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Identification of ACE inhibitory peptides from red alga Mazzaella japonica

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Abstract

Angiotensin I converting enzyme (ACE) inhibition is one of the key factors for cardiovascular disease, and inhibition of ACE activity is related to the prevention of high blood pressure. Until now, some ACE inhibitory peptides have been found in the protein hydrolysates of red algae, and most of them were derived from phycobiliproteins and rubisco. In this study, we modified the preparation method to evaluate the potential of ACE inhibitory activity from protein hydrolysate of red alga Mazzaella japonica except for phycobiliproteins and rubisco. As a result, we identified 11 peptides (YRD, VSEGLD, TIMPHPR, GGPAT, SSNDYPI, SRIYNVKSNG, VDAHY, CPYDWV, YGDPDHY, NLGN and DFGVPGHEP) in the hydrolysate by the reversed phase-HPLC and MALDI-TOF/MS/MS. Among them, YRD would be derived from phycoerythrin α-subunit. However, the others would be from other proteins encoded in chloroplast or nuclear genomes. This study revealed that not only phycobiliproteins and rubisco but also the other proteins in red algae have the potential for the source of ACE inhibitory peptide.

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References

  1. World Health Organization. https://www.who.int

  2. Tsai JS, Lin TC, Chen JL, Pan BS (2017) The inhibitory effects of freshwater clam (Corbicula fluminea, Muller) muscle protein hydrolysates on angiotensin I converting enzyme. Process Biochem 41:2276–2281

    Article  Google Scholar 

  3. Chen J, Wang Y, Ye R, Wu Y, Xia W (2013) Comparison of analytical methods to assay inhibitors of angiotensin I-converting enzyme. Food Chem 141:3329–3334

    Article  CAS  Google Scholar 

  4. Sweitzer NK (2003) What is an angiotensin converting enzyme inhibitor? Circulation 108:E16–E18

    Article  Google Scholar 

  5. Tu M, Cheng S, Lu W, Du M (2018) Advancement and prospects of bioinformatics analysis for studying bioactive peptides from food-derived protein: Sequence, structure, and functions. Trac-Trend Anal Chem 105:7–17

    Article  CAS  Google Scholar 

  6. Li G-H, Le G-W, Shi Y-H, Shrestha S (2004) Angiotensin I–converting enzyme inhibitory peptides derived from food proteins and their physiological and pharmacological effects. Nutr Res 24:469–486

    Article  CAS  Google Scholar 

  7. Balti R, Bougatef A, Sila A, Guillochon D, Dhulster P, Nedjar-Arroume N (2015) Nine novel angiotensin I-converting enzyme (ACE) inhibitory peptides from cuttlefish (Sepia officinalis) muscle protein hydrolysates and antihypertensive effect of the potent active peptide in spontaneously hypertensive rats. Food Chem 170:519–525

    Article  CAS  Google Scholar 

  8. García-Moreno PJ, Espejo-Carpio FJ, Guadix A, Guadix EM (2015) Production and identification of angiotensin I-converting enzyme (ACE) inhibitory peptides from Mediterranean fish discards. J Funct Foods 18:95–105

    Article  Google Scholar 

  9. Amado IR, Vázquez JA, González P, Esteban-Fernández D, Carrera M, Piñeiro C (2014) Identification of the major ACE-inhibitory peptides produced by enzymatic hydrolysis of a protein concentrate from cuttlefish wastewater. Mar Drugs 12:1390–1405

    Article  CAS  Google Scholar 

  10. Ghassem M, Babji AS, Said M, Mahmoodani F, Aeihara K (2014) Angiotensin I-converting enzyme inhibitory peptides from snakehead fish sarcoplasmic protein hydrolysate. J Food Biochem 38:140–149

    Article  CAS  Google Scholar 

  11. Harnedy P-A, FitzGerald R-J (2011) Bioactive proteins, peptides, and amino acid from macroalgae. J Appl Phycol 47:218–232

