiotensin I-converting enzyme inhibitory peptides and antihypertensive effect of milk produced by protease-facilitated lactic fermentation. International Dairy Journal, 17, 641-647.
8. Christensen, J.E., Dudley, E.G., Pederson, J.A. & Steele, J.L. (1999). Peptidases and amino acid catabolism in lactic acid bacteria. Antonie van Leeuwenhoek, 76, 217-246.
9. Church, F.C., Swaisgood, H.E., Porter, D.H. & Catignani, G.L. (1983). Spectrophotometric assay using o-Phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. Journal of Dairy Science, 66, 1219-1227.
10. Dave, R.I. & Shah, N.P. (1998). Ingredient supplementation effects on viability of probiotic bacteria in yogurt. Journal of Dairy Science, 81, 2804-2816.
11. Davies, E.A., Bevis, H.E., Potter, R., Harris, J., Williams, G.C. & Delves-Broughton, J. (1998). Research note: the effect of pH on the stability of nisin solution during autoclaving. Letters in Applied Microbiology, 27, 186-187.
12. Dissanayake, M., Liyanaarachchi, S. & Vasiljevic, T. (2012). Functional properties of whey proteins microparticulated at low pH. Journal of Dairy Science, 95, 1667-1679.
13. Dissanayake, M., Ramchandran, L., Donkor, O.N. & Vasiljevic, T. (2013a). Denaturation of whey proteins as a function of heat, pH and protein concentration. International Dairy Journal, 31, 93-99.
14. Dissanayake, M., Ramchandran, L., Piyadasa, C. & Vasiljevic, T. (2013b). Influence of heat and pH on structure and conformation of whey proteins. International Dairy Journal, 28, 56-61.
15. Doolittle, R. (1983). Angiotensinogen is related to the antitrypsin-antithrombin-ovalbumin family. Science, 222, 417-419.
16. Donkor, O., Henriksson, A., Vasiljevic, T. & Shah, N.P. (2006). Effect of acidification on the activity of probiotics in yoghurt during cold storage. International Dairy Journal, 16, 1181-1189.
17. Donkor, O.N., Henriksson, A., Singh, T.K., Vasiljevic, T. & Shah, N.P. (2007a). ACE-inhibitory activity of probiotic yoghurt. International Dairy Journal, 17, 1321-1331.
18. Donkor, O., Henriksson, A., Vasiljevic, T. & Shah, N.P. (2007b). Proteolytic activity of dairy lactic acid bacteria and probiotics as determinant of growth and in vitro angiotensin-converting enzyme inhibitory activity in fermented milk. Lait, 87, 21-38.
19. Felicio, T.L., Esmerino, E.A., Cruz, A.G. et al. (2013). Cheese. What is its contribution to the sodium intake of Brazilians? Appetite, 66, 84-88.
20. Felicio, T.L., Esmerino, E.A., Vidal, V.A.S. et al. (2016). Physico-chemical changes during storage and sensory acceptance of low sodium probiotic Minas cheese added with arginine. Food Chemistry, 196, 628-637.
21. Fitzgerald, R.J. & Murray, B.A. (2006). Bioactive peptides and lactic fermentations. International Journal of Dairy Technology, 59, 118-125.
22. Fuglsang, A., Rattray, F., Nilsson, D. & Nyborg, N. (2003). Lactic acid bacteria: inhibition of angiotensin converting enzyme; in vitro and in vivo. Antonie van Leeuwenhoek, 83, 27-34.
23. Gauthier, S.F. & Pouliot, Y. (2003). Functional and biological properties of peptides obtained by enzymatic hydrolysis of whey proteins. Journal of Dairy Science, 86(Suppl), E78-E87.
24. Gobbetti, M., Ferranti, P., Smacchi, E., Goffredi, F. & Addeo, F. (2000). Production of Angiotensin-I-converting-enzyme-inhibitory peptides in fermented milks started by Lactobacillus delbrueckiisubsp. bulgaricus SS1 and Lactococcus lactissubsp. cremoris FT4. Applied and Environmental Microbiology, 66, 3898-3904.
25. Gomes, A.M.P., Malcata, F.X. & Klaver, F.A.M. (1998). Growth enhancement of Bifidobacterium lactis Bo and Lactobacillus acidophilus Ki by milk hydrolyzates. Journal of Dairy Science, 81, 2817-2825.
26. He, R., Alashi, A., Malomo, S.A. et al. (2013). Antihypertensive and free radical scavenging properties of enzymatic rapeseed protein hydrolysates. Food Chemistry, 141, 153-159.
27. Juillard, V., Guillot, A., Le Bars, D. & Gripon, J.-C. (1998). Specificity of milk peptide utilization by Lactococcus lactis. Applied and Environmental Microbiology, 64, 1230-1236.
28. Kilpi, E.E.R., Kahala, M.M., Steele, J.L., Pihlanto, A.M. & Joutsjoki, V.V. (2007). Angiotensin I-converting enzyme inhibitory activity in milk fermented by wild-type and peptidase-deletion derivatives of Lactobacillus helveticus CNRZ32. International Dairy Journal, 17, 976-984.
29. Korhonen, H. & Pihlanto, A. (2003). Food-derived bioactive peptides - opportunities for designing future foods. Current Pharmaceutical Design, 9, 1297-1308.
30. Korhonen, H. & Pihlanto, A. (2006). Bioactive peptides: production and functionality. International Dairy Journal, 16, 945-960.
31. Kunji, E.R.S., Fang, G., Jeronimus-Stratingh, C.M., Bruins, A.P., Poolman, B. & Konings, W.N. (1998). Reconstruction of the proteolytic pathway for use of β-casein by Lactococcus lactis. Molecular Microbiology, 27, 1107-1118.
