A peptidomic approach for the identification of antioxidant and ACE-inhibitory peptides in sardinelle protein hydrolysates fermented by Bacillus subtilis A26 and Bacillus amyloliquefaciens An6

Food Research International

Volumn 89, Issue , 2016, Pages 347-358

  Jemil, Ines ^a   Mora, Leticia ^b   Nasri, Rim ^a   Abdelhedi, Ola ^a   Aristoy, Maria Concepción ^b   Hajji, Mohamed ^a   Nasri, Moncef ^a   Toldrá, Fidel ^b  

^a UNIVERSITY OF SFAX   (Tunisia)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

Author keywords

ACE inhibitory activity; Antioxidant activity; Fermentation; Peptidomic analysis; Protein hydrolysates; Sardinella aurita

Indexed keywords

ANTIOXIDANTS; BACTERIOLOGY; FERMENTATION; FREE RADICALS; HYDROLYSIS; PEPTIDES; PLANTS (BOTANY);

ACE-INHIBITORY ACTIVITY; ANTI-OXIDANT ACTIVITIES; PEPTIDOMIC ANALYSIS; PROTEIN HYDROLYSATE; SARDINELLA;

PROTEINS;

EID: 84994462243     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2016.08.020     Document Type: Article

References (81)

1. Abdelhedi, O., Jridi, M., Jemil, I., Mora, L., Toldrá, F., Aristoy, M.C., et al. Combined biocatalytic conversion of smooth hound viscera: Protein hydrolysates elaboration and assessment of their antioxidant, anti-ACE and antibacterial activities. Food Research International 86 (2016), 9–23.
2. Agrebi, R., Haddar, A., Hajji, M., Frikha, F., Manni, L., Jellouli, K., et al. Fibrinolytic enzymes from a newly isolated marine bacterium Bacillus subtilis A26: Characterization and statistical media optimization. Canadian Journal of Microbiology 55 (2009), 1049–1061.
3. Agrebi, R., Hmidet, N., Hajji, M., Ktari, N., Haddar, A., Fakhfakh-Zouari, N., et al. Fibrinolytic serine-protease from Bacillus amyloliquefaciens An6 grown on Mirabilis jalapa tuber powders: Production, partial purification and biochemical characterization. Applied Biochemistry and Biotechnology 162 (2010), 75–88.
4. Alemán, A., Pérez-Santin, E., Bordenave-Juchereau, S., Arnaudin, I., Gomez-Guillén, M.C., Montero, P., Squid gelatin hydrolysates with antihypertensive, anticancer and antioxidant activity. Food Research International 44 (2011), 1044–1051.
5. AOAC, Official methods of analysis. 17th edn, 2000, Association of Official Analytical Chemists, Washington.
6. Ben Khaled, H., Ktari, N., Ghorbel-Bellaaj, O., Jridi, M., Lassoued, I., Nasri, M., Composition, functional properties and in vitro antioxidant activity of protein hydrolysates prepared from sardinelle (Sardinella aurita) muscle. Journal of Food Science and Technology 51 (2014), 622–633.
7. Bersuder, P., Hole, M., Smith, G., Antioxidants from a heated histidine–glucose model system. I. Investigation of the antioxidant role of histidine and isolation of antioxidants by high performance liquid chromatography. Journal of the American Oil Chemists' Society 75 (1998), 181–187.
8. Bkhairia, I., Ben Slama-Ben Salem, R., Nasri, R., Jridi, M., Ghorbel, S., Nasri, M., In vitro antioxidant and functional properties of protein hydrolysates from golden grey mullet prepared by commercial, microbial and visceral proteases. Journal of Food Science and Technology, 2016, 10.1007/s13197-016-2200-5.
9. Chakka, A.K., Elias, M., Jini, R., Sakhare, P.Z., Bhaskar, N., In-vitro antioxidant and antibacterial properties of fermentatively and enzymatically prepared chicken liver protein hydrolysates. Journal of Food Science and Technology 52 (2015), 8059–8067.
10. Chi, C.F., Hu, F.Y., Wang, B., Ren, X.J., Deng, S.G., Wu, C.W., Purification and characterization of three antioxidant peptides from protein hydrolyzate of croceine croaker (Pseudosciaena crocea) muscle. Food Chemistry 168 (2014), 662–667.
11. Connolly, T.M., Condra, C., Feng, D.M., Cook, J.J., Stranieri, M.T., Reilly, C.F., et al. Species variability in platelet and other cellular responsiveness to thrombin receptor-derived peptides. Thrombosis and Haemostasis 72 (1994), 627–633.
