DOI QR코드

DOI QR Code

Screening for Angiotensin 1-Converting Enzyme Inhibitory Activity of Ecklonia cava

  • Athukorala Yasantha (Faculty of Applied Marine Science, Cheju National University) ;
  • Jeon, You-Jin (Faculty of Applied Marine Science, Cheju National University)
  • Published : 2005.06.01

Abstract

Seven brown algal species (Ecklonia cava, Ishige okamurae, Sargassum fulvellum, Sargassum horneri, Sargassum coreanum, Sargassum thunbergii and Scytosiphon lomentaria) were hydrolyzed using five proteases (Protamex, Kojizyme, Neutrase, Flavourzyme and Alcalase) and screened for angiotensin 1-converting enzyme (ACE) inhibitory activities. Most algal species examined showed good ACE inhibitory activities after the enzymatic hydrolysis. However, E. cava was the most potent ACE inhibitor of the seven species. Flavourzyme digest of E. cava exhibited an $IC_{50}$ of around $0.3\;{\mu}g/mL$ for ACE; captopril has an $IC_{50}$ of $\~0.05\;{\mu}g/mL$. The Flavourzyme digest was separated to three fractions by an ultrafiltration membrane (5, 10, 30 kDa MWCO) system according to the molecular weights. The active components were mainly concentrated in >30 kD fraction which are composed of the highest protein content $(27\%)$ and phenolic content (261 mg/100 mL) compared to the other two smaller molecular weight fractions. Therefore, the active compounds appear to be relatively high molecular weight complex molecules associated with protein (glycoprotein) and polyphenols. Therefore, E. cave is a potential source of antihypertensive compound.

