Journal of the Korean Society of Food Science and Nutrition (한국식품영양과학회지)

The Korean Society of Food Science and Nutrition (한국식품영양과학회)
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Effects of Fermentation on the Metabolic Activities of Pine Needle Juice

발효과정이 솔잎 착즙액의 항산화, alpha-Glucosidase 및 Angiotensin Converting Enzyme 저해 활성에 미치는 영향

  • 김소윤 (경남대학교 식품영양학과) ;
  • 이현정 (경남대학교 식품영양학과) ;
  • 박재희 (경남대학교 식품영양학과) ;
  • 김래영 (창신대학 호텔조리제빵과) ;
  • 정현숙 (조선대학교 생명공학과) ;
  • 박은주 (경남대학교 식품영양학과)
  • Received : 2012.09.18
  • Accepted : 2013.02.27
  • Published : 2013.03.31
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Abstract

The objective of this study was to compare the content and metabolic activities between fresh pine needle juice (PNJ) and fermented pine needle juice (FPNJ). A variety of factors were measured, including total phenolic content (TPC), antioxidant activity [DPPH radical scavenging activity (RSA), total radical-trapping antioxidant potential (TRAP), oxygen radical absorbance capacity (ORAC), cellular antioxidant capacity (CAC)], anti-genotoxic activity, ${\alpha}$-glucosidase inhibitory activity, and angiotensin converting enzyme (ACE) inhibitory activity. The TPC was $17.3{\pm}0.2$ and $4.6{\pm}0.0$ mg GAE/g in PNJ and FPNJ, respectively. The DPPH RSA, TRAP, and ORAC values increased in a dose-dependent manner for both PNJ and FPNJ, with significantly higher activities in PNJ than FPNJ. The CAC against AAPH-induced oxidative stress in HepG2 cells was protected by both PNJ and FPNJ. Pretreatment with PNJ and FPNJ in human leukocytes produced significant reductions in $H_2O_2$-induced DNA damage at a concentration of $50{\mu}g/mL$. ${\alpha}$-Glucosidase inhibitory activity was significantly higher in FPNJ than PNJ. The ACE inhibitory activity was about 87.1% and 60.0% in 1:1 diluted PNJ and FPNJ, respectively. This study suggests that the fermentation of PNJ could enhance the regulation of blood glucose metabolism and both PNJ and FPNJ might be a new potential source of natural antioxidant, anti-diabetic, and anti-hypertensive agents applicable to food.