12. Cooper, W.O., Hernandez-Diaz, S., Arbogast, P.G., Dudley, J.A., Dyer, S., Gideon, P.S., et al. Major congenital malformations after first-trimester exposure to ACE inhibitors. New England Journal of Medicine 354 (2006), 2443–2451.
13. Dávalos, A., Gómez-Cordovés, C., Bartolomé, B., Extending applicability of the oxygen radical absorbance capacity (ORAC − Fluorescein) assay. Journal of Agricultural and Food Chemistry 52 (2004), 48–54.
14. Dávalos, A., Miguel, M., Bartolomé, B., López-Fandino, R., Antioxidant activity of peptides derived from egg white proteins by enzymatic hydrolysis. Journal of Food Protection 67 (2004), 1939–1944.
15. Dinis, T.C., Maderia, V.M., Almeida, L.M., Action of phenolic derivatives (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Archives Biochemistry Biophysics 315 (1994), 161–169.
16. Dong, S., Zeng, M., Wang, D., Liu, Z., Zhao, Y., Yang, H., Antioxidant and biochemical properties of protein hydrolysates prepared from silver carp (Hypophthalmichthys molitrix). Food Chemistry 107 (2008), 1485–1493.
17. Escudero, E., Mora, L., Fraser, P.D., Aristoy, M.C., Arihara, K., Toldra, F., Purification and identification of antihypertensive peptides in Spanish dry-cured ham. Journal of Proteomics 78 (2013), 499–507.
18. Esteve, C., Marina, M.L., García, M.C., Novel strategy for the revalorization of olive (Olea europaea) residues based on the extraction of bioactive peptides. Food Chemistry 167 (2015), 272–280.
19. Euston, S.R., Finnigan, S.R., Hirst, R.L., Heat-induced destabilization of oil-in-water emulsions formed from hydrolyzed whey protein. Journal of Agricultural and Food Chemistry 49 (2001), 5576–5583.
20. Fakhfakh, N., Ktari, N., Siala, R., Nasri, M., Wool-waste valorization: Production of protein hydrolysate with high antioxidative potential by fermentation with a new keratinolytic bacterium, Bacillus pumilus A1. Journal of Applied Microbiology 115 (2013), 424–433.
21. Garber, D.W., Handattu, S.P., Datta, G., Mishra, V.K., Gupta, H., White, R., et al. Atherosclerosis and vascular disease: Effects of peptide mimetics of apoliproteins. Current Pharmaceutical Biotechnology 7 (2006), 235–240.
22. Gobbetti, M., Ferranti, P., Smacchi, E., Goffredi, F., Addeo, F., Production of angiotensin-I-converting-enzyme-inhibitory peptides in fermented milks started by Lactobacillus delbrueckii subsp. bulgaricus SS1 and Lactococcus lactis subsp. cremoris FT4. Applied and Environmental Microbiology 66 (2000), 3898–3904.
23. Gu, R.Z., Li, C.Y., Liu, W.Y., Yi, W.X., Cai, M.Y., Angiotensin I-converting enzyme inhibitory activity of low-molecular-weight peptides from Atlantic salmon (Salmo salar L.) skin. Food Research International 44 (2011), 1536–1540.
24. Harnedy, P.A., O'Keeffe, M.B., FitzGerald, R.J., Purification and identification of dipeptidyl peptidase (DPP) IV inhibitory peptides from the macroalga Palmaria palmata. Food Chemistry 172 (2015), 400–406.
25. Harris, T., Cook, E.F., Kannel, W., Schatzkin, A., Goldman, L., Blood pressure experience and risk of cardiovascular disease in the elderly. Hypertension 7 (1985), 118–124.
26. He, H.L., Liu, D., Ma, C.B., Review on the angiotensin-I-converting enzyme (ACE) inhibitor peptides from marine proteins. Applied Biochemistry and Biotechnology 169 (2013), 738–749.
27. Hernandez-Ledesma, B., Amigo, L., Recio, I., Bartolome, B., ACE-inhibitory and radical scavenging activity of peptides derived from beta-lactoglobulin f(19–25). Interactions with ascorbic acid. Journal of Agricultural and Food Chemistry 55 (2007), 3392–3397.
28. Houston, M.C., Nutraceuticals, vitamins, antioxidants, and minerals in the prevention and treatment of hypertension. Progress in Cardiovascular Diseases 47 (2005), 396–449.
29. Ishida, A., Shigeri, Y., Tatsu, Y., Uegaki, K., Kameshita, I., Okuno, S., et al. Critical amino acid residues of AIP, a highly specific inhibitory peptide of calmodulin-dependent protein kinase II. FEBS Letters 427 (1998), 115–118.
