Active peptides from skate (okamejei kenojei) skin gelatin diminish angiotensin-i converting enzyme activity and intracellular free radical-mediated oxidation

Food Chemistry

Volumn 143, Issue , 2014, Pages 246-255

  Ngo, Dai Hung ^a   Ryu, BoMi ^b   Kim, Se Kwon ^a  

^a Pukyong National University   (South Korea)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Ace inhibition; Antioxidative enzymes; Bioactive peptides; Human endothelial; ROS; Skate skin

Indexed keywords

ANTIOXIDANTS; ENDOTHELIAL CELLS; ENZYME INHIBITION; ENZYMES; FREE RADICALS; GENE EXPRESSION; HYDROLYSIS; PEPTIDES; PROTEINS; PURIFICATION;

ACE INHIBITION; ANGIOTENSIN I-CONVERTING ENZYME; ANTI-OXIDATIVE ENZYMES; BIOACTIVE PEPTIDES; FREE RADICAL SCAVENGING ACTIVITY; HUMAN ENDOTHELIAL; HUMAN ENDOTHELIAL CELLS; ULTRAFILTRATION MEMBRANE SYSTEMS;

ENZYME ACTIVITY;

DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; FREE RADICAL; GELATIN; PEPTIDE DERIVATIVE;

AMINO ACID SEQUENCE; ANION EXCHANGE; ANTIHYPERTENSIVE ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FLOW CYTOMETRY; FOOD INDUSTRY; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROLYSIS; IC 50; MACROMOLECULE; MASS SPECTROMETRY; MOLECULAR SIZE; MOLECULAR WEIGHT; NONHUMAN; OKAMEJEI KENOJEI; OXIDATION; OXIDATIVE STRESS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKATES (FISH); SKIN; ULTRAFILTRATION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING;

OKAMEJEI KENOJEI;

EID: 84884578190     PISSN: 03088146     EISSN: 18737072     Source Type: Journal    
DOI: 10.1016/j.foodchem.2013.07.067     Document Type: Article

References (62)

