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Effect of Methyl Gallate on 1-Nitropyrene-Induced Keratinocyte Toxicity in a Human and Canine Skin Model

  • Lee, Woo Jin (School of Food Science and Biotechnology, Kyungpook National University) ;
  • Kim, Min Jeong (School of Food Science and Biotechnology, Kyungpook National University) ;
  • Choi, Hyun-Wook (Department of Functional Food and Biotechnology, Jeonju University) ;
  • Lee, Jeong Jae (Institute of Agricultural Science and Technology, Kyungpook National University) ;
  • Jung, Sung Keun (School of Food Science and Biotechnology, Kyungpook National University)
  • Received : 2022.06.07
  • Accepted : 2022.06.27
  • Published : 2022.07.28

Abstract

The skin, which is the largest organ of the human body, is in direct contact with pollutants in the surrounding atmosphere. Meanwhile, 1-nitropyrene (1-NP), the most abundant nitro-polycyclic aromatic hydrocarbon found in particulate matter, is known to have carcinogenic effects; however, studies on its toxicity in human and canine skin are still needed. In this study, we investigated 1-NP-induced apoptosis and inflammatory pathways in HaCaT cells. In addition, we also measured the cytoprotective effect of methyl gallate (MG), which is widely distributed in medicinal and edible plants and is well known for its anti-inflammatory and antioxidant properties. MG inhibited 1-NP-induced cell death and apoptosis pathways, including the cleavage of PARP and activation of caspase-3, -7, and -9. MG also suppressed 1-NP-induced COX-2 expression and phosphorylation of mitogen-activated protein kinases (MAPKs) and MAPK kinases (MAPKKs). Our findings suggest that 1-NP induces skin toxicity in human and canine through apoptosis and inflammatory responses, and moreover, that this can be prevented by treatment with MG.

Keywords

Acknowledgement

This project was supported by the Ministry of Oceans and Fisheries of Korea (No.20210386), and by the National Research Foundation of Korea grant funded by the Korean government (NRF-2021M3E5E6022715, NRF-2021R1F1A1062889).

