DOI QR코드

DOI QR Code

6'-O-Galloylpaeoniflorin Protects Human Keratinocytes Against Oxidative Stress-Induced Cell Damage

  • Yao, Cheng Wen (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Piao, Mei Jing (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Kim, Ki Cheon (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Zheng, Jian (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Cha, Ji Won (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Hyun, Jin Won (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University)
  • Received : 2013.08.29
  • Accepted : 2013.09.24
  • Published : 2013.09.30

Abstract

6'-O-galloylpaeoniflorin (GPF) is a galloylated derivate of paeoniflorin and a key chemical constituent of the peony root, a perennial flowering plant that is widely used as an herbal medicine in East Asia. This study is the first investigation of the cytoprotective effects of GPF against hydrogen peroxide ($H_2O_2$)-induced cell injury and death in human HaCaT keratinocytes. GPF demonstrated a significant scavenging capacity against the 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radical, $H_2O_2$-generated intracellular reactive oxygen species (ROS), the superoxide anion radical ($O_2^-$), and the hydroxyl radical (${\cdot}$OH). GPF also safeguarded HaCaT keratinocytes against $H_2O_2$-provoked apoptotic cell death and attenuated oxidative macromolecular damage to DNA, lipids, and proteins. The compound exerted its cytoprotective actions in keratinocytes at least in part by decreasing the number of DNA strand breaks, the levels of 8-isoprostane (a stable end-product of lipid peroxidation), and the formation of carbonylated protein species. Taken together, these results indicate that GPF may be developed as a cytoprotector against ROS-mediated oxidative stress.

