Biomolecules & Therapeutics

  • 제27권4호
  • /
  • Pages.395-403
  • /
  • 2019
  • /
  • 1976-9148(pISSN)
  • /
  • 2005-4483(eISSN)
한국응용약물학회 (The Korean Society of Applied Pharmacology)
권호 표지
DOI QR코드

DOI QR Code

Purpurogallin Protects Keratinocytes from Damage and Apoptosis Induced by Ultraviolet B Radiation and Particulate Matter 2.5

  • Zhen, Ao Xuan (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Piao, Mei Jing (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Hyun, Yu Jae (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Kang, Kyoung Ah (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Ryu, Yea Seong (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Cho, Suk Ju (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Kang, Hee Kyoung (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Koh, Young Sang (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine) ;
  • Ahn, Mee Jung (Laboratory of Veterinary Anatomy, College of Veterinary Medicine, Jeju National University) ;
  • Kim, Tae Hoon (Department of Food Science and Biotechnology, Daegu University) ;
  • Hyun, Jin Won (Jeju National University School of Medicine and Jeju Research Center for Natural Medicine)
  • 투고 : 2018.08.07
  • 심사 : 2018.10.06
  • 발행 : 2019.07.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Purpurogallin, a natural phenol obtained from oak nutgalls, has been shown to possess antioxidant, anticancer, and anti-inflammatory effects. Recently, in addition to ultraviolet B (UVB) radiation that induces cell apoptosis via oxidative stress, particulate matter 2.5 ($PM_{2.5}$) was shown to trigger excessive production of reactive oxygen species. In this study, we observed that UVB radiation and $PM_{2.5}$ severely damaged human HaCaT keratinocytes, disrupting cellular DNA, lipids, and proteins and causing mitochondrial depolarization. Purpurogallin protected HaCaT cells from apoptosis induced by UVB radiation and/or $PM_{2.5}$. Furthermore, purpurogallin effectively modulates the pro-apoptotic and anti-apoptotic proteins under UVB irradiation via caspase signaling pathways. Additionally, purpurogallin reduced apoptosis via MAPK signaling pathways, as demonstrated using MAPK-p38, ERK, and JNK inhibitors. These results indicate that purpurogallin possesses antioxidant effects and protects cells from damage and apoptosis induced by UVB radiation and $PM_{2.5}$.