32. Leclerc, P.-L., Gauthier, S.F., Bachelard, H., Santure, M. & Roy, D. (2002). Antihypertensive activity of casein-enriched milk fermented by Lactobacillus helveticus. International Dairy Journal, 12, 995-1004.
33. Lim, S.M., Lee, N.K., Park, K.K., Yoon, Y.C. & Paik, H.D. (2011). ACE-inhibitory effect and physicochemical characteristics of yogurt beverage fortified with whey protein hydrolysates. Korean Journal for Food Science of Animal Resources, 31, 886-892.
34. Lollo, P.C.B., Morato, P.N., Moura, C.S. et al. (2015). Hypertension parameters are attenuated by the continuous consumption of probiotic Minas cheese. Food Research International, 76(Part 3), 611-617.
35. López Expósito, I. & Recio, I. (2006). Antibacterial activity of peptides and folding variants from milk proteins. International Dairy Journal, 16, 1294-1305.
36. Meisel, H. & Bockelmann, W. (1999). Bioactive peptides encrypted in milk proteins: proteolytic activation and thropho-functional properties. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 76, 207-215.
37. Mhurchu, C., Capelin, C., Dunford, E.K., Webster, J.L., Neal, B.C. & Jebb, S.A. (2011). Sodium content of processed foods in the United Kingdom: analysis of 44, 000 foods purchased by 21, 000 households. The American Journal of Clinical Nutrition, 93, 594-600.
38. Muguerza, B., Ramos, M., Sánchez, E. et al. (2006). Antihypertensive activity of milk fermented by Enterococcus faecalis strains isolated from raw milk. International Dairy Journal, 16, 61-69.
39. Nakamura, Y., Yamamoto, N., Sakai, K., Okubo, A., Yamazaki, S. & Takano, T. (1995). Purification and characterization of angiotensin I-converting enzyme inhibitors from sour milk. Journal of Dairy Science, 78, 777-783.
40. Oberg, C.J., Weimer, B.C., Moyes, L.V., Brown, R.J. & Richardson, G.H. (1991). Proteolytic characterization of Lactobacillus delbrueckii ssp. bulgaricus strains by the o-Phthaldialdehyde test and amino acid analysis. Journal of Dairy Science, 74, 398-403.
41. Otte, J., Shalaby, S.M., Zakora, M., Pripp, A.H. & El-Shabrawy, S.A. (2007). Angiotensin-converting enzyme inhibitory activity of milk protein hydrolysates: effect of substrate, enzyme and time of hydrolysis. International Dairy Journal, 17, 488-503.
42. Pan, D. & Guo, Y. (2010). Optimization of sour milk fermentation for the production of ACE-inhibitory peptides and purification of a novel peptide from whey protein hydrolysate. International Dairy Journal, 20, 472-479.
43. Rajapakse, N., Mendis, E., Byun, H.-G. & Kim, S.-K. (2005). Purification and in vitro antioxidative effects of giant squid muscle peptides on free radical-mediated oxidative systems. The Journal of Nutritional Biochemistry, 16, 562-569.
44. Ramchandran, L. & Shah, N.P. (2008). Proteolytic profiles and angiotensin-I converting enzyme and α-Glucosidase inhibitory activities of selected lactic acid bacteria. Journal of Food Science, 73, M75-M81.
45. ® on the growth, proteolytic, ACE- and α-glucosidase inhibitory activities of selected lactic acid bacteria and Bifidobacterium. LWT - Food Science and Technology, 43, 146-152.
46. Ramos, Ó.L., Pereira, J.O., Silva, S.I. et al. (2012). Effect of composition of commercial whey protein preparations upon gelation at various pH values. Food Research International, 48, 681-689.
47. Roy, M.K., Watanabe, Y. & Tamai, Y. (2000). Yeast protease B-digested skimmed milk inhibits angiotensin-I-converting-enzyme activity. Biotechnology and Applied Biochemistry, 31, 95-100.
48. Shihata, A. & Shah, N.P. (2000). Proteolytic profiles of yogurt and probiotic bacteria. International Dairy Journal, 10, 401-408.
49. Tharmaraj, N. & Shah, N.P. (2003). Selective enumeration of Lactobacillus delbrueckii ssp. bulgaricus, Streptococcus thermophilus, Lactobacillus acidophilus, Bifidobacteria, Lactobacillus casei, Lactobacillus rhamnosus, and Propionibacteria. Journal of Dairy Science, 86, 2288-2296.
50. Tsai, J.-S., Chen, T.-J., Pan, B.S., Gong, S.-D. & Chung, M.-Y. (2008). Antihypertensive effect of bioactive peptides produced by protease-facilitated lactic acid fermentation of milk. Food Chemistry, 106, 552-558.
51. Unal, G. & Akalin, A.S. (2012). Antioxidant and angiotensin-converting enzyme inhibitory activity of yoghurt fortified with sodium calcium caseinate or whey protein concentrate. Dairy Science and Technology, 92, 627-639.
52. Wanasundara, P.K.J.P.D., Ross, A.R.S., Amarowicz, R., Ambrose, S.J., Pegg, R.B. & Shand, P.J. (2002). Peptides with angiotensin I-converting enzyme (ACE) inhibitory activity from defibrinated, hydrolyzed bovine plasma. Journal of Agricultural and Food Chemistry, 50, 6981-6988.
53. Yamamoto, N., Akino, A. & Takano, T. (1994). Antihypertensive effect of the peptides derived from casein by an extracellular proteinase from Lactobacillus helveticus CP790. Journal of Dairy Science, 77, 917-922.
54. Ziadi, M., Bergot, G., Courtin, P., Chambellon, E., Hamdi, M. & Yvon, M. (2010). Amino acid catabolism by Lactococcus lactis during milk fermentation. International Dairy Journal, 20, 25-31.