DOI QR코드

DOI QR Code

Screening of Extracts from Marine Green and Brown Algae in Jeju for Potential Marine Angiotensin-I Converting Enzyme (ACE) Inhibitory Activity

제주 자생 해양 녹조류와 갈조류 추출물로부터의 항고혈압 활성

  • Cha, Seon-Heui (Faculty of Applied Marine Science, Cheju National Uniuersity) ;
  • Ahn, Gin-Nae (Faculty of Applied Marine Science, Cheju National Uniuersity) ;
  • Heo, Soo-Jin (Faculty of Applied Marine Science, Cheju National Uniuersity) ;
  • Kim, Kil-Nam (Faculty of Applied Marine Science, Cheju National Uniuersity) ;
  • Lee, Ki-Wan (Faculty of Applied Marine Science, Cheju National Uniuersity) ;
  • Song, Choon-Bok (Faculty of Applied Marine Science, Cheju National Uniuersity) ;
  • K.Cho, So-Mi (Faculty of Biotechology, Cheju National Uniuersity) ;
  • Jeon, You-Jin (Faculty of Applied Marine Science, Cheju National Uniuersity)
  • 차선희 (제주대학교 해양생산과학부) ;
  • 안긴내 (제주대학교 해양생산과학부) ;
  • 허수진 (제주대학교 해양생산과학부) ;
  • 김길남 (제주대학교 해양생산과학부) ;
  • 이기완 (제주대학교 해양생산과학부) ;
  • 송춘복 (제주대학교 해양생산과학부) ;
  • 김소미 (제주대학교 생명공학부) ;
  • 전유진 (제주대학교 해양생산과학부)
  • Published : 2006.03.01

Abstract

This study was conducted to screen in vitro angiotensin converting enzyme (ACE) inhibitory activities of methanol (MeOH) and aqueous extracts which were prepared by four different extractions-80% methanol extracts(ME) at $20^{\circ}C\;and\;70^{\circ}C$, respectively and aqueous extracts (AE) at both temperatures with the residue of the MEs-of ten marine green algae and nineteen brown algae collected along Jeju coast of Korea. Most marine brown algae extracts showed higher capacities than those of marine green algae in ACE inhibitory activity. Particularly, $70^{\circ}C$ MeOH extract (70ME) of Hizikia fusiforme showed the strongest inhibition activity (about 87%) among all the extracts. Also, 70 MEs of Enteromorpha linza, Ishige sinicola, Laminaria ochotensis, Petrospongium rugosum, Sagrassum horneri, Undaria pinnatifida and $20^{\circ}C$ MeOH extracts (20ME) of Myagropsis myagroides, Petrospongium rugosum, $20^{\circ}C$ aqueous extracts (20AE) of Codium contractum, Enteromorpha compressa, and $70^{\circ}C$ aqueous extracts (70AE) of Ecklonia cava, Petrospongium rugosum showed moderate ACE inhibitory activities more than 50% and the other extracts exhibited weak activities. On tile other hand, E. cava had the best ACE inhibitory activity among 70AEs. This indicates that 70AE of E. cava contains potential anti-ACE macromolecular. We tried to proteolytic digest 70AE of E. cava to induce production of anti-ACE peptides from E. cava 70AE. The enzymes used are five pretenses including Kojizyme, Flavourzyme, Neutrase, Alcalase, and Protamex, which are food grade-commercial enzymes from Novo Co. Flavourzyme-digest of E. cava 70AE showed the highest inhibitory activity about 90%. And the five different enzymatic digests of the E. cava 70AE ranged from 2.33 to 3.56 ${\mu}g/mL$, respectively in $IC_{50}$ values of anti-ACE activity.

