SUMMARY. The decrease of Tjp1 gene expression against the background of activation of free radical processes (increase in the content of superoxide anion-radical) was observed during healing of full-thickness skin wounds in rats. The restoration of the expression level of this gene may be mediated by an increase in the expression level of Tlr2 gene. The level of Tjp1 gene expression as well as the content of the superoxide anion radical, was closer to the control values at the specified wound pattern in the absence of Tlr2 gene overexpression upon the treatment with melanin during restoration of skin integrity.
Keywords: Tjp1, Tlr2 gene expression, full-thickness skin wound, melanin
Full text and supplemented materials
References
1. Penn, J.W., Grobbelaar, A.O., and Rolfe, K.J., The role of the TGF-? family in wound healing, burns and scarring: a review, Int. J. Burn. Trauma, 2012, vol. 2, no. 1, pp. 18–28.
2. Kuo, I.-H., Carpenter-Mendini, A., Yoshida, T., McGirt, L.Y., Ivanov, A.I., Barnes, K.C., Gallo, R.L., Borkowski, A.W., Yamasaki, K., Leung, D.Y., Georas, S.N., De Benedetto, A., and Beck, L.A., Activation of epidermal toll-like receptor 2 enhances tight junction function—implications for atopic dermatitis and skin barrier repair, J. Invest. Dermatol., 2013, vol. 133, no. 4, pp. 988–998. https://doi.org/10.1038/jid.2012.437
3. Korotkyi, O., Dvorshchenko, K., Vovk, A., Dranitsina, A., Tymoshenko, M., Kot, L., and Ostapchenko, L., Effect of probiotic composition on oxidative/antioxidant balance in blood of rats under experimental osteoarthritis, Ukr. Biochem. J., 2019, vol. 91, no. 6, pp. 49–58. https://doi.org/10.15407/ubj91.06.049
4. Wagener, F.A., Carels, C.E., and Lundvig, D.M., Targeting the redox balance in inflammatory skin conditions, Int. J. Mol. Sci., 2013, vol. 14, no. 9, pp. 126–167. https://doi.org/10.3390/ijms14059126
5. Dranitsina, A.S., Taburets, O.V., Dvorshchenko, K.O., Grebinyk, D.M., Beregova, T.V., and Ostapchenko, L.I., TGFB 1, PTGS 2 genes expression during dynamics of wound healing and with the treatment of melanin, Res. J. Pharm., Biol. Chem. Sci., 2017, vol. 8, no. 1, pp. 2014–2023. https://doi.org/10.3103/S0095452718030039
6. Addor, F.A.S., Antioxidants in dermatology, An. Bras. Dermatol. 2017, vol. 92, no. 3, pp. 356–362. https://doi.org/10.1590/abd1806-4841.20175697
7. Cario, E., Gerken, G., and Podolsky, D.K., Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C, Gastroenterology. 2004, vol. 127, pp. 224–238. https://doi.org/10.1053/j.gastro.2004.04.015
8. Yuki, T, Yoshida, H., Akazawa, Y., Komiya, A., Sugiyama, Y., and Inoue, S., Activation of TLR2 enhances tight junction barrier in epidermal keratinocytes, J. Immunol., 2011b, vol. 187, pp. 3230–3237. https://doi.org/10.4049/jimmunol.1100058
9. Rajaiah, R., Perkins, D.J., Ireland, D.D.C., and Vogel, S.N., CD14 dependence of TLR4 endocytosis and TRIF signaling displays ligand specificity and is dissociable in endotoxin tolerance, Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, pp. 8391–8396. https://doi.org/10.1073/pnas.1424980112
10. Sun, L., Liu, W., and Zhang, L.-J., The role of Toll-like receptors in skin host defense, psoriasis, and atopic dermatitis, J. Immunol. Res., 2019. https://doi.org/10.1155/2019/1824624
11. Bo Zhang, Yeong Min Choi, Junwoo Lee, In Sook An, Li Li, Congfen He, Yinmao Dong, Seung-hee Bae, and Hong Meng, Toll-like receptor 2 plays a critical role in pathogenesis of acne vulgaris, Med. Dermatol., 2019, vol. 4, pp. 1–6. https://doi.org/10.1186/s41702-019-0042-2
12. Niebuhr, M., Lutat, C., Sigel, S., and Werfel, T., Impaired TLR-2 expression and TLR-2-mediated cytokine secretion in macrophages from patients with atopic dermatitis, Allergy, 2009, vol. 64, pp. 1580–1587. https://doi.org/10.1111/j.1398-9995.2009.02050.x
