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References

  1. Rousi A. 1971. The genus Hippophaë L. A taxonomic study. Ann. Bot. Fennici 8: 177-227.
  2. Zeb A. 2004. Important therapeutic uses of sea buckthorn (Hippophae): a review. J. Biol. Sci. 4: 687-693.
    CrossRef
  3. Guliyev VB, Gul M, Yildirim A. 2004. Hippophae rhamnoides L.:chromatographic methods to determine chemical composition, use in traditional medicine and pharmacological effects. J. Chromatogr. B 812: 291-307.
    CrossRef
  4. Eastwood MA. 1999. Interaction of dietary antioxidants in vivo: how fruit and vegetables prevent disease? Q. J. Med. 92: 527-530.
    CrossRef
  5. Nimse SB, Pal D. 2015. Free radicals, natural antioxidants, and their reaction mechanisms. RSC Adv. 5: 27986-28006.
    CrossRef
  6. Pham-Huy LA, He H, Pham-Huy C. 2008. Free radicals, antioxidants in disease and health. Int. J. Biomed. Sci. 4: 89-96.
    Pubmed PMC
  7. Pandey KB, Rizvi SI. 2009. Plant polyphenols as dietary antioxidants in human health and disease. Oxid. Med. Cell. Longev. 2: 270-278.
    Pubmed PMC CrossRef
  8. Basu M, Prasad R, Jayamurthy P, Pal K, Arumughan C, Sawhney RC. 2007. Anti-atherogenic effects of seabuckthorn (Hippophaea rhamnoides) seed oil. Phytomedicine 14: 770-777.
    Pubmed CrossRef
  9. Ganju L, Padwad Y, Singh R, Karan D, Chanda S, Chopra MK, et al. 2005. Anti-inflammatory activity of seabuckthorn (Hippophae rhamnoides) leaves. Int. Immunopharmacol. 5: 1675-1684.
    Pubmed CrossRef
  10. Süleyman H, Demirezer LÖ, Büyükokuroglu ME, Akcay MF, Gepdiremen A, Banoglu ZN, Göçer F. 2001. Antiulcerogenic effect of Hippophae rhamnoides L. Phytother. Res. 15: 625-627.
    Pubmed CrossRef
  11. Gao Z-L, Gu X-H, Cheng F-T, Jiang F-H. 2003. Effect of sea buckthorn on liver fibrosis: a clinical study. World J. Gastroenterol. 9: 1615-1617.
    Pubmed PMC CrossRef
  12. Gupta A , Kumar R, Pal K, Banerjee PK, Sawhney RC. 2005. A preclinical study of the effects of seabuckthorn (Hippophae rhamnoides L.) leaf extract on cutaneous wound healing in albino rats. Int. J. Low. Extrem. Wounds 4: 88-92.
    Pubmed CrossRef
  13. Geetha S, Ram MS, Singh V, Ilavazhagan G, Sawhney RC. 2002. Anti-oxidant and immunomodulatory properties of seabuckthorn (Hippophae rhamnoides) - an in vitro study. J. Ethnopharmacol. 79: 373-378.
    CrossRef
  14. Geetha S, Singh V, Ram MS, Ilavazhagan G, Banerjee PK, Sawhney RC. 2005. Immunomodulatory effects of seabuckthorn (Hippophae rhamnoides L.) against chromium(VI) induced immunosuppression. Mol. Cell. Biochem. 278: 101-109.
    Pubmed CrossRef
  15. Upadhyay NK, Kumar MSY, Gupta A. 2010. Antioxidant, cytoprotective and antibacterial effects of sea buckthorn (Hippophae rhamnoides L.) leaves. Food Chem. Toxicol. 48:3443-3448.
    Pubmed CrossRef
  16. Kumar MSY, Dutta R, Prasad D, Misra K. 2011. Subcritical water extraction of antioxidant compounds from seabuckthorn (Hippophae rhamnoides) leaves for the comparative evaluation of antioxidant activity. Food Chem. 127: 1309-1316.
    Pubmed CrossRef
  17. Narayanan S, Ruma D, Gitika B, Sharma SK, Pauline T, Ram MS, et al. 2005. Antioxidant activities of seabuckthorn (Hippophae rhamnoides) during hypoxia induced oxidative stress in glial cells. Mol. Cell. Biochem. 278: 9-14.
    Pubmed CrossRef
  18. Emerit J, Edeas M, Bricaire F. 2004. Neurodegenerative diseases and oxidative stress. Biomed. Pharmacother. 58: 39-46.
    Pubmed CrossRef
  19. Cassarino DS, Bennett JP Jr. 1999. An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 29: 1-25.
    CrossRef
  20. Whittemore ER, Loo DT, Watt JA, Cotman CW. 1995. A detailed anaylsis of hydrogen peroxide-induced cell death in primary neuronal culture. Neuroscience 67: 921-932.
    CrossRef
  21. Koh J-Y, Gwag BJ, Lobner D, Choi DW. 1995. Potentiated necrosis of cultured cortical neurons by neurotrophins. Science 268: 573-575.
    Pubmed CrossRef
  22. Kim D-O, Jeong SW, Lee CY. 2003. Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem. 81: 321-326.