솔잎착즙액과 솔잎발효액의 항산화활성을 분석하기 위하여 총 페놀함량, DPPH 라디칼 소거능, 총 항산화능, $ORAC_{ROO{\cdot}}$ 활성, CAC 활성을 분석하였고, 항유전독성을 분석하기 위하여 DNA 손상 억제능을 분석하였으며, 항당뇨효과와 항고혈압 효과를 분석하기 위하여 각각 ${\alpha}$-glucosidase 및 ACE 저해활성을 분석하였다. 총 페놀 함량은 솔잎착즙액(17.3 mg GAE/g)이 솔잎발효액(4.6 mg GAE/g)보다 유의적으로 3.7배 높았으며, 이는 발효가 진행됨에 따라 페놀 성분이 침전된 결과로 보인다. DPPH 라디칼 소거능, 총 항산화능 및 $ORAC_{ROO{\cdot}}$ 활성은 솔잎착즙액이 솔잎발효액 보다 유의적으로 높았다. 즉 1 mg/mL 수준에서 솔잎착즙액과 솔잎발효액의 DPPH 라디칼 소거능은 각각 33.3%, 21.4%로 나타났고, $60{\sim}530{\mu}g/mL$ 농도에서 솔잎착즙액이 솔잎발효액보다 유의적으로 높은 총 항산화능을 나타내었으며, $2{\sim}100{\mu}g/mL$ 농도에서 솔잎착즙액이 솔잎발효액보다 유의적으로 높은 $ORAC_{ROO{\cdot}}$ 활성을 나타내었다. 솔잎착즙액과 솔잎발효액의 CAC 활성은 AAPH 처리군보다 솔잎착즙액 및 솔잎발효액 처리군의 CAC 활성이 농도 의존적으로 증가하였으며, $50{\mu}g/mL$ 농도를 제외하고 두 그룹 간의 유의적인 차이는 나타나지 않았다. 솔잎착즙액과 솔잎발효액의 항산화활성의 상관관계는 총 항산화능과 DPPH 라디칼소거능(r=0.836, p=0.000) 및 ORAC assay(r=0.918, p=0.000) 간의 높은 양의 상관관계가 나타났을 뿐만 아니라 DPPH 라디칼 소거능과 ORAC assay(r=0.909, p=0.000) 간에도 높은 양의 상관관계가 나타나 솔잎착즙액과 솔잎발효액의 높은 항산화활성을 추측할 수 있었다. $H_2O_2$로 유도된 산화적 스트레스에 대한 DNA 손상 억제능은 솔잎착즙액과 솔잎발효액에서 농도의존적으로 증가하였으며, $50{\mu}g/mL$ 농도에서 솔잎발효액이 솔잎착즙액보다 더 높은 경향을 나타내었다. 솔잎착즙액과 솔잎발효액의 항당뇨 효과를 알아보기 위하여 ${\alpha}$-glucosidase 억제능을 실험한 결과 희석배율이 증가할수록 솔잎발효액의 ${\alpha}$-glucosidase 억제능은 급격히 감소하는 반면, 솔잎착즙액은 솔잎발효액보다 높은 활성을 유지하는 것으로 나타났다. 항고혈압 효과 분석을 위한 ACE 저해활성은 2배 희석 시 솔잎착즙액 87.1%, 솔잎발효액 60.0%로 솔잎착즙액의 ACE 저해활성이 높은 경향을 나타내었다. 본 연구를 통해 솔잎착즙액의 다양한 생리활성을 평가하고자 하였으며, 발효가 이러한 생리활성에 미치는 영향을 분석하고자 하였다. 본 연구에서 2년간 발효한 솔잎발효액만을 분석하였고, 발효기간에 따른 활성의 변화를 평가하지 못한 제한점이 있으나 본 연구의 결과는 지금까지 연구가 미흡했던 솔잎착즙액의 생리활성을 보고함으로써 솔잎을 활용한 기능성 소개개발에 유용한 자료로 제안될 수 있을 것이다. 또한 향후 연구에서 솔잎착즙액의 기능성을 증대시킬 수 있는 발효과정에 대한 연구가 수행되어야 할 것이다.