Keywords

References

  1. Kohama Y, Oka H, Kayamori Y, Tsujikawa K, Mimura T, Nagase Y, Satake M. 1991. Potent synthetic analogues of angiotensin-converting enzyme inhibitor derived from tuna muscle. Agric Biol Chem 55: 2169-2170 https://doi.org/10.1271/bbb1961.55.2169
  2. Suetsuna K. 1992. Study on the inhibitory activities against angiotensin I-converting enzyme of the peptides derived from sardine muscle. PhD Dissertation. Tokoku University, Miyagi, Sendai, Japan. p 1-92
  3. Isono Y. 1996. Peptide inhibitors for angiotensin I-converting enzyme from Masai fermented milk. Food Sci Technol Int 2: 213-216 https://doi.org/10.3136/fsti9596t9798.2.213
  4. Kato H, Suzuki T. 1971. Bradykinin-potentiating peptides from the venom of Agkistrodon halys blomhoffii: Isolation of five bradykinin potentiators Band C. Biochem 10: 972-980 https://doi.org/10.1021/bi00782a007
  5. Sawayama T, Itokawa A, Shimada K, Doi Y, Kimura K, Nishimura H. 1990. Synthesis of 1-[(s)-3-acetylthio-2-methylpropanoyl]-L-propyl-L-phenylalanine (Alacepril) and one of its active metabolites, the desacetyl derivative (DU-1227). Chem Pharm Bull 38: 529-531. https://doi.org/10.1248/cpb.38.529
  6. Ondetti MA. 1977. Design of specific inhibitors of angiotensinconverting enzyme: New class of orally active antihypertensive agents. Science 196: 441-444 https://doi.org/10.1126/science.191908
  7. Atkinson AB, Robertson JIS. 1979. Captopril in the treatment of clinical hypertension and cardiac failure. Lancet 2: 836-839
  8. Pihlanto-Leppala A. 2001. Bioactive peptides derived from bovine whey proteins: opioid and ace-inhibitory peptides. Trends Food Sci Technol 11: 347-356 https://doi.org/10.1016/S0924-2244(01)00003-6
  9. Maruyama S, Mitachi H, Awaya J. 1987. Angiotensin I-converting enzyme inhibitory activity of the c-terminal hexapeptide of as l-casein. Agric Biol Chem 51: 2557-2561 https://doi.org/10.1271/bbb1961.51.2557
  10. Kohmura M, Nio N, Kubo K. 1989. Inhibition of angiotensin-converting enzyme by synthetic peptides of humancasein. Agric Biol Chem 53: 2107-2114 https://doi.org/10.1271/bbb1961.53.2107
  11. Miyoshi S, Ishikawa I, Kaneko T, Fukui F, Tanaka H, Maruyama S. 1991. Structures and activity of angiotensinconverting enzyme inhibitors in an $\alpha$ -zein hydrolysate. Agric Biol Chem 55: 1313-1318 https://doi.org/10.1271/bbb1961.55.1313
  12. Yano S, Suzuki K, Funatsu G. 1996. Isolation from alphazein of thermolysin peptides with angiotensin I-converting enzyme inhibitory activity. Biosci Biotech Biochem 60: 661-663 https://doi.org/10.1271/bbb.60.661
  13. Chen JR, Okada T, Muramoto K. 2002. Identification of angiotensin I-converting enzyme inhibitory peptides derived from the peptic digest of soybean protein. J Food Biochem 6: 543-544
  14. Astawan M, Wahyuni M, Yasuhara T. 1995. Effects of angiotensin I-converting enzyme inhibitory substances derived from Indonesian dried-salted fish on blood pressure of rats. Biosci Biotech Biochem 59: 524-529
  15. Fujita H, Sasaki R, Yoshikawa M. 1995. Potentiation of the antihypertensive activity of orally administered ovokinin, a vasorelaxing peptide derived from ovalbumin, by emulsification in egg phosphatidylcholine. Biosci Biotech Biochem 59: 2344-2345 https://doi.org/10.1271/bbb.59.2344
  16. Okamoto A, Matsumoto E, Iwashita A. 1995. Angiotensin I-converting enzyme inhibitory action of fish sauce. Food Sci Technol Int 1: 101-106 https://doi.org/10.3136/fsti9596t9798.1.101