제주 연안에 서식하는 해양 녹조류와 갈조류의 항고혈압 활성을 알아보기 위해 해조류로부터 메탄올과 물을 이용하여 상온($20^{\circ}C$)과 $70^{\circ}C$에서 각각 4가지 종류의 추출물을 제조하여 스크리닝하였다. 결과, 녹조류에서는 비교적 낮은 ACE 저해활성을 보였으나, 갈조류에서는 70ME 잇바디괭생이모자반, 말미역, 바위주름, 넓패, 톳, 다시마 및 70AE 감태에서 ACE 저해활성이 높게 나타났다. 또한 70AE 감태의 가수분해물은 $2.33{\sim}3.56{\mu}g/mL$$IC_{50}$값을 보여 매우 높은 ACE 저해활성을 확인할 수 있었다. 이는 해조류의 ACE 저해활성이 수용성 추출물뿐만 아니라 메탄올 추출물에서도 나타나는 것은 해조류 유래 fucoxanthin, phlorotannin 및 polyphenol계 화합물 등에 의한 영향도 있을 것으로 사료된다.

Keywords

References

  1. Frohlich ED. 1982. Hemodynamic factors in the path-ogenesis and maintenance of hypertension. Fed A Soc Exp Biol 41: 2400-2408
  2. Miyoshi S, Ishikawa H, Kaneko T, Fukui F, Tanaka H, Maruyama S. 1991. Structure and activity of angiotensin- converting enzyme inhibitors in an $\alpha$-zein hydrolysate. Agric Biol Chem 55: 1313-1318 https://doi.org/10.1271/bbb1961.55.1313
  3. Curtiss C, Chon JN, Vrobel T, Francious JA. 1978. Role of the rennin-angiotensin system in the systemic vaso-constriction of chronic congestive heart failure. Circulation 58: 763-770 https://doi.org/10.1161/01.CIR.58.5.763
  4. Maruyama S, Mitachi H, Awaya J, Kurono M, Tomizuka N, Suzuki H. 1989. Angiotensin I-converting enzyme inhibitory activity of the C-terminal hexapeptide of $\alpha$ s1-casein. Agric Biol Chem 53: 2107-2114 https://doi.org/10.1271/bbb1961.53.2107
  5. Dzau VJ. 2001. Tissue angiotensin and pathobiology of vascular disease: a unifying hypothesis. Hypertension 37: 1047-1052 https://doi.org/10.1161/01.HYP.37.4.1047
  6. Cushman DW, Cheung HS. 1971. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem Pharmacol 20: 1637-1648 https://doi.org/10.1016/0006-2952(71)90292-9
  7. Sealey JE, Laragh JH. 1990. Pathophysiology, diagnosis and management. The renin-angiotensin-aldosterone system for normal regulation of blood pressure and sodium and potassium homeostasis. Raven Press, LTD, New York. p 1287-1317
  8. Kato H, Suzuki T. 1971. Bradykinin-potentiating peptides from venom of Agkistrodon halys blomhoffii: Isolation of five bradykinin potentiators and the amino acid sequences of two of them, potentiators B and C. Biochemistry 10: 972-980 https://doi.org/10.1021/bi00782a007
  9. Ondetti MA. 1977. Desine of specific inhibitors of angio-tensin coverting enzyme: New ckass of orally active antihypetensive agents. Science 196: 441-444 https://doi.org/10.1126/science.191908
  10. Sawayama T, Itokawa A, Shumada K, Doi Y, Kimura K, Nishimura H. 1990. Synthesis of 1-[(s)-acetylthio-2-me-thylpro-panoyl]-L-propyl-L-phenylanine (Alacepril) and one of its active metabolites, the desacetyl derivation (DU- 1227). Chem Pharm Bull 38: 529-531 https://doi.org/10.1248/cpb.38.529
  11. Atkinson AB, Rovertson J. 1979. Captopril in the treatment of clinical hypertension and cardiac failure. Lancet 2: 836- 839
  12. Maruyama SH, Mitachi H, Tanaka N, Tomizuka N, Suzuki H. 1987. Studies on the active site and antihypertensive activity of angiotensin I-converting enzyme inhibitors derived from casein. Agric Biol Chem 51: 1581-1586 https://doi.org/10.1271/bbb1961.51.1581
  13. Muramaoto M, Kawamura Y. 1991. Antihypertensive peptides derived from rice protein. Shokuhin Kogyo 11: 18-26
  14. Suh HJ, Suh DB, Chung SH, Whang JH, Sung HJ, Yang HC. 1994. Purification of ACE inhibitor from soybean paste. Korean J Agric Chem Biotech 37: 441-446
  15. Cho YJ, Cha WS, Bok SK, Kim MU, Chun SS, Choi UK, Kim SH, Park KS. 2000. Production and separation of angiotensin I converting enzyme inhibitor during natto fermentation. J Korean Soc Food Sci Nutr 29: 737-742
  16. Saito Y, Nakamura K, Kawato A, Imayasu S. 1992. An-giotensin I converting enzyme inhibitors in sake and its by-products. Nippon Nogeikagaku Kaishi 66: 1081-1087 https://doi.org/10.1271/nogeikagaku1924.66.1081