키워드

참고문헌

  1. Agar, N. S., Halliday, G. M., Barnetson, R. S., Ananthaswamy, H. N., Wheeler, M. and Jones, A. M. (2004) The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 4954-4959. https://doi.org/10.1073/pnas.0401141101
  2. Boakye, C. H. A., Patel, K., Doddapaneni, R., Bagde, A., Behl, G., Chowdhury, N., Safe, S. and Singh, M. (2016) Ultra-flexible nanocarriers for enhanced topical delivery of a highly lipophilic antioxidative molecule for skin cancer chemoprevention. Colloids Surf. B Biointerfaces 143, 156-167. https://doi.org/10.1016/j.colsurfb.2016.03.036
  3. Brentnall, M., Rodriguez-Menocal, L., De Guevara, R. L., Cepero, E. and Boise, L. H. (2013) Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol. 14, 32. https://doi.org/10.1186/1471-2121-14-32
  4. Cao, J., Qin, G., Shi, R., Bai, F., Yang, G., Zhang, M. and Lv, J. (2016) Overproduction of reactive oxygen species and activation of MAPKs are involved in apoptosis induced by $PM_{2.5}$ in rat cardiac H9c2 cells. J. Appl. Toxicol. 36, 609-617. https://doi.org/10.1002/jat.3249
  5. Castaneda, A. R., Pinkerton, K. E., Bein, K. J., Magana-Mendez, A., Yang, H. T., Ashwood, P. and Vogel, C. F. A. (2018) Ambient particulate matter activates the aryl hydrocarbon receptor in dendritic cells and enhances Th17 polarization. Toxicol. Lett. 292, 85-96. https://doi.org/10.1016/j.toxlet.2018.04.020
  6. Cha, J. W., Piao, M. J., Kim, K. C., Yao, C. W., Zheng, J., Kim, S. M., Hyun, C. L., Ahn, Y. S. and Hyun, J. W. (2014) The polyphenol chlorogenic acid attenuates UVB-mediated oxidative stress in human HaCaT keratinocytes. Biomol. Ther. (Seoul) 22, 136-142. https://doi.org/10.4062/biomolther.2014.006
  7. Chang, C. Z., Lin, C. L., Wu, S. C. and Kwan, A. L. (2014) Purpurogallin, a natural phenol, attenuates high-mobility group box 1 in subarachnoid hemorrhage induced vasospasm in a rat model. Int. J. Vasc. Med. 2014, 254270.
  8. De Chiara, G., Marcocci, M. E., Torcia, M., Lucibello, M., Rosini, P., Bonini, P., Higashimoto, Y., Damonte, G., Armirotti, A., Amodei, S., Palamara, A. T., Russo, T., Garaci, E. and Cozzolino, F. (2006) Bcl-2 phosphorylation by p38 MAPK: identification of target sites and biologic consequences. J. Biol. Chem. 281, 21353-21361. https://doi.org/10.1074/jbc.M511052200
  9. Dlugosz, P. J., Billen, L. P., Annis, M. G., Zhu, W., Zhang, Z., Lin, J., Leber, B. and Andrews, D. W. (2006) Bcl-2 changes conformation to inhibit Bax oligomerization. EMBO J. 25, 2287-2296. https://doi.org/10.1038/sj.emboj.7601126
  10. Faggio, C., Sureda, A., Morabito, S., Sanches-Silva, A., Mocan, A., Nabavi, S. F. and Nabavi, S. M. (2017) Flavonoids and platelet aggregation: A brief review. Eur. J. Pharmacol. 807, 91-101. https://doi.org/10.1016/j.ejphar.2017.04.009
  11. Feehan, R. P. and Shantz, L. M. (2016) Molecular signaling cascades involved in nonmelanoma skin carcinogenesis. Biochem. J. 473, 2973-2994. https://doi.org/10.1042/BCJ20160471
  12. Fernando, P. M., Piao, M. J., Kang, K. A., Ryu, Y.S., Hewage, S. R., Chae, S. W. and Hyun, J. W. (2016) Rosmarinic acid attenuates cell damage against UVB radiation-induced oxidative stress via enhancing antioxidant effects in human HaCaT cells. Biomol. Ther. (Seoul) 24, 75-84. https://doi.org/10.4062/biomolther.2015.069
  13. Fulda, S. and Debatin, K. M. (2006) Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25, 4798-4811. https://doi.org/10.1038/sj.onc.1209608
  14. Glady, A., Tanaka, M., Moniaga, C. S., Yasui, M. and Hara-Chikuma, M. (2018) Involvement of NADPH oxidase 1 in UVB-induced cell signaling and cytotoxicity in human keratinocytes. Biochem. Biophys. Rep. 14, 7-15. https://doi.org/10.1016/j.bbrep.2018.03.004
  15. He, M., Ichinose, T., Yoshida, S., Shiba, F., Arashidani, K., Takano, H., Sun, G. and Shibamoto, T. (2016) Differences in allergic inflammatory responses in murine lungs: comparison of $PM_{2.5}$ and coarse PM collected during the hazy events in a Chinese city. Inhal. Toxicol. 28, 706-718. https://doi.org/10.1080/08958378.2016.1260185
  16. Hosseini, M., Dousset, L., Mahfouf, W., Serrano-Sanchez, M., Redonnet-Vernhet, I., Mesli, S., Kasraian, Z., Obre, E., Bonneu, M., Claverol, S., Vlaski, M., Ivanovic, Z., Rachidi, W., Douki, T., Taieb, A., Bouzier-Sore, A. K., Rossignol, R. and Rezvani, H. R. (2018) Energy metabolism rewiring precedes UVB-induced primary skin tumor formation. Cell Rep. 23, 3621-3634. https://doi.org/10.1016/j.celrep.2018.05.060
  17. Kang, C. H., Rhie, S. J. and Kim, Y. C. (2018) Antioxidant and skin antiaging effects of marigold methanol extract. Toxicol. Res. 34, 31-39. https://doi.org/10.5487/TR.2018.34.1.031
  18. Kim, B. J., Ryu, S. W. and Song, B. J. (2006) JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J. Biol. Chem. 281, 21256-21265. https://doi.org/10.1074/jbc.M510644200
  19. Kim, K., Kim, T. H., Ihn, H. J., Kim, J. E., Choi, J. Y., Shin, H. I. and Park, E. K. (2018) Inhibitory effect of Purpurogallin on osteoclast differentiation in vitro through the downregulation of c-Fos and NFATc1. Int. J. Mol. Sci. 19, E601. https://doi.org/10.3390/ijms19020601
