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In Silico Analysis of ACE Inhibitory Peptides from Chloroplast Proteins of Red Alga Grateloupia asiatica

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Abstract

Inhibition of angiotensin I–converting enzyme (ACE) is one of the key factors to repress high blood pressure. Although many studies have been reported that seaweed protein hydrolysates showed the ACE inhibitory activity, the comprehensive understanding of the relationship was still unclear. In this study, we employed chloroplast genome for in silico analysis and compared it with in vitro experiments. We first extracted water-soluble proteins (WSP) from red alga Grateloupia asiatica, which contained mainly PE, PC, APC, and Rbc, and prepared WSP hydrolysate by thermolysin, resulting that the hydrolysate showed ACE inhibitory activity. Then, we determined the complete chloroplast genome of G. asiatica (187,518 bp: 206 protein-coding genes, 29 tRNA, and 3 rRNA) and clarified the amino acid sequences of main WSP, i.e., phycobiliproteins and Rubisco, to perform in silico analysis. Consequently, 190 potential ACE inhibitory peptides existed in the main WSP sequences, and 21 peptides were obtained by in silico thermolysin digestion. By comparing in vitro and in silico analyses, in vitro ACE inhibitory activity was correlated to the IC50 value from in silico digestion. Therefore, in silico approach provides insight into the comprehensive understanding of the potential bioactive peptides from seaweed proteins.

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Abbreviations

ACE:

Angiotensin I–converting enzyme

APC:

Allophycocyanin

CBB:

Coomassie brilliant blue

PC:

Phycocyanin

PCG:

Protein-coding genes

PE:

Phycoerythrin

Rbc:

Ribulose-1, 5-bisphosphate carboxylase/oxygenase

WSP:

Water-soluble proteins

References

  • Beaulieu L, Sirois M, Tamigneaux É (2016) Evaluation of the in vitro biological activity of protein hydrolysates of the edible red alga, Palmaria palmata (dulse) harvested from the Gaspe coast and cultivated in tanks. J Appl Phycol 28:3101–3115

    Article  Google Scholar 

  • Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435

    Article  CAS  Google Scholar 

  • 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 

  • Chen H, Yan X, Zhu P, Lin J (2006) Antioxidant activity and hepatoprotective potential of agaro-oligosaccharides in vitro and in vivo. Nutr J 5:31

    Article  CAS  Google Scholar 

  • Cheung HS, Cushman DW (1973) Inhibition of homogeneous angiotensin-converting enzyme of rabbit lung by synthetic venom peptides of Bothrops jararaca. Biochim Biophys Acta Enzymol 293:451–463

    Article  CAS  Google Scholar 

  • 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 

  • Cian RE, Garzón AG, Ancona DB, Guerrero LC, Drago SR (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

    Article  CAS  Google Scholar 

  • Costa JF, Lin SM, Macaya EC, Fernandez-Garcia C, Verbruggen H (2016) Chloroplast genomes as a tool to resolve red algal phylogenies: a case study in the Nemaliales. BMC Evol Biol 16:1–13

    Article  Google Scholar 

  • Cota-Sánchez JH, Remarchuk K, Ubayasena K (2006) Ready-to-use DNA extracted with a CTAB method adapted for herbarium specimens and mucilaginous plant tissue. Plant Mol Biol Report 24:161–167

    Article  Google Scholar 

  • Daskaya-Dikmen C, Yucetepe A, Karbancioglu-Guler F, Daskaya H, Ozcelik B (2017) Angiotensin-I-converting enzyme (ACE)-inhibitory peptides from plants. Nutrients 9:316

    Article  CAS  Google Scholar 

  • De Ruiter GA, Rudolph B (1997) Carrageenan biotechnology. Trends Food Sci Technol 8:389–395

    Article  Google Scholar 

  • DePriest MS, Bhattacharya D, López-Bautista JM (2013) The plastid genome of the red macroalga Grateloupia taiwanensis (Halymeniaceae). PLoS One 8:e68246

    Article  CAS  Google Scholar 

  • Du Q, Bi G, Mao Y, Sui Z (2016) The complete chloroplast genome of Gracilariopsis lemaneiformis (Rhodophyta) gives new insight into the evolution of family Gracilariaceae. J Phycol 52:441–450

    Article  CAS  Google Scholar 

  • Fitzgerald C, Gallagher E, Tasdemir D, Hayes M (2011) Heart health peptides from macroalgae and their potential use in functional foods. J Agric Food Chem 59:6829–6836

    Article  CAS  Google Scholar 

  • Fitzgerald C, Aluko RE, Hossain M, Rai DK, Hayes M (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 

  • 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 14:32

    Article  CAS  Google Scholar 

  • Glazer AN (1985) Light harvesting by phycobilisomes. Ann Rev Biophys Chem 14:47–77

    Article  CAS  Google Scholar 

  • Harnedy PA, O’Keeffe MB, FitzGerald RJ (2015) Purification and identification of dipeptidyl peptidase (DPP) IV inhibitory peptides from the macroalga Palmaria palmata. Food Chem 172:400–406

    Article  CAS  Google Scholar 

  • He HL, Chen XL, Wu H, Sun CY, Zhang YZ, Zhou BC (2007) High throughput and rapid screening of marine protein hydrolysates enriched in peptides with angiotensin-I-converting enzyme inhibitory activity by capillary electrophoresis. Bioresour Technol 98:3499–3505

    Article  CAS  Google Scholar 

  • Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    Article  CAS  Google Scholar 