30. Jemil, I., Abdelhedi, O., Nasri, R., Mora, L., Marrekchi, R., Jamoussi, K., et al. Hypolipidemic, antiobesity and cardioprotective effects of fermented protein hydrolysates from sardinelle (Sardinella aurita) in high-fat and fructose diet fed Wistar rats. Life Sciences, 2016, 10.1016/j.lfs.2016.07.012.
31. Jemil, I., Jridi, M., Nasri, R., Ktari, N., Ben Slama-Ben Salem, R., Hajji, M., et al. Functional, antioxidant and antibacterial properties of protein hydrolysates prepared from fish meat fermented by Bacillus subtilis A26. Process Biochemistry 49 (2014), 963–972.
32. Jiménez-Escrig, A., Alaiz, M., Vioque, J., Rupérez, P., Health-promoting activities of ultra-filtered okara protein hydrolysates released by in vitro gastrointestinal digestion: identification of active peptide from soybean lipoxygenase. European Food Research and Technology 230 (2010), 655–663.
33. Katayama, K., Anggraeni, H.E., Mori, T., Ahmed, A.M., Kawahara, S., Sugiyama, M., et al. Porcine skeletal muscle troponin is a good source of peptides with angiotensin-I converting enzyme inhibitory activity and antihypertensive effects in spontaneously hypertensive rats. Journal of Agricultural and Food Chemistry 56 (2008), 355–360.
34. Kleekayai, T., Harnedy, P.A., O'Keeffe, M.B., Poyarkov, A.A., Cunha Neves, A.A., Suntornsuk, W.W., et al. Extraction of antioxidant and ACE inhibitory peptides from Thai traditional fermented shrimp pastes. Food Chemistry 176 (2015), 441–447.
35. Klompong, V., Benjakul, S., Kantachote, D., Hayes, K.D., Shahidi, F., Comparative study on antioxidative activity of yellow stripe trevally protein hydrolysate produced from Alcalase and Flavourzyme. International Journal of Food Science and Technology 43 (2008), 1019–1026.
36. Kohmura, M., Nio, N., Kubo, K., Minoshimo, Y., Munekata, E., Ariyoshi, Y., Inhibition of angiotensin-converting enzyme by synthetic peptides of human beta-casein. Agricultural and Biological Chemistry 53 (1989), 2107–2114.
37. Koleva, I.I., Van Beek, T.A., Linssen, J.P.H., De Groot, A., Evstatieva, L.N., Screening of plant extracts for antioxidant activity: A comparative study on three testing methods. Phytochemical Analysis 13 (2002), 8–17.
38. Kumazawa, S., Taniguchi, M., Suzuki, Y., Shimura, M., Kwon, M.S., Nakayama, T., Antioxidant activity of polyphenols in carob pods. Journal of Agricultural and Food Chemistry 50 (2002), 373–377.
39. Lassoued, I., Mora, L., Nasri, R., Aydi, M., Toldrá, F., Aristoy, M.C., et al. Characterization, antioxidative and ACE inhibitory properties of hydrolysates obtained from thornback ray (Raja clavata) muscle. Journal of Proteomics 128 (2015), 458–468.
40. Lavoie, J.L., Sigmund, C.D., Minireview: Overview of the renin-angiotensin system; An endocrine and paracrine system. Endocrinology 144 (2003), 2179–2183.
41. Lee, N.Y., Cheng, J.T., Enomoto, T., Nakano, Y., One peptide derived from hen ovotransferrin as pro-drug to inhibit angiotensin converting enzyme. Journal of Food and Drug Analysis 14 (2006), 31–35.
42. Liu, R., Zheng, W., Li, J., Wang, L., Wu, H., Wang, X., et al. Rapid identification of bioactive peptides with antioxidant activity from the enzymatic hydrolysate of Mactra veneriformis by UHPLC–Q-TOF mass spectrometry. Food Chemistry 167 (2015), 484–489.
43. Liu, X., Zhang, M., Jia, A., Zhang, Y., Zhu, H., Zhang, C., et al. Purification and characterization of angiotensin I converting enzyme inhibitory peptides from jellyfish Rhopilema esculentun. Food Research International 50 (2013), 339–343.
44. Maruyama, S., Mitachi, H., Tanaka, H., Tomizuka, N., Suzuki, H., Angiotensin-I converting enzyme inhibitory activity of the C-terminal hexapeptide of alpha-casein. Agricultural and Biological Chemistry 51 (1987), 2557–2561.
45. Mito, K., Fujii, M., Kuwahara, M., Matsumura, N., Shimizu, T., Sugano, S., et al. Antihypertensive effect of angiotensin I-converting enzyme inhibitory peptides derived from hemoglobin. European Journal of Pharmacology 304 (1996), 93–98.