Keywords

References

  1. Poirer MC, Western A. 2002. DNA damage, DNA repair, and mutagenesis. In Encyclopedia of Cancer. Bertino JR, ed. Academic Press, Boston, MA, USA. p 79-87.
  2. Gutteridege JMC, Halliwel B. 1994. Antioxidants in Nutrition, Health, and Disease. Oxford University Press, Oxford, UK. p 1-62.
  3. Lee JM, Son ES, Oh SS, Han DS. 2001. Contents of total flavonoid and biological activities of edible plants. Korean J Dietary Culture 16: 504-514.
  4. Kim JH, Park JH, Park SD, Choi SY, Seong JH, Mon KD. 2002. Preparation and antioxidant activity of health drink with extract powders from safflower (Carthamus tinctorius L.) seed. Korean J Food Sci Technol 34: 617-624.
  5. Choi HY. 2009. Antioxidant activity and quality characteristics of pine needle cookies. J Korean Soc Food Sci Nutr 38: 1414-1421. https://doi.org/10.3746/jkfn.2009.38.10.1414
  6. RDA. 2006. Food Composition Table. 7th ed. Rural Development Administration, National Institute of Agricultural Science and Technology, Rural Resources Development Institute, Suwon, Korea. p 402-403.
  7. Lim YS, Bae MJ, Lee SH. 2002. Antimicrobial effects of Pinus densiflora Sieb. et Zucc. ethanol extract on Listeria monocytogenes. J Korean Soc Food Sci Nutr 31: 333-337. https://doi.org/10.3746/jkfn.2002.31.2.333
  8. Lee OH, Kim KY, Jang MK, Yu KH, Kim SG, Kim MH, Lee SH. 2008. Evaluation of proanthocyanidin contents in total polyphenolic compounds of pine (Pinus densiflora) needle extracts and their antioxidative activities. J Life Sci 18: 213-219. https://doi.org/10.5352/JLS.2008.18.2.213
  9. Kim SM, Cho YS, Sung SK, Lee IG, Lee SH, Kim DG. 2002. Antioxidative and nitrite scavenging activity of pine needle and green tea extracts. Korean J Food Sci Ani Resour 22: 13-19.
  10. Yoo JH, Cha JY, Jeong YK, Chung KT, Cho YS. 2004. Antioxidative effects of pine (Pinus denstifora) needle extracts. J Life Sci 14: 863-867. https://doi.org/10.5352/JLS.2004.14.5.863
  11. Choi EM. 2007. Antinociceptive and antiinflammatory activity of pine (Pinus densiflora) pollen extract. Phytother Res 21: 471-475. https://doi.org/10.1002/ptr.2103
  12. Choi HD, Koh YJ, Choi IW, Kim YS, Park YK. 2007. Anticariogenic activity and glucosyltransferase inhibitory effects of extracts from pine needle and twig. Korean J Food Sci Technol 39: 336-341.
  13. Jeon JR, Kim JY, Lee KM, Cho DH. 2005. Anti-obese effects of mixture contained pine needle, black tea and green tea extracts. J Korean Soc Appl Biol Chem 48: 375-381.
  14. Kang YH, Park YK, Ha TY, Moon KD. 1996. Effects of pine needle extracts on serum and liver lipid contents in rats fed high fat diet. J Korean Soc Food Nutr 25: 367-373.
  15. Boo YC, Jeon CO, Oh JY. 1994. Isolation of 4-hydroxy-5- methyl-3[2H]-furanone from pine needles as an antioxidative principle. Agric Chem Biotechnol 37: 310-314.
  16. Kim NM, Lee JW, Do JH, Yang JW. 2003. Effects of the fermentation periods on the qualities and functionalities of the fermentation broth of wild vegetables. Korean J Food Sci Technol 35: 272-279.
  17. Cha JY, Yang HJ, Jeong JJ, Seo WS, Park JS, Ok M, Cho YS. 2010. Tyrosinase inhibition activity and antioxidant capacity by fermented products of some medicinal plants. J Life Sci 20: 940-947. https://doi.org/10.5352/JLS.2010.20.6.940
  18. Jung KH, Park CS. 2012. Physiological activities of fermented garlic broth during fermentation. Korean J Food Preserv 19: 406-412. https://doi.org/10.11002/kjfp.2012.19.3.406
  19. Kim MJ, Yang SA, Park JH, Kim HJ, Lee SP. 2011. Quality characteristics and anti-proliferative effects of dropwort extracts fermented with fructooligosaccarides on HepG2 cells. Korean J Food Sci Technol 43: 432-437. https://doi.org/10.9721/KJFST.2011.43.4.432
  20. Cho EK, Chol HE, Choi YJ. 2010. Antioxidant and antibacterial activities, and tyrosinase and elastase inhibitory effect of fermented Omija (Schizandra chinensis Baillon.) beverage. J Appl Biol Chem 53: 212-218. https://doi.org/10.3839/jabc.2010.038
  21. Park GY, Li HX, Hwang ID, Cheong HS. 2006. The functional effects of fermented pine needle extract. Korean J Biotechnol Bioeng 21: 376-383.