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. Al Ghouleh, I., Khoo, N. K., Knaus, U. G., Griendling, K. K., Touyz, R. M., Thannickal, V. J., et al. (2011). Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling. Free Radical Biology and Medicine, 51, 1271-1288.
3. Betoret, E., Betoret, N., Vidal, D., & Fito, P. (2011). Functional foods development: Trends and technologies. Trends in Food Science and Technology, 22, 498-508.
4. Boukortt, F. O., Girard, A., Prost, J., Ait-Yahia, D., Bouchenak, M., & Belleville, J. (2004). Fish protein improves the total antioxidant status of streptozotocininduced diabetes in spontaneously hypertensive rat. Medical Science Monitor, 10, BR397-BR404. (Pubitemid 39546026)
5. Byun, H. G., & Kim, S. K. (2001). Purification and characterization of angiotensin I converting enzyme (ACE) inhibitory peptides from Alaska pollack (Theragra chalcogramma) skin. Process Biochemistry, 36, 1155-1162.
6. Byun, H. G., Lee, J. K., Park, H. G., Jeon, J. K., & Kim, S. K. (2009). Antioxidant peptides isolated from the marine rotifer, Brachionus rotundiformis. Process Biochemistry, 44, 842-846.
7. Cushman, D. W., & Cheung, H. S. (1971). Spectrophotometric assay and properties of the angiotensin I-converting enzyme of rabbit lung. Biochemical Pharmacology, 20, 1637-1648.
8. Elias, R. J., Kellerby, S. S., & Decker, E. A. (2008). Antioxidant activity of proteins and peptides. Critical Reviews in Food Science and Nutrition, 48, 430-441. (Pubitemid 351883136)
9. Enari, H., Takahashi, Y., Kawarasaki, M., Tada, M., & Tatsuta, K. (2008). Identification of angiotensin I-converting enzyme inhibitory peptides derived from salmon muscle and their antihypertensive effect. Fisheries Science, 74, 911-920.
10. Erdmann, K., Cheung, B. W. Y., & Schroder, H. (2008). The possible roles of foodderived bioactive peptides in reducing the risk of cardiovascular disease. Journal of Nutritional Biochemistry, 19, 643-654.
11. Fahmi, A., Morimura, S., Guo, H. C., Shigematsu, T., Kida, K., & Uemura, Y. (2004). Production of angiotensin I converting enzyme inhibitory peptides from sea bream scales. Process Biochemistry, 39, 1195-1200. (Pubitemid 38700218)
12. Fahmy, S. R., & Hamdi, S. A. H. (2011). Curative effect of the Egyptian marine Erugosquilla massavensis extract on carbon tetrachloride-induced oxidative stress in rat liver and erythrocytes. European Review for Medical and Pharmacological Sciences, 15, 303-312.
13. Fujita, H., & Yoshikawa, M. (1999). LKPNM: A prodrug-type ACE-inhibitory peptide derived from fish protein. Immunopharmacology, 44, 123-127.
14. Gambhir, K. J., Lali, P., & Jain, A. K. (1997). Correlation between blood antioxidant levels and lipid peroxidation in rheumatoid arthritis. Clinical Biochemistry, 30, 351-355. (Pubitemid 27282343)
15. Guo, H., Kouzuma, Y., & Yonekura, M. (2009). Structures and properties of antioxidative peptides derived from royal jelly protein. Food Chemistry, 113, 238-245.
16. Hasan, M. F., Kobayashi, Y., Kumada, Y., Katsuda, T., Terashima, M., & Katoh, S. (2007). ACE inhibitory activity and characteristics of tri-peptides obtained from bonito protein. Journal of Chemical Engineering of Japan, 40, 59-62. (Pubitemid 46157799)
17. Hideaki, K., Masayoshi, K., Shigeru, S., Chiyo, D., Kunio, D., Nobuyasu, M., et al. (1993). Oral administration of peptides derived from bonito bowels decreases blood pressure in spontaneously hypertensive rats by inhibiting angiotensin converting enzyme. Comparative Biochemistry and Physiology, C: Comparative Pharmacology, 104, 351-353.
18. Himaya, S. W. A., Ngo, D. H., Ryu, B. M., & Kim, S. K. (2012). An active peptide purified from gastrointestinal enzyme hydrolysate of Pacific cod skin gelatin attenuates angiotensin-1 converting enzyme (ACE) activity and cellular oxidative stress. Food Chemistry, 132, 1872-1882.
19. Hsu, K. C. (2010). Purification of antioxidative peptides prepared from enzymatic hydrolysates of tuna dark muscle by-product. Food Chemistry, 122, 42-48.
20. Hyun, C. K., & Shin, H. K. (2000). Utilization of bovine blood plasma proteins for the production of angiotensin I converting enzyme inhibitory peptides. Process Biochemistry, 36, 65-71.
21. Je, J. Y., Park, P. J., Kwon, J. Y., & Kim, S. K. (2004). A novel angiotensin I converting enzyme inhibitory peptide from Allaska Pollack (Theragra chalcogramma) frame protein hydrolysate. Journal of Agricultural and Food Chemistry, 52, 7842-7845. (Pubitemid 40053665)
22. Jung, W. K., Rajapakse, N., & Kim, S. K. (2005). Antioxidative activity of a low molecular weight peptide derived from the sauce of fermented blue mussel, Mytillus edulis. European Food Research and Technology, 220, 535-539. (Pubitemid 40666402)
