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Comparison of different extraction techniques for obtaining extracts from brown seaweeds and their potential effects as angiotensin I-converting enzyme (ACE) inhibitors

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Abstract

An extraction protocol was developed to maximize the amount of extracts obtained from three brown seaweeds, Lessonia nigrescens (in two stages of development), Macrocystis pyrifera, and Durvillaea antarctica, and to evaluate them as natural inhibitors of the angiotensin I-converting enzyme (ACE). Two extraction methods were used, an enzymatic method (cellulase and α-amylase) and a conventional method (maceration). The extracts were analyzed to determine the extraction yield (%), the total phenolic and carbohydrate concentrations, and the ACE inhibition. Juvenile L. nigrescens extracts obtained by α-amylase exhibited the highest extraction yield (37.72 ± 4.13 %), the highest ACE inhibition (95.61 ± 0.33 %), and the lowest IC50 (10.10 ± 1.55 μg PGE mg−1 seaweed) among the studied extracts. Extraction by maceration produced extracts with chemical characteristics that were less favorable for inhibiting ACE than the enzymatic extraction. The presence of phlorotannins and carbohydrates in these brown seaweeds after enzymatic extraction could be responsible for the superior ACE inhibitory activity of the extracts. Thus, these molecules could be considered as potential phytopharmaceuticals for the development of new ACE inhibitors.

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References

  • Adams JMM, Ross AB, Anastasakis K, Hodgson EM, Gallagher JA, Jones JM, Donnison IS (2011) Seasonal variation in the chemical composition of the bioenergy feedstock Laminaria digitata for thermochemical conversion. Bioresour Technol 102:226–234

    Article  CAS  PubMed  Google Scholar 

  • Al Shohaib S, Raweily E (2000) Acute tubular necrosis due to captopril. Am J Nephrol 20:149–152

    Article  CAS  PubMed  Google Scholar 

  • Arnold TM, Targett NM (1998) Quantifying in situ rates of phlorotannin synthesis and polymerization in marine brown algae. J Chem Ecol 24:577–595

    Article  CAS  Google Scholar 

  • Bhuyan BJ, Mugesh G (2011) Synthesis, characterization and antioxidant activity of angiotensin converting enzyme inhibitors. Org Biomol Chem 9:1356–1365

    Article  CAS  PubMed  Google Scholar 

  • Bhuyan BJ, Mugesh G (2012) Antioxidant activity of peptide-based angiotensin converting enzyme inhibitors. Org Biomol Chem 10:2237–2247

    Article  CAS  PubMed  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Breton F, Cérantola S, Ar Gall E (2011) Distribution and radical scavenging activity of phenols in Ascophyllum nodosum (Phaeophyceae). J Exp Mar Biol Ecol 399:167–172

    Article  CAS  Google Scholar 

  • Cardozo KHM, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol C 146:60–78

    Article  Google Scholar 

  • Cerpa-Calderón FK, Kennedy JA (2008) Berry integrity and extraction of skin and seed proanthocyanidins during red wine fermentation. J Agric Food Chem 56:9006–9014

    Article  PubMed  Google Scholar 

  • Cruces E, Huovinen P, Gómez I (2012) Phlorotannin and antioxidant responses upon short-term exposure to UV radiation and elevated temperature in three south Pacific kelps. Photochem Photobiol 88:58–66

    Article  CAS  PubMed  Google Scholar 

  • DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • El-Said GF, El-Sikaily A (2013) Chemical composition of some seaweed from Mediterranean Sea coast, Egypt. Environ Monit Assess 185:6089–6099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endringer DC, Oliveira OV, Braga FC (2014) In vitro and in silico inhibition of angiotensin-converting enzyme by carbohydrates and cyclitols. Chem Pap 68:37–45

    Article  CAS  Google Scholar 

  • Eriz G, Sanhueza V, Roeckel M, Fernández K (2011) Inhibition of the angiotensin-converting enzyme by grape seed and skin proanthocyanidins extracted from Vitis vinífera L. cv. País. LWT Food Sci Technol 44:860–865

    Article  CAS  Google Scholar 

  • García-Ríos V, Ríos-Leal E, Robledo D, Freile-Pelegrin Y (2012) Polysaccharides composition from tropical brown seaweeds. Phycol Res 60:305–3151

    Article  Google Scholar 

  • Godoy S, Roeckel M, Fernández K (2012) Influence of the structure and composition of the País grape proanthocyanidins on the inhibition of angiotensin I-converting enzyme (ACE). Food Chem 134:346–350

    Article  CAS  Google Scholar 

  • Gómez I, Westermeier R (1995) Energy contents and organic constituents in Antarctic and south Chilean marine brown algae. Polar Biol 15:597–602