    CrossRef
  23. Kim D-O, Lee KW, Lee HJ, Lee CY. 2002. Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J. Agric. Food Chem. 50: 3713-3717.
    Pubmed CrossRef
  24. Gao X, Ohlander M, Jeppsson N, Björk L, Trajkovski V. 2000. Changes in antioxidant effects and their relationship to phytonutrients in fruits of sea buckthorn (Hippophae rhamnoides L.) during maturation. J. Agric. Food Chem. 48:1485-1490.
    Pubmed CrossRef
  25. Lima VLAG, Mélo EA, Maciel MIS, Prazeres FG, Musser RS, Lima DES. 2005. Total phenolic and carotenoid contents in acerola genotypes harvested at three ripening stages. Food Chem. 90: 565-568.
    CrossRef
  26. Jeppsson N, Gao X. 2000. Changes in the contents of kaempherol, quercetin, and L-ascorbic acid in sea buckthorn berries during maturation. Agric. Food Sci. 9: 17-22.
  27. Kallio H, Yang B, Peippo P. 2002. Effects of different origins and harvesting time on vitamin C, tocopherols, and tocotrienols in sea buckthorn (Hippophae rhamnoides) berries. J. Agric. Food Chem. 50: 6136-6142.
    Pubmed CrossRef
  28. Chen C, Zhang H, Xiao W, Yong Z-P, Bai N. 2007. Highperformance liquid chromatographic fingerprint analysis for different origins of sea buckthorn berries. J. Chromatogr. A 1154: 250-259.
    Pubmed CrossRef
  29. Andersson SC, Olsson ME, Johansson E, Rumpunen K. 2009. Carotenoids in sea buckthorn (Hippophae rhamnoides L.) berries during ripening and use of pheophytin a as a maturity marker. J. Agric. Food Chem. 57: 250-258.
    Pubmed CrossRef
  30. Zu Y, Li C, Fu Y, Zhao C. 2006. Simultaneous determination of catechin, rutin, quercetin, kaempferol and isorhamnetin in the extract of sea buckthorn (Hippophae rhamnoides L.) leaves by RP-HPLC with DAD. J. Pharm. Biomed. Anal. 41:714-719.
    Pubmed CrossRef
  31. Kim D-O, Lee CY. 2004. Comprehensive study of vitamin C equivalent antioxidant capacity (VCEAC) of various polyphenolics in scavenging a free radical and its structural relationship. Crit. Rev. Food Sci. Nutr. 44: 253-273.
    Pubmed CrossRef
  32. Liu P, Deng T, Hou X, Wang J. 2009. Antioxidant properties of isolated isorhamnetin from the sea buckthorn marc. Plant Foods Hum. Nutr. 64: 141-145.
    Pubmed CrossRef
  33. Kim G-N, Jang H-D. 2009. Protective mechanism of quercetin and rutin using glutathione metabolism on H2O2induced oxidative stress in HepG2 cells. Ann. N. Y. Acad. Sci. 1171: 530-537.
    Pubmed CrossRef
  34. Crispo JAG, Ansell DR, Piche M, Eibl JK, Khaper N, Ross GM, Tai TC. 2010. Protective effects of polyphenolic compounds on oxidative stress-induced cytotoxicity in PC12 cells. Can. J. Physiol. Pharmacol. 88: 429-438.
    Pubmed CrossRef
  35. Costa LG, Garrick JM, Roquè PJ, Pellacani C. 2016. Mechanisms of neuroprotection by quercetin: counteracting oxidative stress and more. Oxid. Med. Cell. Longev. 2016:2986796.
    Pubmed PMC CrossRef
  36. Kumar ADN, Bevara GB, Kaja LK, Badana AK, Malla RR. 2016. Protective effect of 3-O-methyl quercetin and kaempferol from Semecarpus anacardium against H2O2 induced cytotoxicity in lung and liver cells. BMC Complement. Altern. Med. 16: 376.
    Pubmed PMC CrossRef
  37. Sepand MR, Ghahremani MH, Razavi-Azarkhiavi K, Aghsami M, Rajabi J, Keshavarz-Bahaghighat H, et al. 2016. Ellagic acid confers protection against gentamicin-induced oxidative damage, mitochondrial dysfunction and apoptosisrelated nephrotoxicity. J. Pharm. Pharmacol. 68: 1222-1232.
    Pubmed CrossRef
  38. Hong S-Y, Jeong W-S, Jun M. 2012. Protective effects of the key compounds isolated from Corni fructus against β-amyloidinduced neurotoxicity in PC12 cells. Molecules 17: 10831-10845.
    Pubmed CrossRef
  39. Kang MK, Kang NJ, Jang YJ, Lee KW, Lee HJ. 2009. Gallic acid induces neuronal cell death through activation of c-Jun N-terminal kinase and downregulation of Bcl-2. Ann. N. Y. Acad. Sci. 1171: 514-520.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(7): 1257-1265