46. Miyoshi, S., Ishikawa, H., Kaneko, T., Fukui, F., Tanaka, H., Structure and activity of angiotensin-converting enzyme inhibitors in alpha-zein hydrolysate. Agricultural and Biological Chemistry 55 (1991), 1313–1318.
47. Mojica, L., Chen, K., de Mejia, E.G., Impact of commercial precooking of common bean (Phaseolus vulgaris) on the generation of peptides, after pepsin-pancreatin hydrolysis, capable to inhibit dipeptidyl peptidase-IV. Journal of Food Science 80 (2015), 188–198.
48. Mora, L., Escudero, E., Aristoy, M.C., Toldrá, F., A peptidomic approach to study the contribution of added casein proteins to the peptide profile in Spanish dry-fermented sausages. International Journal of Food Microbiology 212 (2015), 41–48.
49. Morales-Medina, R., Tamm, F., Guadix, A.M., Guadix, E.M., Drusch, S., Functional and antioxidant properties of hydrolysates of sardine (S. pilchardus) and horse mackerel (T. mediterraneus) for the microencapsulation of fish oil by spray-drying. Food Chemistry 194 (2016), 1208–1216.
50. Murase, H., Nagao, A., Terao, J., Antioxidant and emulsifying activity of N-(long-chain-acyl) histidine and N-(long-chain-acyl) carnosine. Journal of Agricultural and Food Chemistry 41 (1993), 1601–1604.
51. Murray, B.A., Fitz Gerald, R.J., Angiotensin converting enzyme inhibitory peptides derived from food proteins: biochemistry, bioactivity and production. Current Pharmaceutical Design 13 (2007), 773–791.
52. Nasri, R., Jridi, M., Lassoued, I., Jemil, I., Ben Slama-Ben Salem, R., Nasri, M., et al. The influence of the extent of enzymatic hydrolysis on antioxidative properties and ACE-inhibitory activities of protein hydrolysates from goby (Zosterisessor ophiocephalus) muscle. Applied Biochemistry and Biotechnology 173 (2014), 1121–1134.
53. Nasri, R., Younes, I., Jridi, M., Trigui, M., Bougatef, A., Nedjar-Arroume, N., et al. ACE inhibitory and antioxidative activities of goby (Zosterissessor ophiocephalus) fish protein hydrolysates: Effect on meat lipid oxidation. Food Research International 54 (2013), 552–561.
54. Nielsen, P.M., Petersen, D., Dambmann, C., Improved method for determining food protein degree of hydrolysis. Journal of Food Science 66 (2001), 642–646.
55. Park, P.J., Jung, W.K., Nam, K.S., Shahidi, F., Kim, S.K., Purification and characterization of antioxidative peptides from protein hydrolysate of lecithin free egg yolk. Journal of the American Oil Chemists' Society 78 (2001), 651–656.
56. Pihlanto-Leppala, A., Koskinen, P., Piilola, K., Tupasela, T., Korhonen, H., Angiotensin I-converting enzyme inhibitory properties of whey protein digests: Concentration and characterization of active peptides. Journal of Dairy Research 67 (2000), 53–64.
57. Qian, Z.J., Jung, W.K., Kim, S.K., Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin, Rana catesbeiana Shaw. Bioresource Technology 99 (2008), 1690–1698.
58. Ringseis, R., Motthes, B., Lehmann, V., Becker, K., Schöps, R., Ulbrich-Hofmann, R., et al. Peptides and hydrolysates from casein and soy protein modulate the release of vasoactive substances from human aortic endothelial cells. Biochimica et Biophysica Acta-General Subjects 1721 (2005), 89–97.
59. Saiga, A., Tanabe, S., Nishimura, T., Antioxidant activity of peptides obtained from porcine myofibrillar proteins by protease treatment. Journal of Agricultural and Food Chemistry 51 (2003), 3661–3667.
60. Salampessy, J., Reddy, N., Kailasapathy, K., Phillips, M., Functional and potential therapeutic ACE-inhibitory peptides derived from bromelain hydrolysis of trevally proteins. Journal of Functional Foods 14 (2015), 716–725.
61. Salvetti, A., Newer ACE inhibitors. A look at the future. Drugs 40 (1990), 800–828.
62. Sentandreu, M.A., Toldrá, F., A rapid, simple and sensitive fluorescence method for the assay of angiotensin-I converting enzyme. Food Chemistry 97 (2006), 546–554.