Keywords

References

  1. Alfadda, A. A. and Sallam, R. M. (2012) Reactive oxygen species in health and disease. J. Biomed. Biotechnol. 2012, 936486.
  2. Antunes, F. and Cadenas, E. (2001) Cellular titration of apoptosis with steady state concentrations of $H_2O_2$: submicromolar levels of $H_2O_2$ induce apoptosis through Fenton chemistry independent of the cellular thiol state. Free Radic. Biol. Med. 30, 1008-1018. https://doi.org/10.1016/S0891-5849(01)00493-2
  3. Beauchamp, M. C., Letendre, E. and Renier, G. (2002) Macrophage lipoprotein lipase expression is increased in patients with heterozygous familial hypercholesterolemia. J. Lipid Res. 43, 215-222.
  4. Bickers, D. R. and Athar, M. (2006) Oxidative stress in the pathogenesis of skin disease. J. Invest. Dermatol. 126, 2565-2575. https://doi.org/10.1038/sj.jid.5700340
  5. Brambilla, D., Mancuso, C., Scuderi, M. R., Bosco, P., Cantarella, G., Lempereur, L., Di Benedetto, G., Pezzino, S. and Bernardini, R. (2008) The role of antioxidant supplement in immune system, neoplastic, and neurodegenerative disorders: a point of view for an assessment of the risk/benefit profile. Nutr. J. 7, 29 https://doi.org/10.1186/1475-2891-7-29
  6. Cai, H. (2005) Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc. Res. 68, 26-36. https://doi.org/10.1016/j.cardiores.2005.06.021
  7. Carmichael, J., DeGraff, W. G., Gazdar, A. F., Minna, J. D. and Mitchell, J. B. (1987) Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 47, 936-942.
  8. Carter, W., Narayanan, P. K. and Robinson, J. (1994) Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J. Leukoc. Biol. 55, 253-258. https://doi.org/10.1002/jlb.55.2.253
  9. Chandra, J., Samali, A. and Orrenius, S. (2000) Triggering and modulation of apoptosis by oxidative stress. Free Radic. Biol. Med. 29, 323-333. https://doi.org/10.1016/S0891-5849(00)00302-6
  10. Dalle-Donne, I., Rossi, R., Giustarini, D., Milzani, A. and Colombo, R. (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin. Chim. Acta 329, 23-38. https://doi.org/10.1016/S0009-8981(03)00003-2
  11. Farber, J. L. (1994) Mechanisms of cell injury by activated oxygen species. Environ. Health Perspect. 102, 17-24. https://doi.org/10.1289/ehp.94102s1017
  12. Gutteridge, J. (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin. Chem. 41, 1819-1828.
  13. Haigis, M. C. and Yankner, B. A. (2010) The aging stress response. Mol. Cell 40, 333-344. https://doi.org/10.1016/j.molcel.2010.10.002
  14. Halliwell, B. (1999) Oxygen and nitrogen are pro-carcinogens. Damage to DNA by reactive oxygen, chlorine and nitrogen species: measurement, mechanism and the effects of nutrition. Mutat. Res. 443, 37-52. https://doi.org/10.1016/S1383-5742(99)00009-5
  15. Halliwell, B. (2007) Oxidative stress and cancer: have we moved forward? Biochem. J. 401, 1-11. https://doi.org/10.1042/BJ20061131
  16. Hampton, M. B. and Orrenius, S. (1998) Redox regulation of apoptotic cell death. BioFactors 8, 1-5. https://doi.org/10.1002/biof.5520080101
  17. Hoffmann, M. E., Mello-Filho, A. C. and Meneghini, R. (1984) Correlation between cytotoxic effect of hydrogen peroxide and the yield of DNA strand breaks in cells of different species. Biochim. Biophys. Acta 781, 234-238. https://doi.org/10.1016/0167-4781(84)90088-5
  18. Horvathova, E., Slamenova, D., Hlincikova, L., Mandal, T. K., Gabelova, A. and Collins, A. R. (1998) The nature and origin of DNA single-strand breaks determined with the comet assay. Mutat. Res. 409, 163-171. https://doi.org/10.1016/S0921-8777(98)00053-6
  19. Kang, S. S., Shin, K. H. and Chi, H. J. (1991) Galloylpaeoniflorin, a new acylated monoterpene glucoside from paeony root. Arch. Pharm. Res. 14, 52-54. https://doi.org/10.1007/BF02857815
  20. Kerksick, C. and Willoughby, D. (2005) The antioxidant role of glutathione and N-acetyl-cysteine supplements and exercise-induced oxidative stress. J. Int. Soc. Sports Nutr. 2, 38-44. https://doi.org/10.1186/1550-2783-2-2-38
  21. Kohno, M., Mizuta, Y., Kusai, M., Masumizu, T. and Makino, K. (1994) Measurements of superoxide anion radical and superoxide anion scavenging activity by electron spin resonance spectroscopy coupled with DMPO spin trapping. Bull. Chem. Soc. Jpn. 67, 1085-1090. https://doi.org/10.1246/bcsj.67.1085
  22. Lee, S. C., Kwon, Y. S., Son, K. H., Kim, H. P. and Heo, M. Y. (2005) Antioxidative constituents from Paeonia lactiflora. Arch. Pharm. Res. 28, 775-783. https://doi.org/10.1007/BF02977342
  23. Li, C. R., Zhou, Z., Zhu, D., Sun, Y. N., Dai, J. M. and Wang, S. Q. (2007) Protective effect of paeoniflorin on irradiation-induced cell damage involved in modulation of reactive oxygen species and the mitogen-activated protein kinases. Int. J. Biochem. Cell Biol. 39, 426-438. https://doi.org/10.1016/j.biocel.2006.09.011
  24. Li, L., Abe, Y., Kanagawa, K., Usui, N., Imai, K., Mashino, T., Mochizuki, M. and Miyata, N. (2004) Distinguishing the 5,5-dimethyl-1-pyrroline N-oxide (DMPO)-OH radical quenching effect from the hydroxyl radical scavenging effect in the ESR spin-trapping method. Anal. Chim. Acta 512, 121-124. https://doi.org/10.1016/j.aca.2004.02.020