Published online July 28, 2017 https://doi.org/10.4014/jmb.1704.04033

Copyright © The Korean Society for Microbiology and Biotechnology.

Sea Buckthorn (Hippophae rhamnoides L.) Leaf Extracts Protect Neuronal PC-12 Cells from Oxidative Stress

Chi Heung Cho 1, Holim Jang 2, Migi Lee 3, Hee Kang 4, Ho Jjn Heo 5 and Dae-Ok Kim 1*

1Department of Food Science and Biotechnology, Kyung Hee University, Yongin 17104, Republic of Korea, 2Damtuh Co., Ltd., Seoul 06561, Republic of Korea, 3Biocenter, Gyeonggido Business and Science Accelerator, Suwon 16229, Republic of Korea, 4Graduate School of East-West Medical Science, Kyung Hee University, Yongin 17104, Republic of Korea, 5Division of Applied Life Science (BK21 Plus), Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 52828, Republic of Korea

Received: April 14, 2017; Accepted: May 21, 2017

Abstract

The present study was carried out to investigate the antioxidative and neuroprotective effects
of sea buckthorn (Hippophae rhamnoides L.) leaves (SBL) harvested at different times. Reversedphase
high-performance liquid chromatography analysis revealed five major phenolic
compounds: ellagic acid, gallic acid, isorhamnetin, kaempferol, and quercetin. SBL harvested
in August had the highest total phenolic and flavonoid contents and antioxidant capacity.
Treatment of neuronal PC-12 cells with the ethyl acetate fraction of SBL harvested in August
increased their viability and membrane integrity and reduced intracellular oxidative stress in
a dose-dependent manner. The relative populations of both early and late apoptotic PC-12
cells were decreased by treatment with the SBL ethyl acetate fraction, based on flow cytometry
analysis using annexin V-FITC/PI staining. These findings suggest that SBL can serve as a
good source of antioxidants and medicinal agents that attenuate oxidative stress.

Keywords: Antioxidant capacity, apoptosis, flow cytometry, high-performance liquid chromatography, total phenolics, total flavonoids