63. Shimada, K., Fujikawa, K., Yahara, K., Nakamura, T., Antioxidative properties of xanthan on the antioxidation of soybean oil in cyclodextrin emulsion. Journal of Agricultural and Food Chemistry 40 (1992), 945–948.
64. Shimizu, M., Tsunogai, M., Arai, S., Transepithelial transport of oligopeptides in the human intestinal cell, Caco-2. Peptides 18 (1997), 681–687.
65. Silveira, S.T., Martínez-Maqueda, D., Recio, I., Hernández-Ledesma, B., Dipeptidyl peptidase-IV inhibitory peptides generated by tryptic hydrolysis of a whey protein concentrate rich in β-lactoglobulin. Food Chemistry 141 (2013), 1072–1077.
66. Srinivas, S., Prakash, V., Effect of cosolvents on the stabilization of bioactive peptides from bovine milk α-casein. Protein and Peptide Letters 15 (2008), 371–376.
67. Stohs, S.J., Bagchi, D., Oxidative mechanisms in the toxicity of metal ions. Free Radical Biology and Medicine 18 (1995), 321–336.
68. Sudhakar, S., Abdul Nazeer, R., Preparation of potent antioxidant peptide from edible part of shortclub cuttlefish against radical mediated lipid and DNA damage. LWT-Food Science and Technology 64 (2015), 593–601.
69. Suryakanth, D.A., Rafiq, M., Azeemuddin, M., Vis-wanatha, G.L., Jagadeesh, M., Sandeep Rao, K.S., et al. Free radical scavenging and hepatoprotective activity of HD-03/ES in experimental models. Journal of Experimental and Integrative Medicine 2 (2012), 161–166.
70. Thiansilakul, Y., Benjakul, S., Shahidi, F., Compositions, functional properties and antioxidative activity of protein hydrolysates prepared from round scad (Decapterus maruadsi). Food Chemistry 103 (2007), 1385–1394.
71. Tomatsu, M., Shimakage, A., Shinbo, M., Yamada, S., Takahashi, S., Novel angiotensin I-converting enzyme inhibitory peptides derived from soya milk. Food Chemistry 136 (2013), 612–616.
72. Toopcham, T., Roytrakul, S., Yongsawatdigul, J., Characterization and identification of angiotensin I-converting enzyme (ACE) inhibitory peptides derived from tilapia using Virgibacillus halodenitrificans SK1-3-7 proteinases. Journal of Functional Foods 14 (2015), 435–444.
73. Torino, M.I., Limón, R.I., Martínez-Villaluenga, C., Mäkinen, S., Pihlanto, A., Vidal-Valverde, C., et al. Antioxidant and antihypertensive properties of liquid and solid state fermented lentils. Food Chemistry 136 (2013), 1030–1037.
74. Tsopmo, A., Romanowski, A., Banda, L., Lavoie, J.C., Jenssen, H., Novel anti-oxidative peptides from enzymatic digestion of human milk. Food Chemistry 126 (2011), 1138–1143.
75. Uchida, K., Kawakishi, S., Sequence-dependant reactivity of histidine containing peptides with copper(II)/ascorbate. Journal of Agricultural and Food Chemistry 40 (1992), 13–16.
76. Wu, X.L., Beecher, G.R., Holden, J.M., Haytowitz, D.B., Gebhardt, S.E., Prior, R.I., Lipophilic and hydrophilic antioxidant capacities of common foods in the United States. Journal of Agricultural and Food Chemistry 52 (2004), 4026–4037.
77. Xu, B.J., Yuan, S.H., Chang, S.K.C., Comparative analyses of phenolic composition and antioxidant capacity of cool season legumes with others elected food legumes. Journal of Food Science 72 (2007), 167–177.
78. Yano, S., Suzuki, K., Funatsu, G., Isolation from alpha-zein of thermolysin peptides with angiotensin I-converting enzyme inhibitory activity. Bioscience, Biotechnology, and Biochemistry 60 (1996), 661–663.
79. Yeh, C.H., Peng, H.C., Yih, J.B., Huang, T.F., A new short chain RGD-containing disintegrin, accutin, inhibits the common pathway of human platelet aggregation. Biochimica et Biophysica Acta 1425 (1995), 493–504.
80. Yildirim, A., Mavi, A., Kara, A.A., Determination of antioxidant and antimicrobial activities of Rumex crispus L. Extracts. Journal of Agricultural and Food Chemistry 49 (2001), 4083–4089.
81. Zambrowicz, A., Pokora, M., Setner, B., Dąbrowska, A., Szołtysik, M., Babij, K., et al. Multifunctional peptides derived from an egg yolk protein hydrolysate: Isolation and characterization. Amino Acid 47 (2015), 369–380.