    Article  CAS  Google Scholar 

  12. Sato M, Hosokawa T, Yamaguchi T, Nakano T, Muramoto K, Kahara T, Funayama K, Kobayashi A, Nakano T (2002) Angiotensin I-converting enzyme inhibitory peptides derived from wakame (Undaria pinnatifida) and their antihypertensive effect in spontaneously hypertensive rats. J Agric Food Chem 50:6245–6252

    Article  CAS  Google Scholar 

  13. Suetsuna K, Maekawa K, Chen J-R (2004) Antihypertensive effects of Undaria pinnatifida (wakame) peptide on blood pressure in spontaneously hypertensive rats. J Nutr Biochem 15:267–272

    Article  CAS  Google Scholar 

  14. Cha S-H, Lee K-W, Jeon Y-J (2006) Screening of extracts from red algae in Jeju for potentials marine angiotensin-I converting enzyme (ACE) inhibitory activity. Algae 21:343–348

    Article  Google Scholar 

  15. He H-L, Chen X-L, Wu H, Sun C-Y, Zhang Y-Z, Zhou B-C (2007) High throughput and rapid screening of marine protein hydrolysates enriched in peptides with angiotensin-I-converting enzyme inhibitory activity by capillary electrophoresis. Bioresour Thechnol 98:3499–3505

    Article  CAS  Google Scholar 

  16. Cian RE, Alaiz M, Vioque J, Drago SR (2013) Enzyme proteolysis enhanced extraction of ACE inhibitory and antioxidant compounds (peptides and polyphenols) from Porphyra columbina residual cake. J Appl Phycol 25:1197–1206

    Article  CAS  Google Scholar 

  17. Fitzgerald C, Aluko RE, Hossain M et al (2014) Potential of a renin inhibitory peptide from the red seaweed Palmaria palmata as a functional food ingredient following confirmation and characterization of a hypotensive effect in spontaneously hypertensive rats. J Agric Food Chem 62:8352–8356

    Article  CAS  Google Scholar 

  18. Cian R, Garzón A-G, Ancona D-B, Guerrero L-C, Drago S (2015) Hydrolyzates from Pyropia columbina seaweed have antiplatelet aggregation, antioxidant and ACE I inhibitory peptides which maintain bioactivity after simulated gastrointestinal digestion. LWT-Food Sci Technol 64:881–888

  19. Cao D, Lv X, Xu X, Yu H, Sun X, Xu N (2017) Purification and identification of a novel ACE inhibitory peptide from marine alga Gracilariopsis lemaneiformis protein hydrolysate. Eur Food Res Technol 243:1829–1837

    Article  CAS  Google Scholar 

  20. Admassu H, Gasmalla MAA, Yang R, Zhao W (2018) Identification of bioactive peptides with α-amylase inhibitory potential from enzymatic protein hydrolysates of red seaweed (Porphyra spp). J Agric Food Chem 66:4872–4882

    Article  CAS  Google Scholar 

  21. Cermeño M, Stack J, Tobin P-R, O'Keeffe M-B, Harnedy P-A, Stengel D-B, FitzGerald R-J (2019) Peptide identification from a Porphyra dioica protein hydrolysate with antioxidant, angiotensin converting enzyme and dipeptidyl peptidase IV inhibitory activities. Food Funct 10:3421–3429

    Article  Google Scholar 

  22. Furuta T, Miyabe Y, Yasui H, Kinoshita Y, Kishimura H (2016) Angiotensin I converting enzyme inhibitory peptides derived from phycobiliproteins of dulse Palmaria palmata. Mar Drugs 14:E32

    Article  Google Scholar 

  23. Sumikawa K, Takei K, Kumagai Y, Shimizu T, Yasui H, Kishimura H (2020) In Silico analysis of ACE inhibitory peptides from chloroplast proteins of red alga Grateloupia asiatica. Mar Biotechnol 246:323–332