References

  1. Roberts W. 2021. Air pollution and skin disorders. Int. J. Women's Dermatol. 7: 91-97. https://doi.org/10.1016/j.ijwd.2020.11.001
  2. Hensel P. 2010. Nutrition and skin diseases in veterinary medicine. Clin. Dermatol. 28: 686-693. https://doi.org/10.1016/j.clindermatol.2010.03.031
  3. Lehtimaki J, Sinkko H, Hielm-Bjorkman A, Laatikainen T, Ruokolainen L, Lohi H. 2020. Simultaneous allergic traits in dogs and their owners are associated with living environment, lifestyle and microbial exposures. Sci. Rep. 10: 21954.
  4. Piao MJ, Ahn MJ, Kang KA, Ryu YS, Hyun YJ, Shilnikova K, et al. 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
  5. Krutmann J, Liu W, Li L, Pan X, Crawford M, Sore G, et al. 2014. Pollution and skin: from epidemiological and mechanistic studies to clinical implications. J. Dermatol. Sci. 76: 163-168. https://doi.org/10.1016/j.jdermsci.2014.08.008
  6. Wang B, Xu S, Lu X, Ma L, Gao L, Zhang SY, et al. 2020. Reactive oxygen species-mediated cellular genotoxic stress is involved in 1-nitropyrene-induced trophoblast cycle arrest and fetal growth restriction. Environ. Pollut. 260: 113984.
  7. de Mejia EG, Ramirez-Mares MV. 2002. Leaf extract from Ardisia compressa protects against 1-nitropyrene-induced cytotoxicity and its antioxidant defense disruption in cultured rat hepatocytes. Toxicology 179: 151-162. https://doi.org/10.1016/S0300-483X(02)00242-1
  8. Asahina R, Maeda S. 2017. A review of the roles of keratinocyte-derived cytokines and chemokines in the pathogenesis of atopic dermatitis in humans and dogs. Vet. Dermatol. 28: 16-e15.
  9. Marsella R, Olivry T, Carlotti D-N, Dermatitis ftITFoCA. 2011. Current evidence of skin barrier dysfunction in human and canine atopic dermatitis. Vet. Dermatol. 22: 239-248. https://doi.org/10.1111/j.1365-3164.2011.00967.x
  10. Banovic F, Dunston S, Linder KE, Rakich P, Olivry T. 2017. Apoptosis as a mechanism for keratinocyte death in canine toxic epidermal necrolysis. Vet. Pathol. 54: 249-253. https://doi.org/10.1177/0300985816666609
  11. Baumer W, Kietzmann M. 2007. Effects of cyclosporin A and cilomilast on activated canine, murine and human keratinocytes. Vet. Dermatol. 18: 107-114. https://doi.org/10.1111/j.1365-3164.2007.00576.x
  12. Teraki Y, Shiohara T. 1999. Apoptosis and the skin. Eur. J. Dermatol. 9: 413-425; quiz 426.
  13. Reefman E, Limburg PC, Kallenberg CG, Bijl M. 2005. Apoptosis in human skin: role in pathogenesis of various diseases and relevance for therapy. Ann. NY Acad. Sci. 1051: 52-63. https://doi.org/10.1196/annals.1361.046
  14. D'Arcy MS. 2019. Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol. Int. 43: 582-592. https://doi.org/10.1002/cbin.11137
  15. Dubois RN, Abramson SB, Crofford L, Gupta RA, Simon LS, Van De Putte LB, et al. 1998. Cyclooxygenase in biology and disease. FASEB J. 12: 1063-1073. https://doi.org/10.1096/fasebj.12.12.1063
  16. Zhang R, Li S. 2009. COX-2 as a novel target of CRF family peptides' participating in inflammation. Biochem. Biophys. Res. Commun. 382: 483-485. https://doi.org/10.1016/j.bbrc.2009.03.064
  17. Penning TD, Talley JJ, Bertenshaw SR, Carter JS, Collins PW, Docter S, et al. 1997. Synthesis and biological evaluation of the 1,5-diarylpyrazole class of cyclooxygenase-2 inhibitors: identification of 4-[5-(4-methylphenyl)-3-(trifluoromethyl)-1H-pyrazol-1-yl]benze nesulfonamide (SC-58635, celecoxib). J. Med. Chem. 40: 1347-1365. https://doi.org/10.1021/jm960803q
  18. Turini ME, DuBois RN. 2002. Cyclooxygenase-2: a therapeutic target. Ann. Rev. Med. 53: 35-57. https://doi.org/10.1146/annurev.med.53.082901.103952
  19. Wan MLY, Co VA, El-Nezami H. 2021. Dietary polyphenol impact on gut health and microbiota. Crit. Rev. Food Sci. Nutr. 61: 690-711. https://doi.org/10.1080/10408398.2020.1744512
  20. Myburgh KH. 2014. Polyphenol supplementation: benefits for exercise performance or oxidative stress? Sports Med. 44 Suppl 1: S57-70. https://doi.org/10.1007/s40279-014-0151-4
  21. Rahman N, Jeon M, Kim YS. 2016. Methyl gallate, a potent antioxidant inhibits mouse and human adipocyte differentiation and oxidative stress in adipocytes through impairment of mitotic clonal expansion. Biofactors 42: 716-726. https://doi.org/10.1002/biof.1310
  22. Anzoise ML, Basso AR, Del Mauro JS, Carranza A, Ordieres GL, Gorzalczany S. 2018. Potential usefulness of methyl gallate in the treatment of experimental colitis. Inflammopharmacology 26: 839-849. https://doi.org/10.1007/s10787-017-0412-6
  23. Schlickmann F, de Souza P, Boeing T, Mariano LNB, Steimbach VMB, Krueger CMA, et al. 2017. Chemical composition and diuretic, natriuretic and kaliuretic effects of extracts of Mimosa bimucronata (DC.) Kuntze leaves and its majority constituent methyl gallate in rats. J. Pharm. Pharmacol. 69: 1615-1624. https://doi.org/10.1111/jphp.12785
  24. Park DJ, Jung HJ, Park CH, Yokozawa T, Jeong JC. 2019. Root bark of paeonia suffruticosa extract and its component methyl gallate possess peroxynitrite scavenging activity and anti-inflammatory properties through NF-kappaB inhibition in LPS-treated mice. Molecules 24: 3483.
  25. Hsieh TJ, Liu TZ, Chia YC, Chern CL, Lu FJ, Chuang MC, et al. 2004. Protective effect of methyl gallate from Toona sinensis (Meliaceae) against hydrogen peroxide-induced oxidative stress and DNA damage in MDCK cells. Food Chem. Toxicol. 42: 843-850. https://doi.org/10.1016/j.fct.2004.01.008
