Peptide identification in a porcine gelatin prolyl endoproteinase hydrolysate with angiotensin converting enzyme (ACE) inhibitory and hypotensive activity

Journal of Functional Foods

Volumn 34, Issue , 2017, Pages 77-88

  O'Keeffe, Martina B ^a   Norris, Roseanne ^a   Alashi, Monisola A ^b   Aluko, Rotimi E ^b   FitzGerald, Richard J ^a  

^a UNIVERSITY OF LIMERICK   (Ireland)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Angiotensin converting enzyme; Aspergillus niger prolyl endoproteinase (An PEP); Bioactive peptides; Gelatin hydrolysate; LC MS; Protein hydrolysate; Spontaneously hypertensive rats

Indexed keywords

EID: 85018468682     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2017.04.018     Document Type: Article

References (43)

1. Adler-Nissen, J., A review of food hydrolysis specific areas. Adler-Nissen, J., (eds.) Enzymatic hydrolysis of food proteins, 1986, Elsevier Applied Science Publishers, New York, 57–109.
2. Alemán, A., Pérez-Santín, E., Bordenave-Juchereau, S., Arnaudin, I., Gómez-Guillén, M.C., Montero, P., Squid gelatin hydrolysates with antihypertensive, anticancer and antioxidant activity. Food Research International 44:4 (2011), 1044–1051.
3. Byun, H.-G., Kim, S.-K., Purification and characterization of angiotensin I converting enzyme (ACE) inhibitory peptides from Alaska pollack (Theragra chalcogramma) skin. Process Biochemistry 36:12 (2001), 1155–1162.
4. Byun, H.-G., Kim, S.-K., Structure and activity of angiotensin I converting enzyme inhibitory peptides derived from Alaskan pollack skin. BMB Reports 35:2 (2002), 239–243.
5. Connolly, A., O'Keeffe, M.B., Piggott, C.O., Nongonierma, A.B., FitzGerald, R.J., Generation and identification of angiotensin converting enzyme (ACE) inhibitory peptides from a brewers’ spent grain protein isolate. Food Chemistry 176 (2015), 64–71.
6. Edens, L., Dekker, P., van der Hoeven, R., Deen, F., de Roos, A., Floris, R., Extracellular prolyl endoprotease from Aspergillus niger and its use in the debittering of protein hydrolysates. Journal of Agricultural and Food Chemistry 53:20 (2005), 7950–7957.
7. Edens, L., Roos, A. L., & Van Platerlink, C. (2009). Blood pressure lowering protein hydrolysates. US Patent 0042809 A1.
8. Faria, M., da Costa, E.L., Gontijo, J.A.R., Netto, F.M., Evaluation of the hypotensive potential of bovine and porcine collagen hydrolysates. Journal of Medicinal Food 11:3 (2008), 560–567.
9. Gómez-Guillén, M.C., Giménez, B., López-Caballero, M.E., Montero, M.P., Functional and bioactive properties of collagen and gelatin from alternative sources: A review. Food Hydrocolloids 25:8 (2011), 1813–1827.
10. Harnedy, P.A., FitzGerald, R.J., In vitro assessment of the cardioprotective, anti-diabetic and antioxidant potential of Palmaria palmata protein hydrolysates. Journal of Applied Phycology 25 (2013), 1793–1803.
11. Herregods, G., Van Camp, J., Morel, N., Ghesquière, B., Gevaert, K., Vercruysse, L., Smagghe, G., Angiotensin I-converting enzyme inhibitory activity of gelatin hydrolysates and identification of bioactive peptides. Journal of Agricultural and Food Chemistry 59:2 (2011), 552–558.
12. Ichimura, T., Yamanaka, A., Otsuka, T., Yamashita, E., Maruyama, S., Antihypertensive effect of enzymatic hydrolysate of collagen and Gly-Pro in spontaneously hypertensive rats. Bioscience, Biotechnology, and Biochemistry 73:10 (2009), 2317–2319.