  17. Wako Y, Abe Y, Handa T, Ishikawa S. 1999. Angiotensin I-converting enzyme inhibitors in fish water soluble protein hydrolyzates prepared by bioreactor. Food Sci Technol Res 5: 378-380 https://doi.org/10.3136/fstr.5.378
  18. Suetsuna K. 1998. Purification and identification of angiotensin l-converting enzyme inhibitors from the red alga Porphyra yezoensis. J Mar Biotech 6: 163-167
  19. Suetsuna K, Nakano T. 2000. Identification of an antihypertensive peptide frompeptic digest of wakame (Undaria pinnatifida). J Nutr Biochem 11: 450-454 https://doi.org/10.1016/S0955-2863(00)00110-8
  20. Lowry OH, Rosebrough NJ, Farr L, Rindall RJ. 1951. Protein mesurement with the folin phenol reagent. J Biol Chem 193: 256-259
  21. Cushman DW, Chung HS. 1970. Spectrometric assay and properties of the angitensin I-converting enzyme of rabbit lung. Biochem Pharmaco 20: 1637-1684
  22. Chandler SF, Dodds JH. 1993. The effect of phosphate, nitrogen and sucrose on the production phenolics and solasidine in callus cultures of Solanum laciniatum. Plant Cell Rep 2: 105-110 https://doi.org/10.1007/BF00270178
  23. Choi HS, Cho HY, Yang HC, Ra KS, Suh HI. 2001. Angiotensin l-converting enzyme inhibitor from Grifola frondosa. Food Res Int 34: 117-182 https://doi.org/10.1016/S0963-9969(00)00138-1
  24. Adler-Nissen J. 1979. Determination of the degree of hydrolysis of food protein hydrolysates by trinitrobenzenesulfonic acid. J Agric Food Chem 27: 1256-1262 https://doi.org/10.1021/jf60226a042
  25. Mahmoud MI, Malone WT, Cordle CT. 1992. Enzymatic hydrolysis of casein: effect of degree of hydrolysis on antigenicity and physical properties. J Food Sci 57: 1223-1229 https://doi.org/10.1111/j.1365-2621.1992.tb11304.x
  26. Watanabe T, Mazumder TK, Nagai S, Tsuji K, Terabe S. 2003. Analysis method of the angiotensin-I converting enzyme inhibitory activity based on micellar electrokinetic chromatography. Anal Sci 19: 159-161 https://doi.org/10.2116/analsci.19.159
  27. Kim JM, Whang JH, Suh HJ. 2004. Enhancement of angitensin l-converting enzyme inhibitory activity and improvement of the emulsifying and foaming properties of com glutein hydrolysate using ultrafiltration membranes. Eur Food Res Technol 218: 133-138 https://doi.org/10.1007/s00217-003-0825-x
  28. Paulis JW, Bietz JA. 1986. Separation of alcohol soluble maize proteins by reversed phase high performance liquid chromatography. J Cereal Sci 4: 205-211 https://doi.org/10.1016/S0733-5210(86)80022-4
  29. Liu JC, Hsu FL, Tsai JC, Chan P, Liu JYH, Thomas GN, Tomlinson B, Lo MY, Lin JY. 2003. Antihypertensive effects of tannins isolated from traditional Chinese herbs as non-specific inhibitors of angiotensin converting enzyme. Life Sci 73: 1543-1555 https://doi.org/10.1016/S0024-3205(03)00481-8
  30. Rojas A, Bah M, Rojas JI, Gutierrez DM. 2000. Smooth muscle relaxing activity of gentiopicroside isolated from Gentiana spathacea. Planta Med 66: 765-767 https://doi.org/10.1055/s-2000-9774
  31. Black HR, Ming S, Poll DS, Wen YF, Zhou HY, Zhang ZQ, Chung YK, Wu YS. 1986. A comparison of the treatment of hypertension with Chinese herbal and Western medication. J Clin Hypertens 24: 371-378
  32. Mao HY, Tu YS, Nei FD, Liang GF, Feng YB. 1981. Rapid antihypertensive effect of rhomotoxin in 105 hypertension cases. Chinese Med J 94: 733-736