  • Kitade Y, Miyabe Y, Yamamoto Y, Takeda H, Shimizu T, Yasui H, Kishimura H (2018) Structural characteristics of phycobiliproteins from red alga Mazzaella japonica. J Food Biochem 42:e12436

    Article  CAS  Google Scholar 

  • Kumagai Y, Miyabe Y, Takeda T, Adachi K, Yasui H, Kishimura H (2019a) 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 17:190

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  Google Scholar 

  • Lee SY, Hur SJ (2017) Antihypertensive peptides from animal products, marine organisms, and plants. Food Chem 228:506–517

    Article  CAS  Google Scholar 

  • Lee KY, Mooney DJ (2012) Alginate: properties and biomedical applications. Prog Polym Sci 37:106–126

    Article  CAS  Google Scholar 

  • Mai K, Mercer JP, Donlon J (1994) Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata L and Haliotis discus hannai Ino: II Amino acid composition of abalone and six species of macroalgae with an assessment of their nutritional value. Aquaculture 128:115–130

    Article  CAS  Google Scholar 

  • Miyabe Y, Furuta T, Takeda T, Kanno G, Shimizu T, Tanaka Y, Gai Z, Yasui H, Kishimura H (2017) Structural properties of phycoerythrin from dulse Palmaria palmata. J Food Biochem 41:e12301

    Article  CAS  Google Scholar 

  • Ng PK, Lin SM, Lim PE, Liu LC, Chen CM, Pai TW (2017) Complete chloroplast genome of Gracilaria firma (Gracilariaceae, Rhodophyta), with discussion on the use of chloroplast phylogenomics in the subclass Rhodymeniophycidae. BCM Genomics 18:40

    Article  CAS  Google Scholar 

  • Sato N, Furuta T, Takeda T, Miyabe Y, Ura K, Takagi Y, Yasui H, Kumagai Y, Kishimura H (2018) Antioxidant activity of proteins extracted from red alga dulse harvested in Japan. J Food Biochem 43:e12709

    Article  CAS  Google Scholar 

  • Schmieder RE, Hilgers KF, Schlaich MP, Schmidt BMW (2007) Renin-angiotensin system and cardiovascular risk. Lancet 369:1208–1219

    Article  CAS  Google Scholar 

  • Sfriso AA, Gallo M, Baldi F (2018) Phycoerythrin productivity and diversity from five red macroalgae. J Appl Phycol 30:2523–2531

    Article  CAS  Google Scholar 

  • Sonani RR, Singh NK, Kumar J, Thakar D, Madamwar D (2014) Concurrent purification and antioxidant activity of phycobiliproteins from Lyngbya sp. A09DM: an antioxidant and anti-aging potential of phycoerythrin in Caenorhabditis elegans. Process Biochem 49:1757–1766

    Article  CAS  Google Scholar 

  • Suetsuna K (1998) Purification and identification of angiotensin I-converting enzyme inhibitors from the red alga Porphyra yezoensis. J Mar Biotechnol 6:163–167

    PubMed  CAS  Google Scholar 

  • Suetsuna K, Nakano T (2000) Identification of an antihypertensive peptide from peptic digest of wakame (Undaria pinnatifida). J Nutr Biochem 11:450–454

    Article  CAS  Google Scholar 

  • 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 Part B 4:2543–2544

    Article  Google Scholar 

  • 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 

  • Yang EC, Kim KM, Kim SY, Lee JM, Boo GH, Lee JH, Nelson WA, Yi G, Schmidt WE, Fredericq S, Boo SM, Bhattacharya D, Yoon HS (2015) Highly conserved mitochondrial genomes among multicellular red algae of the Florideophyceae. Genome Biol Evol 7:2394–2406

    Article  CAS  Google Scholar 

  • Yang EC, Boo SM, Bhattacharya D, Saunders GW, Knoll AH, Fredericq S, Yoon HS (2016) Divergence time estimates and the evolution of major lineages in the florideophyte red algae. Sci Rep 6:21361

    Article  CAS  Google Scholar 

  • Zhang J, Tang X, Chen WZ, Liu T, Li Y (2018) The complete plastid genome of Grateloupia filicina (Rhodophyta) and phylogenetic analysis. Mitochondrial DNA B 3:1172–1173

    Article  Google Scholar 

Download references

Funding

This study was partially supported by the “Regional Innovation Cluster Program (Global Type), Ministry of Education, Culture, Sports, Science and Technology, Japan” and the “Science and technology research promotion program for agriculture, forestry, fisheries and food industry (27004B).”

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Authors and Affiliations

  1. Chair of Marine Chemical Resource Development, Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Kana Sumikawa & Kentaro Takei

  2. Laboratory of Marine Chemical Resource Development, Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Yuya Kumagai & Hideki Kishimura

  3. Department of Research and Development, Hokkaido Industrial Technology Center, Hakodate, Hokkaido, 041-0801, Japan

    Takeshi Shimizu

  4. Laboratory of Humans and the Ocean, Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Hajime Yasui

Authors
  1. Kana Sumikawa
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  2. Kentaro Takei
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  3. Yuya Kumagai
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  4. Takeshi Shimizu
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  5. Hajime Yasui
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  6. Hideki Kishimura
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Correspondence to Hideki Kishimura.

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Sumikawa, K., Takei, K., Kumagai, Y. et al. In Silico Analysis of ACE Inhibitory Peptides from Chloroplast Proteins of Red Alga Grateloupia asiatica. Mar Biotechnol 22, 391–402 (2020). https://doi.org/10.1007/s10126-020-09959-2

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  • DOI: https://doi.org/10.1007/s10126-020-09959-2

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