23. Kearney, P. M., Whelton, M., Reynolds, K., Muntner, P., Whelton, P. K., & He, J. (2005). Global burden of hypertension: analysis of worldwide data. The Lancet, 365, 217-223. (Pubitemid 40138015)
24. Kim, S. Y., Je, J. Y., & Kim, S. K. (2007). Purification and characterization of antioxidant peptide from hoki (Johnius belengerii) frame protein by gastrointestinal digestion. Journal of Nutritional Biochemistry, 18, 31-38.
25. Kizhakekuttu, T. J., & Widlansky, M. E. (2010). Natural antioxidants and hypertension: promise and challenges. Cardiovascular Therapeutics, 28, e20-e32.
26. Ko, S. C., Kim, D., & Jeon, Y. J. (2012). Protective effect of a novel antioxidative peptide purified from a marine Chlorella ellipsoidea protein against free radicalinduced oxidative stress. Food and Chemical Toxicology, 50, 2294-2302.
27. Korhonen, H., & Pihlanto, A. (2006). Bioactive peptides: Production and functionality. International Dairy Journal, 16, 945-960. (Pubitemid 44255683)
28. Kristinsson, H. G., & Rasco, B. A. (2000). Fish protein hydrolysates: production, biochemical and functional properties. Critical Reviews in Food Science and Nutrition, 40, 43-81.
29. Lee, J. K., Hong, S., Jeon, J. K., Kim, S. K., & Byun, H. G. (2009). Purification and characterization of angiotensin I converting enzyme inhibitory peptides from the rotifer, Brachionus rotundiformis. Bioresource Technology, 100, 5255-5259.
30. Lee, S. H., Qian, Z. J., & Kim, S. K. (2010). A novel angiotensin I converting enzyme inhibitory peptide from tuna frame protein hydrolysate and its antihypertensive effect in spontaneously hypertensive rats. Food Chemistry, 118, 96-102.
31. Li, G. H., Wan, J. Z., Le, G. W., & Shi, Y. H. (2006). Novel angiotensin I-converting enzyme inhibitory peptides isolated from Alcalase hydrolysate of mung bean protein. Journal of Peptide Science, 12, 509-514.
32. Li, R., Yu, H., Xing, R., Liu, S., Qing, Y., Li, K., et al. (2012). Isolation, identification and characterization of a novel antioxidant protein from the nematocyst of the jellyfish Stomolophus meleagris. International Journal of Biological Macromolecules, 51, 274-278.
33. Lindqvist, H. M., Langkilde, A. M., Undeland, I., & Sandberg, A. S. (2009). Herring (Clupea harengus) intake influences lipoproteins but not inflammatory and oxidation markers in overweight men. British Journal of Nutrition, 101, 383-390.
34. Lun, H. H., Lan, C. X., Yun, S. C., Zhong, Z. Y., & Cheng, Z. B. (2006). Analysis of novel angiotensin-I-converting enzyme inhibitory peptides from protease-hydrolyzed marine shrimp Acetes chinensis. Journal of Peptide Science, 12, 726-733.
35. Marchbank, T., Limdi, J. K., Mahmood, A., Elia, G., & Playford, R. J. (2008). Clinical trial: protective effect of a commercial fish protein hydrolysate against indomethacin (NSAID)-induced small intestinal injury. Alimentary Pharmacology and Therapeutics, 28, 799-804.
36. Matsufuji, H., Matsui, T., Seki, E., Osajima, K., Nakashima, M., & Osajima, Y. (1994). Angiotensin I-converting enzyme inhibitory peptides in an alkaline protease hydrolyzate derived from sardine muscle. Bioscience, Biotechnology, and Biochemistry, 58, 2244-2245.
37. Nazeer, R. A., Sampath Kumar, N. S., & Jai Ganesh, R. (2012). In vitro and in vivo studies on the antioxidant activity of fish peptide isolated from the croaker (Otolithes ruber) muscle protein hydrolysate. Peptides, 35, 261-268.
38. Ngo, D. H., Qian, Z. J., Ryu, B. M., Park, J. W., & Kim, S. K. (2010). In vitro antioxidant activity of a peptide isolated from Nile tilapia (Oreochromis niloticus) scale gelatin in free radical-mediated oxidative systems. Journal of Functional Foods, 2, 107-117.
39. Ngo, D. H., Qian, Z. J., Vo, T. S., Ryu, B. M., Ngo, D. N., & Kim, S. K. (2011a). Antioxidant activity of gallate-chitooligosaccharides in mouse macrophage RAW264.7 cells. Carbohydrate Polymers, 84, 1282-1288.
40. Ngo, D. H., Ryu, B. M., Vo, T. S., Himaya, S. W. A., Wijesekara, I., & Kim, S. K. (2011b). Free radical scavenging and angiotensin-I converting enzyme inhibitory peptides from Pacific cod (Gadus macrocephalus) skin gelatin. International Journal of Biological Macromolecules, 49, 1110-1116.
41. Ngo, D. H., Vo, T. S., Ngo, D. N., Wijesekara, I., & Kim, S. K. (2012). Biological activities and potential health benefits of bioactive peptides derived from marine organisms. International Journal of Biological Macromolecules, 51, 378-383.
42. Pan, D., Luo, Y., & Tanokura, M. (2005). Antihypertensive peptides from skimmed milk hydrolysate digested by cell-free extract of Lactobacillus helveticus JCM1004. Food Chemistry, 91, 123-129. (Pubitemid 39572541)