13. Iwai, K., Hasegawa, T., Taguchi, Y., Morimatsu, F., Sato, K., Nakamura, Y., Ohtsuki, K., Identification of food-derived collagen peptides in human blood after oral ingestion of gelatin hydrolysates. Journal of Agricultural and Food Chemistry 53:16 (2005), 6531–6536.
14. Kim, S.-K., Byun, H.-G., Park, P.-J., Shahidi, F., Angiotensin I converting enzyme inhibitory peptides purified from bovine skin gelatin hydrolysate. Journal of Agricultural and Food Chemistry 49:6 (2001), 2992–2997.
15. Kleekayai, T., Harnedy, P.A., O'Keeffe, M.B., Poyarkov, A.A., CunhaNeves, A., Suntornsuk, W., FitzGerald, R.J., Extraction of antioxidant and ACE inhibitory peptides from Thai traditional fermented shrimp pastes. Food Chemistry 176 (2015), 441–447.
16. Lin, L., Lv, S., Li, B., Angiotensin-I-converting enzyme (ACE)-inhibitory and antihypertensive properties of squid skin gelatin hydrolysates. Food Chemistry 131:1 (2012), 225–230.
17. Ma, B., Zhang, K., Hendrie, C., Liang, C., Li, M., Doherty-Kirby, A., Lajoie, G., PEAKS: Powerful software for peptide de novo sequencing by tandem mass spectrometry. Rapid Communications in Mass Spectrometry 17:20 (2003), 2337–2342.
18. Makinen, S., Kelloniemi, J., Pihlanto, A., Makinen, K., Korhonen, H., Hopia, A., Valkonen, J.P., Inhibition of angiotensin converting enzyme I caused by autolysis of potato proteins by enzymatic activities confined to different parts of the potato tuber. Journal of Agriculture and Food Chemistry 56:21 (2008), 9875–9883.
19. Meng, Q.C., Balcells, E., Dell'Italia, L., Durand, J., Oparil, S., Sensitive method for quantitation of angiotensin-converting enzyme (ACE) activity in tissue. Biochemical Pharmacology 50:9 (1995), 1445–1450.
20. Miguel, M., Contreras, M.M., Recio, I., Aleixandre, A., ACE-inhibitory and antihypertensive properties of a bovine casein hydrolysate. Food Chemistry 112:1 (2009), 211–214.
21. Mine, Y., Li-Chan, E.C.Y., Jiang, B., Biologically active food proteins and peptides in health: An overview bioactive proteins and peptides as functional foods and nutraceuticals. 2010, Wiley-Blackwell, 3–11.
22. Minkiewicz, P., Dziuba, J., Iwaniak, A., Dziuba, M., Darewicz, M., BIOPEP database and other programs for processing bioactive peptide sequences. Journal of AOAC International 91:4 (2008), 965–980.
23. Ngo, D.-H., Kang, K.-H., Ryu, B., Vo, T.-S., Jung, W.-K., Byun, H.-G., Kim, S.-K., Angiotensin-I converting enzyme inhibitory peptides from antihypertensive skate (Okamejei kenojei) skin gelatin hydrolysate in spontaneously hypertensive rats. Food Chemistry 174 (2015), 37–43.
24. Nongonierma, A.B., O'Keeffe, M.B., FitzGerald, R.J., Milk protein hydrolysates and bioactive peptides. McSweeney, P.L.H., O'Mahony, J.A., (eds.) Advanced dairy chemistry, 2016, Springer, New York, 417–482.
25. Norris, R., Casey, F., FitzGerald, R.J., Shields, D., Mooney, C., Predictive modelling of angiotensin converting enzyme inhibitory dipeptides. Food Chemistry 133:4 (2012), 1349–1354.
26. Norris, R., O'Keeffe, M.B., Poyarkov, A., FitzGerald, R.J., Peptide identification and angiotensin converting enzyme (ACE) inhibitory activity in prolyl endoproteinase digests of bovine αs-casein. Food Chemistry 188 (2015), 210–217.
27. Norris, R., Poyarkov, A., O'Keeffe, M.B., FitzGerald, R.J., Characterisation of the hydrolytic specificity of Aspergillus niger derived prolyl endoproteinase on bovine β-casein and determination of ACE inhibitory activity. Food Chemistry 156 (2014), 29–36.