    Google Scholar 

  24. Kumagai Y, Miyabe Y, Takeda T, Adachi K, Yasui H, Kishimura H (2019) In silico analysis of relationship between proteins from plastid genome of red alga Palmaria sp. (Japan) and angiotensin I converting enzyme inhibitory peptides. Mar Drugs 17:E190

  25. Kumagai Y, Tsubouchi R, Miyabe Y, Takeda T, Adachi K, Yasui H, Kishimura H (2019) Complete sequence of mitochondrial DNA of red alga dulse Palmaria palmata (Linnaeus) Weber & Mohr in Japan. Mitochondrial DNA B 4:3177–3178

    Article  Google Scholar 

  26. Kitade Y, Miyabe Y, Yamamoto Y, Takeda H, Shimizu T, Yasui H, Kishimura H (2017) Structural characteristics of phycobiliproteins from red alga Mazzaella japonica. J Food Biochem 42:E12436

    Article  Google Scholar 

  27. Baldwin J-E, Adlington R-M, Russell A-T, Smith M-L (1995) Carbon based nucleophilic ring opening of activated monocyclic β-lactams; synthesis and stereochemical assignment of the ACE inhibitor WF-10129. Tetrahedron 51:4733–4762

    Article  CAS  Google Scholar 

  28. Hooper N-M (1991) Angiotensin converting enzyme: implications from molecular biology for its physiological functions. Int J Biochem 23:641–647

    Article  CAS  Google Scholar 

  29. Kobayashi M, Kumagai Y, Yamamoto Y, Yasui H, Kishimura H (2020) Identification of a key enzyme for the hydrolysis of β-(1→3)-xylosyl linkage in red alga dulse xylooligosaccharide from Bifidobacterium adolescentis. Mar Drugs 18:E174

    Article  Google Scholar 

  30. Yamamoto Y, Kishimura H, Kinoshita Y, Saburi W, Kumagai Y, Yasui H, Ojima T (2019) Enzymatic production of xylooligosaccharides from red alga dulse (Palmaria sp.) wasted in Japan. Process Biochem 82:117–122

    Article  CAS  Google Scholar 

  31. Leblanc C, Boyen C, Richard O et al (1995) Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales). Gene content and genome organization. J Mol Biol 250:484–495

    Article  CAS  Google Scholar 

  32. Moreira D, Le Guyader H, Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405:69–72

    Article  CAS  Google Scholar 

  33. Matsuzaki M, Misumi O, Shin-i T et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  Google Scholar 

  34. Collén J, Porcel B, Carré W et al (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus; shed light on evolution of the Archaeplastida. Proc Natl Acad Sci 110:5247–5252

    Article  Google Scholar 

  35. Nakamura Y, Sasaki N, Kobayashi M et al (2013) The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS ONE 8:e57122

    Article  CAS  Google Scholar 

  36. Watanabe K, Kishimoto T, Kumagai Y, Shimizu T, Uji T, Yasui H, Kishimura H (2019) Complete sequence of mitochondrial DNA of Gloiopeltis furcata (Postels and Ruprecht). J Agardh Mitochondrial DNA B 4:2543–2544

    Article  Google Scholar 

  37. Tu M, Liu H, Zhang R, Chen H, Mao F, Cheng S, Lu W, Du M (2018) Analysis and evaluation of the inhibitory mechanism of a novel angiotensin-I-converting enzyme inhibitory peptide derived from casein hydrolysate. J Agric Food Chem 66:4139–4144

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was partially supported by the “Science and technology research promotion program for agriculture, forestry, fisheries and food industry (27004B)”.

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Correspondence to Hideki Kishimura.

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Kumagai, Y., Kitade, Y., Kobayashi, M. et al. Identification of ACE inhibitory peptides from red alga Mazzaella japonica. Eur Food Res Technol 246, 2225–2231 (2020). https://doi.org/10.1007/s00217-020-03567-z

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  • DOI: https://doi.org/10.1007/s00217-020-03567-z

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