References

  1. Rousi A. 1971. The genus Hippophaë L. A taxonomic study. Ann. Bot. Fennici 8: 177-227.
  2. Zeb A. 2004. Important therapeutic uses of sea buckthorn (Hippophae): a review. J. Biol. Sci. 4: 687-693.
    CrossRef
  3. Guliyev VB, Gul M, Yildirim A. 2004. Hippophae rhamnoides L.:chromatographic methods to determine chemical composition, use in traditional medicine and pharmacological effects. J. Chromatogr. B 812: 291-307.
    CrossRef
  4. Eastwood MA. 1999. Interaction of dietary antioxidants in vivo: how fruit and vegetables prevent disease? Q. J. Med. 92: 527-530.
    CrossRef
  5. Nimse SB, Pal D. 2015. Free radicals, natural antioxidants, and their reaction mechanisms. RSC Adv. 5: 27986-28006.
    CrossRef
  6. Pham-Huy LA, He H, Pham-Huy C. 2008. Free radicals, antioxidants in disease and health. Int. J. Biomed. Sci. 4: 89-96.
    Pubmed KoreaMed
  7. Pandey KB, Rizvi SI. 2009. Plant polyphenols as dietary antioxidants in human health and disease. Oxid. Med. Cell. Longev. 2: 270-278.
    Pubmed KoreaMed CrossRef
  8. Basu M, Prasad R, Jayamurthy P, Pal K, Arumughan C, Sawhney RC. 2007. Anti-atherogenic effects of seabuckthorn (Hippophaea rhamnoides) seed oil. Phytomedicine 14: 770-777.
    Pubmed CrossRef
  9. Ganju L, Padwad Y, Singh R, Karan D, Chanda S, Chopra MK, et al. 2005. Anti-inflammatory activity of seabuckthorn (Hippophae rhamnoides) leaves. Int. Immunopharmacol. 5: 1675-1684.
    Pubmed CrossRef
  10. Süleyman H, Demirezer LÖ, Büyükokuroglu ME, Akcay MF, Gepdiremen A, Banoglu ZN, Göçer F. 2001. Antiulcerogenic effect of Hippophae rhamnoides L. Phytother. Res. 15: 625-627.
    Pubmed CrossRef
  11. Gao Z-L, Gu X-H, Cheng F-T, Jiang F-H. 2003. Effect of sea buckthorn on liver fibrosis: a clinical study. World J. Gastroenterol. 9: 1615-1617.
    Pubmed KoreaMed CrossRef
  12. Gupta A , Kumar R, Pal K, Banerjee PK, Sawhney RC. 2005. A preclinical study of the effects of seabuckthorn (Hippophae rhamnoides L.) leaf extract on cutaneous wound healing in albino rats. Int. J. Low. Extrem. Wounds 4: 88-92.
    Pubmed CrossRef
  13. Geetha S, Ram MS, Singh V, Ilavazhagan G, Sawhney RC. 2002. Anti-oxidant and immunomodulatory properties of seabuckthorn (Hippophae rhamnoides) - an in vitro study. J. Ethnopharmacol. 79: 373-378.
    CrossRef
  14. Geetha S, Singh V, Ram MS, Ilavazhagan G, Banerjee PK, Sawhney RC. 2005. Immunomodulatory effects of seabuckthorn (Hippophae rhamnoides L.) against chromium(VI) induced immunosuppression. Mol. Cell. Biochem. 278: 101-109.
    Pubmed CrossRef
  15. Upadhyay NK, Kumar MSY, Gupta A. 2010. Antioxidant, cytoprotective and antibacterial effects of sea buckthorn (Hippophae rhamnoides L.) leaves. Food Chem. Toxicol. 48:3443-3448.
    Pubmed CrossRef
  16. Kumar MSY, Dutta R, Prasad D, Misra K. 2011. Subcritical water extraction of antioxidant compounds from seabuckthorn (Hippophae rhamnoides) leaves for the comparative evaluation of antioxidant activity. Food Chem. 127: 1309-1316.
    Pubmed CrossRef
  17. Narayanan S, Ruma D, Gitika B, Sharma SK, Pauline T, Ram MS, et al. 2005. Antioxidant activities of seabuckthorn (Hippophae rhamnoides) during hypoxia induced oxidative stress in glial cells. Mol. Cell. Biochem. 278: 9-14.
    Pubmed CrossRef
  18. Emerit J, Edeas M, Bricaire F. 2004. Neurodegenerative diseases and oxidative stress. Biomed. Pharmacother. 58: 39-46.
    Pubmed CrossRef
  19. Cassarino DS, Bennett JP Jr. 1999. An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 29: 1-25.
    CrossRef
  20. Whittemore ER, Loo DT, Watt JA, Cotman CW. 1995. A detailed anaylsis of hydrogen peroxide-induced cell death in primary neuronal culture. Neuroscience 67: 921-932.
    CrossRef
  21. Koh J-Y, Gwag BJ, Lobner D, Choi DW. 1995. Potentiated necrosis of cultured cortical neurons by neurotrophins. Science 268: 573-575.
    Pubmed CrossRef
  22. Kim D-O, Jeong SW, Lee CY. 2003. Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem. 81: 321-326.