28. O'Keeffe, M.B., FitzGerald, R.J., Identification of short peptide sequences in complex milk protein hydrolysates. Food Chemistry 184 (2015), 140–146.
29. Pripp, A., Isaksson, T., Stepaniak, L., Sørhaug, T., Quantitative structure-activity relationship modelling of ACE-inhibitory peptides derived from milk proteins. European Food Research and Technology 219:6 (2004), 579–583.
30. Ramshaw, J.A., Shah, N.K., Brodsky, B., Gly-X-Y tripeptide frequencies in collagen: A context for host-guest triple-helical peptides. Journal of Structural Biology 122:1–2 (1998), 86–91.
31. Russell, J.D., Dolphin, J.M., Koppang, M.D., Selective analysis of secondary amino acids in gelatin using pulsed electrochemical detection. Analytical Chemistry 79:17 (2007), 6615–6621.
32. Sagardia, I., Roa-Ureta, R.H., Bald, C., A new QSAR model, for angiotensin I-converting enzyme inhibitory oligopeptides. Food Chemistry 136:3–4 (2013), 1370–1376.
33. Saiga, A., Iwai, K., Hayakawa, T., Takahata, Y., Kitamura, S., Nishimura, T., Morimatsu, F., Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate. Journal of Agricultural and Food Chemistry 56:20 (2008), 9586–9591.
34. Sebela, M., Rehulka, P., Kabrt, J., Rehulkova, H., Ozdian, T., Raus, M., Chmelik, J., Identification of N-glycosylation in prolyl endoprotease from Aspergillus niger and evaluation of the enzyme for its possible application in proteomics. Journal of Mass Spectrometry 44:11 (2009), 1587–1595.
35. Sentandreu, M.A., Toldra, F., A fluorescence-based protocol for quantifying angiotensin-converting enzyme activity. Nature Protocols 1:5 (2006), 2423–2427.
36. Spellman, D., Kenny, P., O'Cuinn, G., FitzGerald, R.J., Aggregation properties of whey protein hydrolysates generated with Bacillus licheniformis proteinase activities. Journal of Agricultural and Food Chemistry 53:4 (2005), 1258–1265.
37. Spellman, D., O'Cuinn, G., FitzGerald, R.J., Bitterness in Bacillus proteinase hydrolysates of whey proteins. Food Chemistry 114:2 (2009), 440–446.
38. Taga, Y., Kusubata, M., Ogawa-Goto, K., Hattori, S., Efficient absorption of X-hydroxyproline (Hyp)-Gly after oral administration of a novel gelatin hydrolysate prepared using ginger protease. Journal of Agricultural and Food Chemistry 64:14 (2016), 2962–2970.
39. Vermeirssen, V., Van Camp, J., Verstraete, W., Bioavailability of angiotensin I converting enzyme inhibitory peptides. British Journal of Nutrition 92:03 (2004), 357–366.
40. Wu, J., Aluko, R.E., Nakai, S., Structural requirements of angiotensin I-converting enzyme inhibitory peptides: Quantitative structure−activity relationship study of di- and tripeptides. Journal of Agricultural and Food Chemistry 54:3 (2006), 732–738.
41. Zhang, G., Liu, T., Wang, Q., Chen, L., Lei, J., Luo, J., Su, Z., Mass spectrometric detection of marker peptides in tryptic digests of gelatin: A new method to differentiate between bovine and porcine gelatin. Food Hydrocolloids 23:7 (2009), 2001–2007.
42. Zhao, Y., Li, B., Liu, Z., Dong, S., Zhao, X., Zeng, M., Antihypertensive effect and purification of an ACE inhibitory peptide from sea cucumber gelatin hydrolysate. Process Biochemistry 42:12 (2007), 1586–1591.
43. Zhuang, Y., Sun, L., Zhang, Y., Liu, G., Antihypertensive effect of long-term oral administration of jellyfish (Rhopilema esculentum) collagen peptides on renovascular hypertension. Marine Drugs, 10(2), 2012, 417.