  25. Liu, B., Jian, Z., Li, Q., Li, K., Wang, Z., Liu, L., Tang, L., Yi, X., Wang, H., Li, C. and Gao, T. (2012) Baicalein protects human melanocytes from H2O2-induced apoptosis via inhibiting mitochondria-dependent caspase activation and the p38 MAPK pathway. Free Radic. Biol. Med. 53, 183-193. https://doi.org/10.1016/j.freeradbiomed.2012.04.015
  26. Maioli, E., Greci, L., Soucek, K., Hyzdalova, M., Pecorelli, A., Fortino, V. and Valacchi, G. (2009) Rottlerin inhibits ROS formation and prevents $NF{\kappa}B$ activation in MCF-7 and HT-29 cells. J. Biomed. Biotechnol. 2009, 742936.
  27. Matsuda, H., Ohta, T., Kawaguchi, A. and Yoshikawa, M. (2001) Bioactive constituents of chinese natural medicines. VI. Moutan cortex. (2): structures and radical scavenging effects of suffruticosides A, B, C, D, and E and galloyl-oxypaeoniflorin. Chem. Pharm. Bull. 49, 69-72. https://doi.org/10.1248/cpb.49.69
  28. Meyers, D. G., Maloley, P. A. and Weeks, D. (1996) Safety of antioxidant vitamins. Arch. Intern. Med. 156, 925-935. https://doi.org/10.1001/archinte.1996.00440090015002
  29. Morrow, J. D., Frei, B., Longmire, A. W., Gaziano, J. M., Lynch, S. M., Shyr, Y., Strauss, W. E., Oates, J. A. and Roberts, L. J. (1995) Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers-smoking as a cause of oxidative damage. N. Engl. J. Med. 332, 1198-1203. https://doi.org/10.1056/NEJM199505043321804
  30. Motterlini, R., Foresti, R., Bassi, R. and Green, C. J. (2000) Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Radic. Biol. Med. 28, 1303-1312. https://doi.org/10.1016/S0891-5849(00)00294-X
  31. Nguyen, C. N., Kim, H. E. and Lee, S. G. (2013) Caffeoylserotonin protects human keratinocyte HaCaT cells against $H_2O_2$-induced oxidative stress and apoptosis through upregulation of HO-1 expression via activation of the PI3K/Akt/Nrf2 pathway. Phytother. Res. doi:10.1002/ptr.4931. [Epub ahead of print]
  32. Okimotoa, Y., Watanabe, A., Niki, E., Yamashita, T. and Noguchi, N. (2000) A novel fluorescent probe diphenyl-1-pyrenylphosphine to follow lipid peroxidation in cell membranes. FEBS Lett. 474, 137-140. https://doi.org/10.1016/S0014-5793(00)01587-8
  33. Paravicini, T. M. and Touyz, R. M. (2006) Redox signaling in hypertension. Cardiovasc. Res. 71, 247-258. https://doi.org/10.1016/j.cardiores.2006.05.001
  34. Patel, V. P. and Chu, C. T. (2011) Nuclear transport, oxidative stress, and neurodegeneration. Int. J. Clin. Exp. Pathol. 4, 215-229.
  35. Pignatello, J. J., Oliveros, E. and MacKay, A. (2006) Advanced oxidation processes for organic contaminant destruction based on the Fenton reaction and related chemistry. Crit. Rev. Environ. Sci. Technol. 36, 1-84. https://doi.org/10.1080/10643380500326564
  36. Poljsak, B. (2011) Strategies for reducing or preventing the generation of oxidative stress. Oxid. Med. Cell. Longev. 2011, 194586.
  37. Pryor, W. A. (2000) Vitamin E and heart disease: Basic science to clinical intervention trials. Free Radic. Biol. Med. 28, 141-164. https://doi.org/10.1016/S0891-5849(99)00224-5
  38. Rajagopalan, R., Ranjan, S. K. and Nair, C. K. K. (2003) Effect of vinblastine sulfate on ${\gamma}$-radiation-induced DNA single-strand breaks in murine tissues. Mutat. Res. 536, 15-25. https://doi.org/10.1016/S1383-5718(03)00015-9
  39. Ray, P. D., Huang, B. W. and Tsuji, Y. (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 24, 981-990. https://doi.org/10.1016/j.cellsig.2012.01.008
  40. Rosenkranz, A. R., Schmaldienst, S., Stuhlmeier, K. M., Chen, W., Knapp, W. and Zlabinger, G. J. (1992) A microplate assay for the detection of oxidative products using 2, 7′-dichlorofluorescin-diacetate. J. Immunol. Methods 156, 39-45. https://doi.org/10.1016/0022-1759(92)90008-H
  41. Scandalios, J. G. (2002) The rise of ROS. Trends Biochem. Sci. 27, 483-486. https://doi.org/10.1016/S0968-0004(02)02170-9
  42. Shacter, E. (2000) Quantification and significance of protein oxidation in biological samples. Drug Metab. Rev. 32, 307-326. https://doi.org/10.1081/DMR-100102336
  43. Singh, N. P. (2000) Microgels for estimation of DNA strand breaks, DNA protein crosslinks and apoptosis. Mutat. Res. 455, 111-127. https://doi.org/10.1016/S0027-5107(00)00075-0
  44. Srivastava, A., Jagan Mohan Rao, L. and Shivanandappa, T. (2012) A novel cytoprotective antioxidant: 4-Hydroxyisophthalic acid. Food Chem. 132, 1959-1965. https://doi.org/10.1016/j.foodchem.2011.12.032
  45. Wankun, X., Wenzhen, Y., Min, Z., Weiyan, Z., Huan, C., Wei, D., Lvzhen, H., Xu, Y. and Xiaoxin, L. (2011) Protective effect of paeoniflorin against oxidative stress in human retinal pigment epithelium in vitro. Mol. Vis. 17, 3512-3522.
  46. Waris, G. and Ahsan, H. (2006) Reactive oxygen species: role in the development of cancer and various chronic conditions. J. Carcinog. 5, 14. https://doi.org/10.1186/1477-3163-5-14
  47. Witting, P. K., Rayner, B. S., Wu, B.J., Ellis, N. A. and Stocker, R. (2008) Hydrogen peroxide promotes endothelial dysfunction by stimulating multiple sources of superoxide anion radical production and decreasing nitric oxide bioavailability. Cell. Physiol. Biochem. 20, 255-268.
  48. Wyllie, A., Morris, R., Smith, A. and Dunlop, D. (1984) Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142, 67-77. https://doi.org/10.1002/path.1711420112