Cited by

  1. Radical scavenging capacity and cytoprotective effect of enzymatic digests of Ishige okamurae vol.20, pp.6, 2008, https://doi.org/10.1007/s10811-008-9320-x
  2. Antioxidant activity and cell protective effect of loliolide isolated from Sargassum ringgoldianum subsp. coreanum vol.26, pp.2, 2011, https://doi.org/10.4490/algae.2011.26.2.201
  3. Hepatoprotective effects of dieckol-rich phlorotannins from Ecklonia cava, a brown seaweed, against ethanol induced liver damage in BALB/c mice vol.50, pp.6, 2012, https://doi.org/10.1016/j.fct.2012.03.078
  4. Phlorotannins as bioactive agents from brown algae vol.46, pp.12, 2011, https://doi.org/10.1016/j.procbio.2011.09.015
  5. Protective Effect of Enzymatic Extracts from Sargassum coreanum on H2O2-induced Cell Damage vol.13, pp.1, 2010, https://doi.org/10.5657/fas.2010.13.1.026
  6. Antioxidant Effect of Sargassum coreanum Root and Stem Extracts vol.30, pp.4, 2015, https://doi.org/10.7841/ksbbj.2015.30.4.155
  7. Phlorotannins from Ecklonia cava (Phaeophyceae): Biological activities and potential health benefits vol.36, pp.6, 2010, https://doi.org/10.1002/biof.114
  8. Characterisation of a new antihypertensive angiotensin I-converting enzyme inhibitory peptide from Pleurotus cornucopiae vol.127, pp.2, 2011, https://doi.org/10.1016/j.foodchem.2011.01.010
  9. Thermostability of a marine polyphenolic antioxidant dieckol, derived from the brown seaweed Ecklonia cava vol.27, pp.3, 2012, https://doi.org/10.4490/algae.2012.27.3.205
  10. Effect of phlorotannins isolated fromEcklonia cavaon angiotensin I-converting enzyme (ACE) inhibitory activity vol.5, pp.2, 2011, https://doi.org/10.4162/nrp.2011.5.2.93
  11. ACE, α-Glucosidase and Cancer Cell Growth Inhibitory Activities of Extracts and Fractions from Marine Microalgae, Nannochloropsis oculata vol.43, pp.5, 2010, https://doi.org/10.5657/kfas.2010.43.5.437
  12. Enzyme-assisted extraction of κ/ι-hybrid carrageenan from Mastocarpus stellatus for obtaining bioactive ingredients and their application for edible active film development vol.5, pp.2, 2014, https://doi.org/10.1039/C3FO60310E
  13. Screening of Extracts from Red Algae in Jeju for Potentials MarineAngiotensin - I Converting Enzyme (ACE) Inhibitory Activity vol.21, pp.3, 2006, https://doi.org/10.4490/ALGAE.2006.21.3.343
  14. Dieckol isolated from brown seaweed Ecklonia cava attenuates type ІІ diabetes in db/db mouse model vol.53, 2013, https://doi.org/10.1016/j.fct.2012.12.012
  15. Exploiting biological activities of brown seaweedEcklonia cavafor potential industrial applications: a review vol.63, pp.2, 2012, https://doi.org/10.3109/09637486.2011.619965
  16. Antihypertensive Angiotensin I-Converting Enzyme Inhibitory Activity and Antioxidant Activity ofVitishybrid-Vitis coignetiaeRed Wine Made withSaccharomyces cerevisiae vol.39, pp.2, 2011, https://doi.org/10.4489/MYCO.2011.39.2.137
  17. Evaluation of Angiotensin -I- Converting Enzyme Inhibitory Activity and Protein Changes of Enzymatic Hydrolysate Extracted from Hanwoo Loin and Round Myosin B vol.49, pp.1, 2007, https://doi.org/10.5187/JAST.2007.49.1.129
  18. Radical Scavenging Potential of Hydrophilic Phlorotannins of Hizikia fusiformis vol.20, pp.1, 2005, https://doi.org/10.4490/ALGAE.2005.20.1.069
  19. Enzyme-assisted extraction of cactus bioactive molecules under high hydrostatic pressure vol.94, pp.5, 2014, https://doi.org/10.1002/jsfa.6317
  20. Microalgal lipids biochemistry and biotechnological perspectives vol.32, pp.8, 2014, https://doi.org/10.1016/j.biotechadv.2014.10.003
  21. Effects of dietary supplementation with citrus pomace and Ecklonia cava residue on the physiological changes and growth of disk abalone, Haliotis discus discus vol.28, pp.1, 2015, https://doi.org/10.7847/jfp.2015.28.1.053
  22. A Molecular Sex Identification Using Duplex PCR Method for SRY and ZFX-ZFY Genes in Red Deer and Elk vol.49, pp.1, 2007, https://doi.org/10.5187/JAST.2007.49.1.001
  23. Comparison of biological activities in Sargassum siliquanstrum fermented by isolated lactic acid bacteria vol.20, pp.2, 2015, https://doi.org/10.1007/s12257-015-0112-2
  24. Enzyme proteolysis enhanced extraction of ACE inhibitory and antioxidant compounds (peptides and polyphenols) from Porphyra columbina residual cake vol.25, pp.4, 2013, https://doi.org/10.1007/s10811-012-9913-2