    Article  Google Scholar 

  • Gupta S, Abu-Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci Technol 22:315–326

    Article  CAS  Google Scholar 

  • Heo SJ, Park EJ, Lee KW, Jeon YJ (2005) Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresour Technol 96:1613–1623

    Article  CAS  PubMed  Google Scholar 

  • Je J, Park P, Kim B, Kim S (2006) Antihypertensive activity of chitin derivatives. Biopolymers 83:250–254

    Article  CAS  PubMed  Google Scholar 

  • Jerez M, Selga A, Sineiro J, Torres JL, Núñez MJ (2007) A comparison between bark extracts from Pinus pinaster and Pinus radiata: antioxidant activity and procyanidin composition. Food Chem 100:439–444

    Article  CAS  Google Scholar 

  • Julius S, Nesbitt SD, Egan BM et al (2006) Feasibility of treating prehypertension with an angiotensin-receptor blocker. New Engl J Med 354:1685–1697

    Article  CAS  PubMed  Google Scholar 

  • Kadam SU, Tiwari BK, O’Donnell CP (2013) Application of novel extraction technologies for bioactives from marine algae. J Agric Food Chem 61:4667–4675

    Article  CAS  PubMed  Google Scholar 

  • Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, He J (2005) Global burden of hypertension: analysis of worldwide data. Lancet 365:217–223

    Article  PubMed  Google Scholar 

  • Kendel M, Couzinet-Mossion A, Viau M, Fleurence J, Barnathan G, Wielgosz-Collin G (2012) Seasonal composition of lipids, fatty acids, and sterols in the edible red alga Grateloupia turuturu. J Appl Phycol 25:425–432

    Article  Google Scholar 

  • Kim SK, Himaya SWA (2011) Medicinal effects of phlorotannins from marine brown algae. Adv Food Nutr Res 64:97–109

    Article  CAS  PubMed  Google Scholar 

  • Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005) Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J Chem Ecol 31:195–212

    Article  CAS  PubMed  Google Scholar 

  • Koivikko R, Loponen J, Pihlaja K, Jormalainen V (2007) High-performance liquid chromatographic analysis of phlorotannins from the brown alga Fucus vesiculosus. Phytochem Anal 18:326–332

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Qian ZJ, Ryu B, Lee SH, Kim MM, Kim SK (2009) Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg Med Chem 17:1963–1973

    Article  CAS  PubMed  Google Scholar 

  • Li YX, Wijesekara I, Li Y, Kim SK (2011) Phlorotannins as bioactive agents from brown algae. Process Biochem 46:2219–2224

    Article  CAS  Google Scholar 

  • Lohith K, Vijayakumar GR, Somashekar BR, Sivakumar R, Divakar S (2006) Glycosides and amino acyl esters of carbohydrates as potent inhibitors of angiotensin converting enzyme. Eur J Med Chem 41:1059–1072

    Article  CAS  PubMed  Google Scholar 

  • Lordan S, Smyth TJ, Soler-Vila A, Stanton C, Ross RP (2013) The α-amylase and α-glucosidase inhibitory effects of Irish seaweed extracts. Food Chem 141:2170–2176

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Macaya EC, Rothäusler E, Thiel M, Molis M, Wahl M (2005) Induction of defenses and within-alga variation of palatability in two brown algae from the northern-central coast of Chile: effects of mesograzers and UV radiation. J Exp Mar Bio Ecol 325:214–227

    Article  Google Scholar 

  • Manns D, Deutschle AL, Saake B, Meyer AS (2014) Methodology for quantitative determination of the carbohydrate composition of brown seaweeds (Laminariaceae). RSC Adv 4:25736

    Article  CAS  Google Scholar 

  • Marinho-Soriano E, Fonseca PC, Carneiro MAA, Moreira WSC (2006) Seasonal variation in the chemical composition of two tropical seaweeds. Bioresour Technol 97:2402–2406

    Article  CAS  PubMed  Google Scholar 

  • Michalak I, Chojnacka K (2015) Algae as production systems of bioactive compounds. Eng. Life Sci 15:160–176

    Article  CAS  Google Scholar 

  • Murray CJ, Lopez D (1997) Global mortality, disability, and the contribution of risk factors: Global Burden of Disease Study. Lancet 349:1436–1442

    Article  CAS  PubMed  Google Scholar 

  • Ngo DN, Qian ZJ, Je JY, Kim MM, Kim SK (2008) Aminoethyl chitooligosaccharides inhibit the activity of angiotensin converting enzyme. Process Biochem 43:119–123

    Article  CAS  Google Scholar 

  • Papenfus HB, Stirk WA, Finnie JF, Van Staden J (2012) Seasonal variation in the polyamines of Ecklonia maxima. Bot Mar 55:539–546