  17. Saito Y, Wanezaki K, Kawato A, Imayasu S. 1994. Anti-hyperthensive effects of peptide in sake and its by-products on spontaeously hypertensive rates. Biosci Biotech Biochem 58: 812-816 https://doi.org/10.1271/bbb.58.812
  18. Matsufuj H, Matsui T, Seki E, Osajima K, Nakashima M, Osajima Y. 1994. Angiotensin I-converting enzyme inhibitory peptides in an alkaline protease hydrolyzate derived from sardine muscle. Biosci Biotech Biochem 58: 2244- 2245 https://doi.org/10.1271/bbb.58.2244
  19. 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
  20. Matsumura N, Fujii M, Takeda Y, Shimizu T. 1993. Isolation and characterization of angiotensin I-converting enzyme inhibitory peptides derived from bonito bowels. Biosci Biotech Biochem 57: 1743-1744 https://doi.org/10.1271/bbb.57.1743
  21. Yokoyama K, Chiba H, Yoshikawa M. 1992. Peptide inhibitors for angiotensin-converting enzyme from thermolysin digest of dried bonito. Biosci Biotech Biochem 56: 1541- 1545 https://doi.org/10.1271/bbb.56.1541
  22. Yeum Dm, Lee TG, Byun HS, Kim SB, Park YH. 1992. Angiotensin-I converting enzyme inhibitory activity of enzymatic hydrolysates of mackerel muscle protein. Bull Korean Fish Soc 25: 229-235
  23. Suh HJ, Cho SJ, Whang JH, Lee H, Yang HC. 1997. Characterization of angiotensin converting enzyme inhibitor from squid hydrolysate. Food and Biotechnology 6: 122-124
  24. Choi YR, Park PJ, Choi JH, Byun HG, Jeong IC, Moon SH, Kim SK. 2000. Purification and characterization of angiotensin I converting enzyme inhibitory peptides from enzymatic hydrolysate of cod liver protein. Korean J Life Sci 10: 140-149
  25. Heo SJ, Lee KW, Song SB, Jeon YJ. 2003. Antioxidant activity of enzymatic extracts from brown seaweeds. Algae 18: 71-81 https://doi.org/10.4490/ALGAE.2003.18.1.071
  26. Hyun CK, Shin HK. 2000. Utilization of bovine blood plasma proteins for the production of angiotensin I converting enzyme inhibitory peptides. Process Biochemistry 36: 65-71 https://doi.org/10.1016/S0032-9592(00)00176-X
  27. Yeum DM, Lee TG, Byum HS, Kim SB, Park TH. 1992. Angiotensin-I converting enzyme inhibitory activity of enzymatic hydrolysates of mackerel muscle protein. J Korean Fish Soc 32: 738-746
  28. Yasantha A, Jeon YJ. 2005. Screening for angiotensin-I converting enzyme inhibitiory activity of Ecklonia cava. J Food Sci Nutr 10: 134-139 https://doi.org/10.3746/jfn.2005.10.2.134
  29. Lee TG, Yeum DM, Kim SB. 2002. Characteristics of angiotensin converting enzyme inhibitory peptides from thermolysin hydrolysate of manila clam, Ruditapes philippinarum proteins. J Korean Fish Soc 35: 529-533
  30. Kim DS, Park DC, Do JR. 2002. Angiotensin I converting enzyme inhibitory activity of krill (Euphausia superba) hydrolysate. Fisheries Sci Technol 5: 21-27
  31. Jung WK, Mendis E, Je JY, Park PJ, Son BW, Kim HC, Choi YK, Kim SK. 2006. Angiotensin I-converting enzyme inhibitory peptide from yellowfin sole (Limanda aspera) frame protein and its antihypertensive effect in spon-taneously hypertensive rats. Food Chemistry 94: 26-32 https://doi.org/10.1016/j.foodchem.2004.09.048
  32. Je JY, Park PJ, Byun HG, Jung WK, Kim SK. 2005. Angiotensin I converting enzyme (ACE) inhibitory peptide derived from the sauce of fermented blue mussel, Mytilus edulis. Bioresource Technology 96: 1624-1629 https://doi.org/10.1016/j.biortech.2005.01.001
  33. Kunio S, Takahisa N. 2000. Identification of an anti-hypertensive peptide from peptic digest of Wakame (Undaria pinnatifida). J Nutr Biochem 11: 450-456 https://doi.org/10.1016/S0955-2863(00)00110-8
  34. Kunio S, Keisei M, Chen JR. 2004. Antihypertensive effects of Undaria pinnatifida (Wakame) peptide on blood pressure in spontaneously hypertensive rats. J Nutr Biochem 15: 267-272 https://doi.org/10.1016/j.jnutbio.2003.11.004
  35. Mustafa MG, Nakagawa H. 1995. Dietary benefits of algae as an additive in fish feed. Isreali J Aqua 47: 155-162