  22. Folin O, Denis W. 1912. On phosphotungstic-phosphomolybdic compounds as color reagents. J Biol Chem 12: 239-243.
  23. Mensor LL, Menezes FS, Leitão GG, Reis AS, dos Santos TC, Coube CS, Leitao SG. 2001. Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical method. Phytother Res 15: 127-130. https://doi.org/10.1002/ptr.687
  24. Rice-Evans C, Miller NJ. 1994. Total antioxidant status in plasma and body fluids. Methods Enzymol 234: 279-293. https://doi.org/10.1016/0076-6879(94)34095-1
  25. Kurihara H, Fukami H, Asami S, Toyoda Y, Nakai M, Shibata H, Yao XS. 2004. Effects of oolong tea on plasma antioxidative capacity in mice loaded with restraint stress assessed using the oxygen radical absorbance capacity (ORAC) assay. Biol Pharm Bull 27: 1093-1098. https://doi.org/10.1248/bpb.27.1093
  26. Ou B, Hampsch-Woodill M, Prior RL. 2001. Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe. J Agric Food Chem 49: 4619-4626. https://doi.org/10.1021/jf010586o
  27. Lautraite S, Bigot-Lasserre D, Bars R, Carmichael N. 2003. Optimisation of cell-based assays for medium throughput screening of oxidative stress. Toxicol In Vitro 17: 207-220. https://doi.org/10.1016/S0887-2333(03)00005-5
  28. Shrestha BM. 2012. The Declaration of Helsinki in relation to medical research: historical and current perspectives. J Nepal Health Res Counc 10: 254-257.
  29. Singh NP, McCoy MT, Tice RR, Schneider EL. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175: 184-191. https://doi.org/10.1016/0014-4827(88)90265-0
  30. Kim HY, Jun BS, Kim SK, Cha JY, Cho YS. 2000. Polyphenolic compound content and antioxidative activities by extracts from seed, sprout and flower of safflower (Carthamus tinctorius L.). J Korean Soc Food Sci Nutr 29: 1127-1132.
  31. Van Buren JP, Robinson WB. 1969. Formation of complexes between protein and tannic acid. J Agric Food Chem 17: 772-777. https://doi.org/10.1021/jf60164a003
  32. Oh HI, Hoff JE. 1987. pH dependence of complex formation between condensed tannins and proteins. J Food Sci 52: 1267-1269. https://doi.org/10.1111/j.1365-2621.1987.tb14059.x
  33. Lee SJ, Lee KW, Hur HJ, Chun JY, Kim SY, Lee HJ. 2007. Phenolic phytochemicals derived from red pine (Pinus densiflora) inhibit the invasion and migration of SK-Hep-1 human hepatocellular carcinoma cells. Ann N Y Acad Sci 1095: 536-544. https://doi.org/10.1196/annals.1397.058
  34. Kwak CS, Moon SC, Lee MS. 2006. Antioxidant, antimutagenic, and antitumor effects of pine needles (Pinus densiflora). Nutr Cancer 56: 162-171. https://doi.org/10.1207/s15327914nc5602_7
  35. González-Castejón M, Rodriguez-Casado A. 2011. Dietary phytochemicals and their potential effects on obesity: a review. Pharmacol Res 64: 438-455. https://doi.org/10.1016/j.phrs.2011.07.004
  36. Ariga T, Hamano M. 1990. Radical scavenging action and its mode in procyanidins B-1, and B-3 from azuki beans to peroxyl radicals. Agric Biol Chem 54: 2499-2504. https://doi.org/10.1271/bbb1961.54.2499
  37. Ricardo Da Silva JM, Darman N, Fernandez Y, Mitjavila S. 1991. Oxygen free radical scavenger capacity in aqueous models of different procyanidins from grape seeds. J Agric Food Chem 39: 1549-1552. https://doi.org/10.1021/jf00009a002
  38. Kim NY, Jang MK, Lee DG, Yu KH, Jang H, Kim M, Kim SG, Yoo BH, Lee SH. 2010. Comparison of methods for proanthocyanidin extraction from pine (Pinus densiflora) needles and biological activities of the extracts. Nutr Res Pract 4: 16-22. https://doi.org/10.4162/nrp.2010.4.1.16
  39. Park YS, Jeon MH, Hwang HJ, Park MR, Lee SH, Kim SG, Kim M. 2011. Antioxidant activity and analysis of proanthocyanidins from pine (Pinus densiflora) needles. Nutr Res Pract 5: 281-287. https://doi.org/10.4162/nrp.2011.5.4.281
  40. Kim KB, Yoo KH, Park HY, Jeong JM. 2006. Anti-oxidative activities of commercial edible plant extracts distributed in Korea. J Korean Soc Appl Biol Chem 49: 328-333.
  41. Cherdshewasart W, Sutjit W. 2008. Correlation of antioxidant activity and major isoflavonoid contents of the phytoestrogen-rich Pueraria mirifica and Pueraria lobata tubers. Phytomedicine 15: 38-43. https://doi.org/10.1016/j.phymed.2007.07.058