    CrossRef
  23. Kim D-O, Lee KW, Lee HJ, Lee CY. 2002. Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J. Agric. Food Chem. 50: 3713-3717.
    Pubmed CrossRef
  24. Gao X, Ohlander M, Jeppsson N, Björk L, Trajkovski V. 2000. Changes in antioxidant effects and their relationship to phytonutrients in fruits of sea buckthorn (Hippophae rhamnoides L.) during maturation. J. Agric. Food Chem. 48:1485-1490.
    Pubmed CrossRef
  25. Lima VLAG, Mélo EA, Maciel MIS, Prazeres FG, Musser RS, Lima DES. 2005. Total phenolic and carotenoid contents in acerola genotypes harvested at three ripening stages. Food Chem. 90: 565-568.
    CrossRef
  26. Jeppsson N, Gao X. 2000. Changes in the contents of kaempherol, quercetin, and L-ascorbic acid in sea buckthorn berries during maturation. Agric. Food Sci. 9: 17-22.
  27. Kallio H, Yang B, Peippo P. 2002. Effects of different origins and harvesting time on vitamin C, tocopherols, and tocotrienols in sea buckthorn (Hippophae rhamnoides) berries. J. Agric. Food Chem. 50: 6136-6142.
    Pubmed CrossRef
  28. Chen C, Zhang H, Xiao W, Yong Z-P, Bai N. 2007. Highperformance liquid chromatographic fingerprint analysis for different origins of sea buckthorn berries. J. Chromatogr. A 1154: 250-259.
    Pubmed CrossRef
  29. Andersson SC, Olsson ME, Johansson E, Rumpunen K. 2009. Carotenoids in sea buckthorn (Hippophae rhamnoides L.) berries during ripening and use of pheophytin a as a maturity marker. J. Agric. Food Chem. 57: 250-258.
    Pubmed CrossRef
  30. Zu Y, Li C, Fu Y, Zhao C. 2006. Simultaneous determination of catechin, rutin, quercetin, kaempferol and isorhamnetin in the extract of sea buckthorn (Hippophae rhamnoides L.) leaves by RP-HPLC with DAD. J. Pharm. Biomed. Anal. 41:714-719.
    Pubmed CrossRef
  31. Kim D-O, Lee CY. 2004. Comprehensive study of vitamin C equivalent antioxidant capacity (VCEAC) of various polyphenolics in scavenging a free radical and its structural relationship. Crit. Rev. Food Sci. Nutr. 44: 253-273.
    Pubmed CrossRef
  32. Liu P, Deng T, Hou X, Wang J. 2009. Antioxidant properties of isolated isorhamnetin from the sea buckthorn marc. Plant Foods Hum. Nutr. 64: 141-145.
    Pubmed CrossRef
  33. Kim G-N, Jang H-D. 2009. Protective mechanism of quercetin and rutin using glutathione metabolism on H2O2induced oxidative stress in HepG2 cells. Ann. N. Y. Acad. Sci. 1171: 530-537.
    Pubmed CrossRef
  34. Crispo JAG, Ansell DR, Piche M, Eibl JK, Khaper N, Ross GM, Tai TC. 2010. Protective effects of polyphenolic compounds on oxidative stress-induced cytotoxicity in PC12 cells. Can. J. Physiol. Pharmacol. 88: 429-438.
    Pubmed CrossRef
  35. Costa LG, Garrick JM, Roquè PJ, Pellacani C. 2016. Mechanisms of neuroprotection by quercetin: counteracting oxidative stress and more. Oxid. Med. Cell. Longev. 2016:2986796.
    Pubmed KoreaMed CrossRef
  36. Kumar ADN, Bevara GB, Kaja LK, Badana AK, Malla RR. 2016. Protective effect of 3-O-methyl quercetin and kaempferol from Semecarpus anacardium against H2O2 induced cytotoxicity in lung and liver cells. BMC Complement. Altern. Med. 16: 376.
    Pubmed KoreaMed CrossRef
  37. Sepand MR, Ghahremani MH, Razavi-Azarkhiavi K, Aghsami M, Rajabi J, Keshavarz-Bahaghighat H, et al. 2016. Ellagic acid confers protection against gentamicin-induced oxidative damage, mitochondrial dysfunction and apoptosisrelated nephrotoxicity. J. Pharm. Pharmacol. 68: 1222-1232.
    Pubmed CrossRef
  38. Hong S-Y, Jeong W-S, Jun M. 2012. Protective effects of the key compounds isolated from Corni fructus against β-amyloidinduced neurotoxicity in PC12 cells. Molecules 17: 10831-10845.
    Pubmed CrossRef
  39. Kang MK, Kang NJ, Jang YJ, Lee KW, Lee HJ. 2009. Gallic acid induces neuronal cell death through activation of c-Jun N-terminal kinase and downregulation of Bcl-2. Ann. N. Y. Acad. Sci. 1171: 514-520.
    Pubmed CrossRef