Cited by

  1. Effects of Colpomenia sinuosa Extract on Serum Lipid Level and Bone Formation in Ovariectomized Rats vol.45, pp.4, 2016, https://doi.org/10.3746/jkfn.2016.45.4.492
  2. Evaluation of Biological Activities of Fermented Hizikia fusiformis Extracts vol.24, pp.3, 2014, https://doi.org/10.5352/JLS.2014.24.3.304
  3. 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
  4. Antioxidant and Antihypertensive Activities of Solvent Extract from Styela clava Tunic, Fishery Waste vol.24, pp.7, 2015, https://doi.org/10.5322/JESI.2015.24.7.917
  5. Effect of Gamma Irradiation on Immune Activity and Physicochemical Properties of Myagropsis myagroides Water Extract vol.44, pp.1, 2011, https://doi.org/10.5657/kfas.2011.44.1.050
  6. Radical Scavenging Potential of Hydrophilic Phlorotannins of Hizikia fusiformis vol.20, pp.1, 2005, https://doi.org/10.4490/ALGAE.2005.20.1.069
  7. Seaweed Fermentation and Probiotic Properties of Lactic Acid Bacteria Isolated from Korean Traditional Foods vol.45, pp.10, 2016, https://doi.org/10.3746/jkfn.2016.45.10.1481
  8. Analysis of the isoflavone content, antioxidant activity, and SDS-PAGE of cheese analogs produced with different proteolysis and soymilk residue contents vol.58, pp.4, 2015, https://doi.org/10.1007/s13765-015-0064-4
  9. Evaluation of Antioxidant and Nitrite Scavenging Activity of Seaweed Extracts vol.21, pp.4, 2011, https://doi.org/10.5352/JLS.2011.21.4.576
  10. Effect of Solvent Extracts from Sargassum hemiphyllum on Inhibition of Growth of Human Cancer Cell Lines and Antioxidant Activity vol.17, pp.11, 2007, https://doi.org/10.5352/JLS.2007.17.11.1533
  11. 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
  12. 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
  13. BIOACTIVE PROTEINS, PEPTIDES, AND AMINO ACIDS FROM MACROALGAE1 vol.47, pp.2, 2011, https://doi.org/10.1111/j.1529-8817.2011.00969.x
  14. 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
  15. Inhibitory Effects of Maesaengi (Capsosiphon fulvescens) Extracts on Angiotensin Converting Enzyme and α-Glucosidase vol.21, pp.6, 2011, https://doi.org/10.5352/JLS.2011.21.6.811
  16. Phenolic Content, DPPH Radical Scavenging, and Tyrosinase Inhibitory Activities of Ecklonia cava Extracted with the Ultrasonic Wave Method vol.23, pp.7, 2013, https://doi.org/10.5352/JLS.2013.23.7.913
  17. Cytoprotective Effects of Phaeophyta Extracts from the Coast of Jeju Island in HT-22 Mouse Neuronal Cells vol.43, pp.2, 2014, https://doi.org/10.3746/jkfn.2014.43.2.224
  18. Characteristics and in vitro Anti-diabetic Properties of the Korean Rice Wine, Makgeolli Fermented with Laminaria japonica vol.19, pp.2, 2014, https://doi.org/10.3746/pnf.2014.19.2.098