  20. Kong, L., Wang, S., Wu, X., Zuo, F., Qin, H. and Wu, J. (2016) Paeoniflorin attenuates ultraviolet B-induced apoptosis in human keratinocytes by inhibiting the ROS-p38-p53 pathway. Mol. Med. Rep. 13, 3553-3558. https://doi.org/10.3892/mmr.2016.4953
  21. Lee, S. J., Kim, M. S., Park, J. Y., Woo, J. S. and Kim, Y. K. (2008) 15-Deoxy-delta 12,14-prostaglandin J2 induces apoptosis via JNKmediated mitochondrial pathway in osteoblastic cells. Toxicology 248, 121-129. https://doi.org/10.1016/j.tox.2008.03.014
  22. Liu, Q., Xu, C., Ji, G. X., Liu, H., Shao, W., Zhang, C., Gu, A. and Zhao, P. (2017) Effect of exposure to ambient $PM_{2.5}$ pollution on the risk of respiratory tract diseases: a meta-analysis of cohort studies. J. Biomed. Res. 31, 130-142.
  23. Nohynek, G. J. and Schaefer, H. (2001) Benefit and risk of organic ultraviolet filters. Regul. Toxicol. Pharmacol. 33, 285-299. https://doi.org/10.1006/rtph.2001.1476
  24. Oh, M. C., Piao, M. J., Fernando, P. M., Han, X., Madduma Hewage, S. R., Park, J. E., Ko, M.S., Jung, U., Kim, I. G. and Hyun, J. W. (2016) Baicalein protects human skin cells against ultraviolet B-induced oxidative stress. Biomol. Ther. (Seoul) 24, 616-622. https://doi.org/10.4062/biomolther.2016.022
  25. Park, H. Y., Kim, T. H., Kim, C. G., Kim, G. Y., Kim, C. M., Kim, N. D., Kim, B. W., Hwang, H. J. and Choi, Y. H. (2013) Purpurogallin exerts anti-inflammatory effects in lipopolysaccharide-stimulated BV2 microglial cells through the inactivation of the NF-${\kappa}$B and MAPK signaling pathways. Int. J. Mol. Med. 32, 1171-1178. https://doi.org/10.3892/ijmm.2013.1478
  26. Piao, M. J., Ahn, M. J., Kang, K. A., Ryu, Y. S., Hyun, Y. J., Shilnikova, K., Zhen, A. X., Jeong, J. W., Choi, Y. H., Kang, H. K., Koh, Y. S. and Hyun, J. W. (2018) Particulate matter 2.5 damages skin cells by inducing oxidative stress, subcellular organelle dysfunction, and apoptosis. Arch. Toxicol. 92, 2077-2091. https://doi.org/10.1007/s00204-018-2197-9
  27. Prasad, K. and Laxdal, V. A. (1994) Evaluation of hydroxyl radicalscavenging property of purpurogallin using high pressure liquid chromatography. Mol. Cell Biochem. 135, 153-158. https://doi.org/10.1007/BF00926518
  28. Rajawat, J., Shukla, N. and Mishra, D. P. (2017) Therapeutic targeting of poly(ADP-Ribose) polymerase-1 (PARP1) in cancer: current developments, therapeutic strategies, and future opportunities. Med. Res. Rev. 37, 1461-1491. https://doi.org/10.1002/med.21442
  29. Reed, J. C. (2006) Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities. Cell Death Differ. 13, 1378-1386. https://doi.org/10.1038/sj.cdd.4401975
  30. Wang, Y., Xiong, L. and Tang, M. (2017) Toxicity of inhaled particulate matter on the central nervous system: neuroinflammation, neuropsychological effects and neurodegenerative disease. J. Appl. Toxicol. 37, 644-667. https://doi.org/10.1002/jat.3451
  31. Wu, T. W., Zeng, L. H., Wu, J., Fung, K. P., Weisel, R. D., Hempel, A. and Camerman, N. (1996) Molecular structure and antioxidant specificity of purpurogallin in three types of human cardiovascular cells. Biochem. Pharmacol. 52, 1073-1080. https://doi.org/10.1016/0006-2952(96)00447-9
  32. Würstle, M. L., Laussmann, M. A. and Rehm, M. (2012) The central role of initiator caspase-9 in apoptosis signal transduction and the regulation of its activation and activity on the apoptosome. Exp. Cell Res. 318, 1213-1220. https://doi.org/10.1016/j.yexcr.2012.02.013
  33. Yin, Q., Park, H. H., Chung, J. Y., Lin, S. C., Lo, Y. C., da Graca, L.S., Jiang, X. and Wu, H. (2006) Caspase-9 holoenzyme is a specific and optimal procaspase-3 processing machine. Mol. Cell 22, 259-268. https://doi.org/10.1016/j.molcel.2006.03.030
  34. Zeng, L. H. and Wu, T. W. (1992) Purpurogallin is a more powerful protector of kidney cells than Trolox and allopurinol. Biochem. Cell Biol. 70, 684-690. https://doi.org/10.1139/o92-104
  35. Zheng, J., Piao, M. J., Kim, K. C., Yao, C. W., Cha, J. W., Shin, J. H., Yoo, S. J. and Hyun, J. W. (2014) Photo-protective effect of americanin B against ultraviolet B-induced damage in cultured human keratinocytes. Environ. Toxicol. Pharmacol. 38, 891-900. https://doi.org/10.1016/j.etap.2014.08.017
  36. Zheng, W., Wang, B., Si, M., Zou, H., Song, R., Gu, J., Yuan, Y., Liu, X., Zhu, G., Bai, J., Bian, J. and Liu, Z. (2018) Zearalenone altered the cytoskeletal structure via ER stress- autophagy- oxidative stress pathway in mouse TM4 Sertoli cells. Sci. Rep. 8, 3320. https://doi.org/10.1038/s41598-018-21567-8

피인용 문헌

  1. Eckol Inhibits Particulate Matter 2.5-Induced Skin Keratinocyte Damage via MAPK Signaling Pathway vol.17, pp.8, 2019, https://doi.org/10.3390/md17080444
  2. Niacinamide Protects Skin Cells from Oxidative Stress Induced by Particulate Matter vol.27, pp.6, 2019, https://doi.org/10.4062/biomolther.2019.061