  42. Gheldof N, Engeseth NJ. 2002. Antioxidant capacity of honeys from various floral sources based on the determination of oxygen radical absorbance capacity and inhibition of in vitro lipoprotein oxidation in human serum samples. J Agric Food Chem 50: 3050-3055. https://doi.org/10.1021/jf0114637
  43. Choi JH, Kim HS, Jung MJ, Choi JS. 2001. (+)-Catechin, an antioxidant principle from the leaves of Pinus densiflora that acts on 1,1-diphenyl-2-picrylhydrazyl radical. Nat Prod Sci 7: 1-4.
  44. Ruiz-Larrea MB, Leal AM, Liza M, Lacort M, de Groot H. 1994. Antioxidant effects of estradiol and 2-hydroxyestradiol on iron-induced lipid peroxidation of rat liver microsomes. Steroids 59: 383-388. https://doi.org/10.1016/0039-128X(94)90006-X
  45. Jung MJ, Chung HY, Choi JH, Choi JS. 2003. Antioxidant principles from the needles of red pine, Pinus densiflora. Phytother Res 17: 1064-1068. https://doi.org/10.1002/ptr.1302
  46. Prior RL, Wu X, Schaich K. 2005. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53: 4290-4302. https://doi.org/10.1021/jf0502698
  47. Jung MJ, Jung HA, Kang SS, Hwang GS, Choi JS. 2009. A new abietic acid-type diterpene glucoside from the needles of Pinus densiflora. Arch Pharm Res 32: 1699-1704. https://doi.org/10.1007/s12272-009-2206-x
  48. Keston AS, Brandt R. 1965. The fluorometric analysis of ultramicro quantities of hydrogen peroxide. Anal Biochem 11: 1-5. https://doi.org/10.1016/0003-2697(65)90034-5
  49. Takamatsu S, Galal AM, Ross SA, Ferreira D, ElSohly MA, Ibrahim AR, El-Feraly FS. 2003. Antioxidant effect of flavonoids on DCF production in HL-60 cells. Phytotber Res 17: 963-966. https://doi.org/10.1002/ptr.1289
  50. Collins AR. 2004. The comet assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol 26: 249-261. https://doi.org/10.1385/MB:26:3:249
  51. Poli P, Buschini A, Restivo FM, Ficarelli A, Cassoni F, Ferrero I, Rossi C. 1999. Comet assay application in environmental monitoring: DNA damage in human leukocytes and plant cells in comparison with bacterial and yeast tests. Mutagenesis 14: 547-556. https://doi.org/10.1093/mutage/14.6.547
  52. Soltani F, Mosaffa F, Iranshahi M, Karimi G, Malekaneh M, Haghighi F, Behravan J. 2009. Evaluation of antigenotoxicity effects of umbelliprenin on human peripheral lymphocytes exposed to oxidative stress. Cell Biol Toxicol 25: 291-296. https://doi.org/10.1007/s10565-008-9083-9
  53. Jeong JB, Seo EW, Jeong HJ. 2009. Effect of extracts from pine needle against oxidative DNA damage and apoptosis induced by hydroxyl radical via antioxidant activity. Food Chem Toxicol 47: 2135-2141. https://doi.org/10.1016/j.fct.2009.05.034
  54. Tappel AL. 1980. Vitamin E and selenium protection from in vivo lipid peroxidation. Ann N Y Acad Sci 355: 18-31. https://doi.org/10.1111/j.1749-6632.1980.tb21324.x
  55. van de Laar FA, Lucassen PL, Akkermans RP, van de Lisdonk EH, Rutten GE, van Weel C. 2005. ${\alpha}$-Glucosidase inhibitors for patients with type 2 diabetes: results from a Cochrane systematic review and meta-analysis. Diabetes Care 28: 154-163. https://doi.org/10.2337/diacare.28.1.154
  56. Maruyama SK, Nakagomi N, Tomizuka N, Suzuki H. 1985. Angiotensin I-converting enzyme inhibitor derived from an enzymatic hydrolysate of casein. II. Isolation and bradykinin- potentiating activity on the uterus and the ileum of rats. Agric Biol Chem 49: 1405-1410. https://doi.org/10.1271/bbb1961.49.1405
  57. Hong TG, Lee YR, Yim MH, Hyun CN. 2004. Physiological functionality and nitrite scavenging ability of fermentation extracts from pine needles. Korean J Food Preserv 11: 94-99.
  58. Cho EK, Song HJ, Cho HE, Kim MH, Choi IS, Choi YJ. 2009. Inhibitory effects of ethanol extracts from pine buds (Pinus densiflora) on angiotensin converting enzyme, xanthine oxidase and nitric oxide synthesis. J Life Sci 19: 1629-1636. https://doi.org/10.5352/JLS.2009.19.11.1629
  59. Bae IY, Shin HK, Yang CB. 1999. Studies on the inhibitory activity of angiotensin I converting enzyme of various vegetables. The Journal of Korean Living Science Research 17: 5-15.

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