  26. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC. 1994. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371: 346-347. https://doi.org/10.1038/371346a0
  27. Mazumder S, Plesca D, Almasan A. 2008. Caspase-3 activation is a critical determinant of genotoxic stress-induced apoptosis. Methods Mol. Biol. 414: 13-21.
  28. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. 1998. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell. 1: 949-957. https://doi.org/10.1016/S1097-2765(00)80095-7
  29. Martinou J-C, Desagher S, Antonsson B. 2000. Cytochrome c release from mitochondria: all or nothing. Nat. Cell Biol. 2: E41-E43. https://doi.org/10.1038/35004069
  30. Prescott SL, Larcombe DL, Logan AC, West C, Burks W, Caraballo L, et al. 2017. The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming. World Allergy Organ J. 10: 29.
  31. Cashman JN. 1996. The mechanisms of action of NSAIDs in analgesia. Drugs 52 Suppl 5: 13-23. https://doi.org/10.2165/00003495-199600525-00004
  32. Tsatsanis C, Androulidaki A, Venihaki M, Margioris AN. 2006. Signalling networks regulating cyclooxygenase-2. Int. J. Biochem. Cell Biol. 38: 1654-1661. https://doi.org/10.1016/j.biocel.2006.03.021
  33. Cargnello M, Roux PP. 2011. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75: 50-83. https://doi.org/10.1128/MMBR.00031-10
  34. Orru H, Ebi KL, Forsberg B. 2017. The interplay of climate change and air pollution on health. Curr. Environ. Health Rep. 4: 504-513. https://doi.org/10.1007/s40572-017-0168-6
  35. Araviiskaia E, Berardesca E, Bieber T, Gontijo G, Sanchez Viera M, Marrot L, et al. 2019. The impact of airborne pollution on skin. J. Eur. Acad. Dermatol. Venereol. 33: 1496-1505. https://doi.org/10.1111/jdv.15583
  36. Oya E, Ovrevik J, Arlt VM, Nagy E, Phillips DH, Holme JA. 2011. DNA damage and DNA damage response in human bronchial epithelial BEAS-2B cells following exposure to 2-nitrobenzanthrone and 3-nitrobenzanthrone: role in apoptosis. Mutagenesis 26: 697-708. https://doi.org/10.1093/mutage/ger035
  37. Landvik NE, Gorria M, Arlt VM, Asare N, Solhaug A, Lagadic-Gossmann D, et al. 2007. Effects of nitrated-polycyclic aromatic hydrocarbons and diesel exhaust particle extracts on cell signalling related to apoptosis: possible implications for their mutagenic and carcinogenic effects. Toxicology 231: 159-174. https://doi.org/10.1016/j.tox.2006.12.009
  38. Toriba A, Kitaoka H, Dills RL, Mizukami S, Tanabe K, Takeuchi N, et al. 2007. Identification and quantification of 1-nitropyrene metabolites in human urine as a proposed biomarker for exposure to diesel exhaust. Chem. Res. Toxicol. 20: 999-1007. https://doi.org/10.1021/tx700015q
  39. Miller-Schulze JP, Paulsen M, Kameda T, Toriba A, Tang N, Tamura K, et al. 2013. Evaluation of urinary metabolites of 1-nitropyrene as biomarkers for exposure to diesel exhaust in taxi drivers of Shenyang, China. J. Exp. Sci. Environ. Epidemiol. 23: 170-175. https://doi.org/10.1038/jes.2012.40
  40. Laumbach R, Tong J, Zhang L, Ohman-Strickland P, Stern A, Fiedler N, et al. 2009. Quantification of 1-aminopyrene in human urine after a controlled exposure to diesel exhaust. J. Environ. Monit. 11: 153-159. https://doi.org/10.1039/B810039J
  41. Chen Q, Kang J, Fu C. 2018. The independence of and associations among apoptosis, autophagy, and necrosis. Signal Transduct. Target. Ther. 3: 18.
  42. Fischer U, Schulze-Osthoff K. 2005. New approaches and therapeutics targeting apoptosis in disease. Pharmacol. Rev. 57: 187-215. https://doi.org/10.1124/pr.57.2.6
  43. Wesierska-Gadek J, Gueorguieva M, Wojciechowski J, Tudzarova-Trajkovska S. 2004. In vivo activated caspase-3 cleaves PARP-1 in rat liver after administration of the hepatocarcinogen N-nitrosomorpholine (NNM) generating the 85 kDa fragment. J. Cell Biochem. 93: 774-787. https://doi.org/10.1002/jcb.20181
  44. Asare N, Landvik NE, Lagadic-Gossmann D, Rissel M, Tekpli X, Ask K, et al. 2008. 1-Nitropyrene (1-NP) induces apoptosis and apparently a non-apoptotic programmed cell death (paraptosis) in Hepa1c1c7 cells. Toxicol. Appl. Pharmacol. 230: 175-186. https://doi.org/10.1016/j.taap.2008.02.015
  45. Wu SW, Su CH, Ho YC, Huang-Liu R, Tseng CC, Chiang YW, et al. 2021. Genotoxic effects of 1-nitropyrene in macrophages are mediated through a p53-dependent pathway involving cytochrome c release, caspase activation, and PARP-1 cleavage. Ecotoxicol. Environ. Saf. 213: 112062.
  46. Rumzhum NN, Ammit AJ. 2016. Cyclooxygenase 2: its regulation, role and impact in airway inflammation. Clin. Exp. Allergy 46: 397-410. https://doi.org/10.1111/cea.12697
  47. Davies G, Martin LA, Sacks N, Dowsett M. 2002. Cyclooxygenase-2 (COX-2), aromatase and breast cancer: a possible role for COX2 inhibitors in breast cancer chemoprevention. Ann. Oncol. 13: 669-678. https://doi.org/10.1093/annonc/mdf125
  48. Derijard B, Raingeaud J, Barrett T, Wu IH, Han J, Ulevitch RJ, et al. 1995. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267: 682-685. https://doi.org/10.1126/science.7839144
  49. Yuan L, Wang J, Xiao H, Wu W, Wang Y, Liu X. 2013. MAPK signaling pathways regulate mitochondrial-mediated apoptosis induced by isoorientin in human hepatoblastoma cancer cells. Food Chem. Toxicol. 53: 62-68. https://doi.org/10.1016/j.fct.2012.11.048
  50. Huang P, Han J, Hui L. 2010. MAPK signaling in inflammation-associated cancer development. Protein Cell 1: 218-226. https://doi.org/10.1007/s13238-010-0019-9