  19. Angiotensin I-converting enzyme (ACE) inhibitory activity of Fucus spiralis macroalgae and influence of the extracts storage temperature—A short report vol.131, 2016, https://doi.org/10.1016/j.jpba.2016.08.029
  20. Effects of Fermented Sargassum thunbergii on Platelet Aggregation and Serum Lipid Levels in Obese Rat induced by High Fat Diet vol.25, pp.4, 2015, https://doi.org/10.5352/JLS.2015.25.4.456
  21. Marine Algae-Derived Bioactive Peptides for Human Nutrition and Health vol.62, pp.38, 2014, https://doi.org/10.1021/jf502420h
  22. 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
  23. 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
  24. Production of Eco-friendly Aminotosan®Fertilizer from Waste Livestock Blood using Chitosan Coagulation vol.48, pp.6, 2015, https://doi.org/10.7745/KJSSF.2015.48.6.724
  25. Verification of the Fractions with Strong Estrogenic Activities from Brown Algae vol.20, pp.12, 2010, https://doi.org/10.5352/JLS.2010.20.12.1807
  26. Bioactive compounds in seaweed: functional food applications and legislation vol.23, pp.3, 2011, https://doi.org/10.1007/s10811-010-9632-5
  27. In vitro assessment of the cardioprotective, anti-diabetic and antioxidant potential of Palmaria palmata protein hydrolysates vol.25, pp.6, 2013, https://doi.org/10.1007/s10811-013-0017-4
  28. The Effects of Seaweed Gongjindan on Estrogen like Activities, Platelet Aggregation and Serum Lipid Levels in Ovariectomized Rats vol.23, pp.9, 2013, https://doi.org/10.5352/JLS.2013.23.9.1155
  29. Algal Proteins: Extraction, Application, and Challenges Concerning Production vol.6, pp.5, 2017, https://doi.org/10.3390/foods6050033
  30. Inhibitory Effects of Solvent Extracts from Seven Brown Algae on Mutagenicity and Growth of Human Cancer Cells vol.16, pp.7, 2006, https://doi.org/10.5352/JLS.2006.16.7.1080
  31. Effects of Mandarin, Broccoli, Cabbage, and Carrot Concentrate on in Vitro Biological Activities of Lactic Acid Bacteria-Fermented Cereal Mixtures of Rice Bran and Germinated Barley vol.33, pp.6, 2017, https://doi.org/10.9724/kfcs.2017.33.6.662
  32. Overview on the Antihypertensive and Anti-Obesity Effects of Secondary Metabolites from Seaweeds vol.16, pp.7, 2018, https://doi.org/10.3390/md16070237
  33. 감태(Ecklonia cava) 줄기 및 잎의 효소적 추출물과 메탄올 추출물에 의한 항산화 활성비교 vol.35, pp.9, 2006, https://doi.org/10.3746/jkfn.2006.35.9.1139
  34. Antidiabetic Potential of Marine Brown Algae—a Mini Review vol.2020, pp.None, 2006, https://doi.org/10.1155/2020/1230218
  35. Edible Seaweeds: A Potential Novel Source of Bioactive Metabolites and Nutraceuticals With Human Health Benefits vol.8, pp.None, 2006, https://doi.org/10.3389/fmars.2021.740054
  36. Macroalgae as Protein Sources-A Review on Protein Bioactivity, Extraction, Purification and Characterization vol.11, pp.17, 2006, https://doi.org/10.3390/app11177969