Cited by

  1. Cytoprotective effects of 6′-O-galloylpaeoniflorin against ultraviolet B radiation-induced cell damage in human keratinocytes vol.50, pp.7, 2014, https://doi.org/10.1007/s11626-014-9747-0
  2. The skin-depigmenting potential of Paeonia lactiflora root extract and paeoniflorin:in vitroevaluation using reconstructed pigmented human epidermis vol.38, pp.5, 2016, https://doi.org/10.1111/ics.12309
  3. Chemical Components and Pharmacological Activities of Terpene Natural Products from the Genus Paeonia vol.21, pp.10, 2016, https://doi.org/10.3390/molecules21101362
  4. The study of inducing apoptosis effect of fructose 1,6-bisphosphate on the papillary thyroid carcinoma cell and its related mechanism vol.35, pp.5, 2014, https://doi.org/10.1007/s13277-013-1597-y
  5. Vitamin C attenuates the toxic effect of aristolochic acid on renal tubular cells via decreasing oxidative stress-mediated cell death pathways vol.12, pp.4, 2015, https://doi.org/10.3892/mmr.2015.4167
  6. Origins, Phytochemistry, Pharmacology, Analytical Methods and Safety of Cortex Moutan (Paeonia suffruticosa Andrew): A Systematic Review vol.22, pp.6, 2017, https://doi.org/10.3390/molecules22060946
  7. -Galloylpaeoniflorin Attenuates Cerebral Ischemia Reperfusion-Induced Neuroinflammation and Oxidative Stress via PI3K/Akt/Nrf2 Activation vol.2018, pp.1942-0994, 2018, https://doi.org/10.1155/2018/8678267
  8. Vitamin E (α-tocopherol) ameliorates aristolochic acid-induced renal tubular epithelial cell death by attenuating oxidative stress and caspase-3 activation vol.17, pp.1, 2013, https://doi.org/10.3892/mmr.2017.7921
  9. Cell Chromatography-Based Screening of the Active Components in Buyang Huanwu Decoction Promoting Axonal Regeneration vol.2019, pp.None, 2013, https://doi.org/10.1155/2019/6970198
  10. 6′-O-galloylpaeoniflorin regulates proliferation and metastasis of non-small cell lung cancer through AMPK/miR-299-5p/ATF2 axis vol.21, pp.1, 2013, https://doi.org/10.1186/s12931-020-1277-6
  11. Insight into Seasonal Change of Phytochemicals, Antioxidant, and Anti-Aging Activities of Root Bark of Paeonia suffruticosa (Cortex Moutan) Combined with Multivariate Statistical Analysis vol.26, pp.20, 2013, https://doi.org/10.3390/molecules26206102