  25. Angiotensin-converting enzyme I inhibitory activity of phlorotannins from Ecklonia stolonifera vol.72, pp.6, 2006, https://doi.org/10.1111/j.1444-2906.2006.01288.x
  26. Hypoglycemic Effect of Sargassum ringgoldianum Extract in STZ-induced Diabetic Mice vol.17, pp.1, 2012, https://doi.org/10.3746/pnf.2012.17.1.008
  27. Protective effect of fucoidan against AAPH-induced oxidative stress in zebrafish model vol.102, 2014, https://doi.org/10.1016/j.carbpol.2013.11.022
  28. Protective effect of Ecklonia cava on UVB-induced oxidative stress: in vitro and in vivo zebrafish model vol.23, pp.4, 2011, https://doi.org/10.1007/s10811-010-9565-z
  29. Potential pharmacological applications of polyphenolic derivatives from marine brown algae vol.32, pp.3, 2011, https://doi.org/10.1016/j.etap.2011.09.004
  30. Biological Properties of Fucoxanthin in Oil Recovered from Two Brown Seaweeds Using Supercritical CO2 Extraction vol.13, pp.6, 2015, https://doi.org/10.3390/md13063422
  31. Angiotensin-I-Converting Enzyme (ACE) Inhibitors from Marine Resources: Prospects in the Pharmaceutical Industry vol.8, pp.4, 2010, https://doi.org/10.3390/md8041080
  32. Bio-functionalities of proteins derived from marine algae — A review vol.48, pp.2, 2012, https://doi.org/10.1016/j.foodres.2012.03.013
  33. Processing Optimization of Ecklonia cava Extract-Added Seasoning Sauce for Instant Noodles vol.44, pp.3, 2011, https://doi.org/10.5657/KFAS.2011.0197
  34. Improvement on the Antioxidant Activity of Instant Noodles Containing Enzymatic Extracts from Ecklonia cava and Its Quality Characterization vol.43, pp.5, 2010, https://doi.org/10.5657/kfas.2010.43.5.391
  35. Antioxidant Activity of Enzymatic Extracts from Sargassum coreanum vol.39, pp.4, 2010, https://doi.org/10.3746/jkfn.2010.39.4.494
  36. Angiotensin I-Converting Enzyme (ACE) Inhibitory Activity, Antioxidant Properties, Phenolic Content and Amino Acid Profiles of Fucus spiralis L. Protein Hydrolysate Fractions vol.15, pp.10, 2017, https://doi.org/10.3390/md15100311
  37. Extract Attenuates Palmitate-Induced Toxicity and Enhances Insulin Secretion in Pancreatic Beta-Cells vol.2018, pp.1942-0994, 2018, https://doi.org/10.1155/2018/4973851
  38. Potential Role of Seaweed Polyphenols in Cardiovascular-Associated Disorders vol.16, pp.8, 2018, https://doi.org/10.3390/md16080250
  39. elucidation of angiotensin-I-converting enzyme inhibition and antioxidant potential vol.21, pp.1, 2018, https://doi.org/10.1080/10942912.2018.1454465
  40. Dual BACE1 and Cholinesterase Inhibitory Effects of Phlorotannins from Ecklonia cava—An In Vitro and in Silico Study vol.17, pp.2, 2019, https://doi.org/10.3390/md17020091
  41. 제주 자생 해양 녹조류와 갈조류 추출물로부터의 항고혈압 활성 vol.35, pp.3, 2005, https://doi.org/10.3746/jkfn.2006.35.3.307
  42. 감태(Ecklonia cava) 줄기 및 잎의 효소적 추출물과 메탄올 추출물에 의한 항산화 활성비교 vol.35, pp.9, 2005, https://doi.org/10.3746/jkfn.2006.35.9.1139
  43. Purification of angiotensin‐converting enzyme from human plasma and investigation of the effect of some active ingredients isolated from Nigella sativa L. extract on the enzyme activity vol.32, pp.5, 2018, https://doi.org/10.1002/bmc.4175
  44. 5-Bromoprotocatechualdehyde Combats against Palmitate Toxicity by Inhibiting Parkin Degradation and Reducing ROS-Induced Mitochondrial Damage in Pancreatic β-Cells vol.10, pp.2, 2005, https://doi.org/10.3390/antiox10020264
  45. Attenuating Effects of Dieckol on Endothelial Cell Dysfunction via Modulation of Th17/Treg Balance in the Intestine and Aorta of Spontaneously Hypertensive Rats vol.10, pp.2, 2005, https://doi.org/10.3390/antiox10020298
  46. A Systemic Review on Microalgal Peptides: Bioprocess and Sustainable Applications vol.13, pp.6, 2005, https://doi.org/10.3390/su13063262
  47. Ecklonia cava Extract and Its Derivative Dieckol Promote Vasodilation by Modulating Calcium Signaling and PI3K/AKT/eNOS Pathway in In Vitro and In Vivo Models vol.9, pp.4, 2021, https://doi.org/10.3390/biomedicines9040438
  48. Prospecting the Effects on Abalone (H. discus) Growth under Low-Salinity Stress after Feeding Citrus Peel (CP) and Ecklonia cava disuse (ECD) as Feed Additives vol.9, pp.7, 2005, https://doi.org/10.3390/jmse9070707
  49. Dieckol Reduces Muscle Atrophy by Modulating Angiotensin Type II Type 1 Receptor and NADPH Oxidase in Spontaneously Hypertensive Rats vol.10, pp.10, 2005, https://doi.org/10.3390/antiox10101561