    Article  CAS  Google Scholar 

  • Park PJ, Je JY, Kim SK (2003) Angiotensin I converting enzyme (ACE) inhibitory activity of hetero-chitooligosaccharides prepared from partially different deacetylated chitosans. J Agric Food Chem 51:4930–4934

    Article  CAS  PubMed  Google Scholar 

  • Percival E, McDowell RH (1967) Chemistry and enzymology of marine algal polysaccharides. Academic Press, London, 219 pp

    Google Scholar 

  • Rengasamy KRR, Aderogba MA, Amoo SO, Stirk WA, Van Staden J (2013) Potential antiradical and alpha-glucosidase inhibitors from Ecklonia maxima (Osbeck) Papenfuss. Food Chem 141:1412–1415

    Article  CAS  PubMed  Google Scholar 

  • Samarakoon KW, O-Nam K, Ko JY, Lee JH, Kang MC, Kim D, Lee JB, Lee JS, Jeon YJ (2013) Purification and identification of novel angiotensin-I converting enzyme (ACE) inhibitory peptides from cultured marine microalgae (Nannochloropsis oculata) protein hydrolysate. J Appl Phycol 25:1595–1606

    Article  CAS  Google Scholar 

  • Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373

    Article  CAS  Google Scholar 

  • Schoenwaelder MEA, Clayton MN (1998) Secretion of phenolic substances into the zygote wall and cell plate in embryos of Hormosira andAcrocarpia (Fucales, Phaeophyceae). J Phycol 34:969–980

    Article  CAS  Google Scholar 

  • Serrano E, Laurent V, Elena I, Mendiola JA, Ana T, Luc M, Vale S (2013) Green improved processes to extract bioactive phenolic compounds from brown macroalgae using Sargassum muticum as model. Talanta 104:44–52

    Article  Google Scholar 

  • Smith JL, Summers G, Wong R (2010) Nutrient and heavy metal content of edible seaweeds in New Zealand. N Z J Crop Hort Sci 38:19–28

    Article  CAS  Google Scholar 

  • Thomas NV, Kim SK (2011) Potential pharmacological applications of polyphenolic derivatives from marine brown algae. Environ Toxicol Pharmacol 32:325–335

    Article  CAS  PubMed  Google Scholar 

  • Vijayabaskar P, Shiyamala V (2012) Antioxidant properties of seaweed polyphenol from Turbinaria ornata (Turner) J. Agardh, 1848. Asian Pac J Trop Biomed 2:S90–S98

    Article  Google Scholar 

  • Vo TS, Ngo DH, Kim SK (2012) Marine algae as a potential pharmaceutical source for anti-allergic therapeutics. Process Biochem 47:386–394

    Article  CAS  Google Scholar 

  • Westermeier R, Murúa P, Patiño DJ, Muñoz L, Ruiz A, Müller DG (2012) Variations of chemical composition and energy content in natural and genetically defined cultivars of Macrocystis from Chile. J Appl Phycol 24:1191–1201

    Article  CAS  Google Scholar 

  • Wijesekara I, Kim SK (2010) Angiotensin-I-converting enzyme (ACE) inhibitors from marine resources: prospects in the pharmaceutical industry. Mar Drugs 8:1080–1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wijesinghe WP, Jeon YJ (2012) Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia 83:6–12

    Article  CAS  PubMed  Google Scholar 

  • Wijesinghe WP, Ko SC, Jeon YJ (2011) Effect of phlorotannins isolated from Ecklonia cava on angiotensin I-converting enzyme (ACE) inhibitory activity. Nutr Res Pract 5:93–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wijesinghe WP, Ahn G, Lee WW, Kang MC, Kim EA, Jeon YJ (2013) Anti-inflammatory activity of phlorotannin-rich fermented Ecklonia cava processing by-product extract in lipopolysaccharide-stimulated RAW 264.7 macrophages. J Appl Phycol 25:1207–1213

    Article  CAS  Google Scholar 

  • Yamada A, Sakurai T, Ochi D, Mitsuyama E, Yamauchi K, Abe F (2013) Novel angiotensin I-converting enzyme inhibitory peptide derived from bovine casein. Food Chem 141:3781–3789

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank FONDECYT-Chile for the financial support for this research Project No. 1120148.

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Correspondence to Katherina Fernández.

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Olivares-Molina, A., Fernández, K. Comparison of different extraction techniques for obtaining extracts from brown seaweeds and their potential effects as angiotensin I-converting enzyme (ACE) inhibitors. J Appl Phycol 28, 1295–1302 (2016). https://doi.org/10.1007/s10811-015-0665-7

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