43. Parra, D., Bandarra, N. M., Kiely, M., Thorsdottir, I., & Martinez, J. A. (2007). Impact of fish intake on oxidative stress when included into a moderate energy-restricted program to treat obesity. European Journal of Nutrition, 46, 460-467. (Pubitemid 50004078)
44. Qian, Z. J., Jung, W. K., & Kim, S. K. (2008). Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin, Rana catesbeiana Shaw. Bioresource Technology, 99, 1690-1698.
45. Qian, Z. J., Jung, W. K., Lee, S. H., Byun, H. G., & Kim, S. K. (2007). Antihypertensive effect of an angiotensin I-converting enzyme inhibitory peptide from bullfrog (Rana catesbeiana Shaw) muscle protein in spontaneously hypertensive rats. Process Biochemistry, 42, 1443-1448.
46. Rosenkranz, A. R., Schmaldienst, S., Stuhlmeier, K. M., Chen, W., Knapp, W., & Zlabinger, G. J. (1992). A microplate assay for the detection of oxidative products using 20, 70-dichlorofluorescein-diacetate. Journal of Immunological Methods, 156, 39-45.
47. Ryan, J. T., Ross, R. P., Bolton, D., Fitzgerald, G. F., & Stanton, C. (2011). Bioactive peptides from muscle sources: Meat and fish. Nutrients, 3, 765-791.
48. Ryu, B. M., Kang, K. H., Ngo, D. H., Qian, Z. J., & Kim, S. K. (2012). Statistical optimization of microalgae Pavlova lutheri cultivation conditions and its fermentation conditions by yeast, Candida rugopelliculosa. Bioresource Technology, 107, 307-313.
49. Samaranayaka, A. G. P. (2010). Pacific hake (Merluccius productus) fish protein hydrolysates with antioxidative properties. Doctor of Philosophy in The Faculty of Graduate Studies (Food Science), The University of British Columbia, Vancouver.
50. Sampath Kumar, N. S., Nazeer, R. A., & Jaiganesh, R. (2012). Purification and identification of antioxidant peptides from the skin protein hydrolysate of two marine fishes, horse mackerel (Magalaspis cordyla) and croaker (Otolithes ruber). Amino Acids, 42, 1641-1649.
51. Sanchez-Reus, M. I., Peinado, I. I., Molina-Jimenez, M. F., & Benedi, J. (2005). Flaxetin prevents rotenone-induced apoptosis by induction of endogenous glutathione in human neuroblastoma cells. Neuroscience Research, 53, 48-56. (Pubitemid 41073727)
52. Sato, M., Hosokawa, T., Yamaguchi, T., Nakano, T., Muramoto, K., Kahara, T., et al. (2002). Angiotensin I-converting enzyme inhibitory peptides derived from wakame (Undaria pinnatifida) and their antihypertensive effect in spontaneously hypertensive rats. Journal of Agricultural and Food Chemistry, 50, 6245-6252. (Pubitemid 35155365)
53. Senaratne, L. S., Park, P. J., & Kim, S. K. (2006). Isolation and characterization of collagen from brown backed toadfish (Lagocephalus gloveri) skin. Bioresource Technology, 97, 191-197. (Pubitemid 41317965)
54. Sheih, I. C., Fang, T. J., & Wu, T. K. (2009). Isolation and characterization of a novel angiotensin I-converting enzyme (ACE) inhibitory peptide from the algae protein waste. Food Chemistry, 115, 279-284.
55. Sheih, I. C., Fang, T. J., Wu, T. K., & Lin, P. H. (2010). Anticancer and antioxidant activities of the peptide fraction from algae protein waste. Journal of Agricultural and Food Chemistry, 58, 1202-1207.
56. Suetsuna, K., & Nakano, T. (2000). Identification of an antihypertensive peptide from peptic digest of wakame (Undaria pinnatifida). Journal of Nutritional Biochemistry, 11, 450-454.
57. Tsai, J. S., Chen, J. L., & Pan, B. S. (2008). ACE-inhibitory peptides identified from the muscle protein hydrolysate of hard clam (Meretrix lusoria). Process Biochemistry, 43, 743-747.
58. Vo, T. S., Ngo, D. H., & Kim, S. K. (2012). Gallic acid-grafted chitooligosaccharides suppress antigen-induced allergic reactions in RBL-2H3 mast cells. European Journal of Pharmaceutical Sciences, 47, 527-533.
59. Vo, T. S., Ngo, D. H., Kim, J. A., Ryu, B. M., & Kim, S. K. (2011). An antihypertensive peptide from tilapia gelatin diminishes free radical formation in murine microglial cells. Journal of Agricultural and Food Chemistry, 59, 12193-12197.
60. Wang, B., Li, Z. R., Chi, C. F., Zhang, Q. H., & Luo, H. Y. (2012). Preparation and evaluation of antioxidant peptides from ethanol-soluble proteins hydrolysate of Sphyrna lewini muscle. Peptides, 36, 240-250.
61. Wu, H., He, H. L., Chen, X. L., Sun, C. Y., Zhang, Y. Z., & Zhou, B. C. (2008). Purification and identification of novel angiotensin-I-converting enzyme inhibitory peptides from shark meat hydrolysate. Process Biochemistry, 43, 457-461.
62. Zhao, Y., Bafang, L., Dong, S., Liu, Z., Zhao, X., Wang, J., et al. (2009). A novel ACE inhibitory peptide isolated from Acaudina molpadioidea hydrolysate. Peptides, 30, 1028-1033.