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http://dx.doi.org/10.4014/jmb.2206.06004

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)
Publication Information
Journal of Microbiology and Biotechnology / v.32, no.7, 2022 , pp. 869-876 More about this Journal
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
Apoptosis; canine skin; HaCaT cells; methyl gallate; 1-nitropyrene; skin toxicity;
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1 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.   DOI
2 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.   DOI
3 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.   DOI
4 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.   DOI
5 Turini ME, DuBois RN. 2002. Cyclooxygenase-2: a therapeutic target. Ann. Rev. Med. 53: 35-57.   DOI
6 Myburgh KH. 2014. Polyphenol supplementation: benefits for exercise performance or oxidative stress? Sports Med. 44 Suppl 1: S57-70.   DOI
7 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.   DOI
8 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.   DOI
9 D'Arcy MS. 2019. Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol. Int. 43: 582-592.   DOI
10 Roberts W. 2021. Air pollution and skin disorders. Int. J. Women's Dermatol. 7: 91-97.   DOI
11 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.   DOI
12 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.   DOI
13 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.   DOI
14 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.   DOI
15 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.   DOI
16 Wan MLY, Co VA, El-Nezami H. 2021. Dietary polyphenol impact on gut health and microbiota. Crit. Rev. Food Sci. Nutr. 61: 690-711.   DOI
17 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.   DOI
18 Martinou J-C, Desagher S, Antonsson B. 2000. Cytochrome c release from mitochondria: all or nothing. Nat. Cell Biol. 2: E41-E43.   DOI
19 Cashman JN. 1996. The mechanisms of action of NSAIDs in analgesia. Drugs 52 Suppl 5: 13-23.   DOI
20 Tsatsanis C, Androulidaki A, Venihaki M, Margioris AN. 2006. Signalling networks regulating cyclooxygenase-2. Int. J. Biochem. Cell Biol. 38: 1654-1661.   DOI
21 Orru H, Ebi KL, Forsberg B. 2017. The interplay of climate change and air pollution on health. Curr. Environ. Health Rep. 4: 504-513.   DOI
22 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.   DOI
23 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.   DOI
24 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.   DOI
25 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.
26 Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. 1998. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell. 1: 949-957.   DOI
27 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.
28 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.   DOI
29 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.
30 Chen Q, Kang J, Fu C. 2018. The independence of and associations among apoptosis, autophagy, and necrosis. Signal Transduct. Target. Ther. 3: 18.
31 Fischer U, Schulze-Osthoff K. 2005. New approaches and therapeutics targeting apoptosis in disease. Pharmacol. Rev. 57: 187-215.   DOI
32 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.
33 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.   DOI
34 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.   DOI
35 Hensel P. 2010. Nutrition and skin diseases in veterinary medicine. Clin. Dermatol. 28: 686-693.   DOI
36 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.   DOI
37 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.
38 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.
39 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.   DOI
40 Baumer W, Kietzmann M. 2007. Effects of cyclosporin A and cilomilast on activated canine, murine and human keratinocytes. Vet. Dermatol. 18: 107-114.   DOI
41 Huang P, Han J, Hui L. 2010. MAPK signaling in inflammation-associated cancer development. Protein Cell 1: 218-226.   DOI
42 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.   DOI
43 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.   DOI
44 Teraki Y, Shiohara T. 1999. Apoptosis and the skin. Eur. J. Dermatol. 9: 413-425; quiz 426.
45 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.   DOI
46 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.
47 Rumzhum NN, Ammit AJ. 2016. Cyclooxygenase 2: its regulation, role and impact in airway inflammation. Clin. Exp. Allergy 46: 397-410.   DOI
48 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.   DOI
49 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.   DOI
50 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.   DOI