13. Brandner, J.M., Kief, S., Grund, C., Rendl, M., Houdek, P., Kuhn, C., Tschachler, E., Franke, W.W., and Moll, I., Organization and formation of the tight junction system in human epidermis and cultured keratinocytes, Eur. J. Cell Biol., 2002, vol. 81, pp. 253–263. https://doi.org/10.1078/0171-9335-00244
14. Qiao X, Roth I, F?raille E, Hasler U. Different effects of ZO-1, ZO-2 and ZO-3 silencing on kidney collecting duct principal cell proliferation and adhesion, Cell Cycle, 2014, vol. 13, no. 19, pp. 3059–3075. https://doi.org/10.4161/15384101.2014.949091
15. Steed, E., Balda, M.S., and Matter, K., Dynamics and functions of tight junctions, Trends Cell Biol., 2010, vol. 20, pp. 142–149.https://doi.org/10.1016/j.tcb.2009.12.002
16. Bauer, H., Zweimueller-Mayer, J., Steinbacher, P., Lametschwandtner, A., and Bauer, H.C., The dual role of zonula occludens (ZO) proteins, J. Biomed. Biotechnol., 2010, vol. 2010, p. 402593. https://doi.org/10.1155/2010/402593
17. Stacey, A. N. D’Mello, Graeme, J. Finlay, Bruce C., Baguley, Marjan, E., Askarian-Amiri., Signal. Path. Melanog., 2016, vol. 17, no. 7, p. 1144. https://doi.org/10.3390/ijms17071144
18. El-Obeid, A., Al-Harbi, S., Al-Jomah, N., Hassib, A., Herbal melanin modulates tumor necrosis factor (TNF-alfa), interleukin 6 (IL-6) and vascular endothelial growth factor (VEGF) production, Phytomedicine, 2006, vol. 13, pp. 324–33. https://doi.org/10.1016/j.phymed.2005.03.007
19. Golyshkin, D.V., Falaleeva, T.M., Neporada, K.S., and Beregova, T.V., Effect of melanin on the condition of gastric mucosa and reaction of the hypothalamic-pituitary-adrenal axis under acute stress, Physiol. J., 2015, vol. 61, no. 2, pp. 65–72. https://doi.org/10.15407/fz61.02.065
20. Henry, S.L., Concannon, M.J., and Yee, G.J., The effect of magnetic fields on wound healing. Experimental study and review of the literature, Open Acc. J. Plast. Surg., 2008, vol. 8, pp. 393–399.
21. Bilyayeva, O., Neshta, V.V., Golub, A., and Sams-Dodd, F., Effects of sea silon wound healing in the rat, J. Wound Care, 2014, vol. 23, no. 8, pp. 140–146. https://doi.org/10.12968/jowc.2014.23.8.410
22. Schafer, M. and Werner, S., Oxidative stress in normal and impaired wound repair, Pharmacol. Res., 2008, vol. 58, pp. 165–171. https://doi.org/10.1016/j.phrs.2008.06.004
23. Sutherland, M.W. and Learmonth, B.A., The tetrazolium dyes MTS and XTT provide new quantitative assays for superoxide and superoxide dismutase, Free Radic. Res., 1997, vol. 27, no. 3, pp. 283–289. https://doi.org/10.3109/10715769709065766
24. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J., Protein measurement with the Folin phenol reagent, J. Biol. Chem., 1951, vol. 193, no. 1, pp. 265–275. PubMed PMID: 14907713
25. Chomczynski, P. and Sacchi, N., Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction, Anal. Biochem., 1987, vol. 162, no. 1, pp. 156–159. https://doi.org/10.1006/abio.1987.9999
26. Lee, W.H., Sonntag, W.E., Mitschelen, M., Yan, H., and Lee, Y.W., Irradiation induces regionally specific alterations in pro-inflammatory environments in rat brain, Int. J. Radiat. Biol., 2010, vol. 280, no. 2, pp. 132–144. https://doi.org/10.3109/09553000903419346
27. Sakuma, S., Kitamura, T., Kuroda, C., Takeda, K., Nakano, S., Hamashima, T., Kohda, T., Wada, S., Arakawa, Y., and Fujimoto, Y., All-trans arachidonic acid generates reactive oxygen species via xanthine dehydrogenase/xanthine oxidase interconversion in the rat liver cytosol in vitro, J. Clin. Biochem. Nutr., 2012, vol. 51, no. 1, vol. 51, no. 1, pp. 55–60. https://doi.org/10.3164/jcbn.11-97
28. Langbein, H., Brunssen, C., Hofmann, A., Cimalla, P., Brux, M., Bornstein, S.R., Deussen, A., Koch, E., and Morawietz, H., NADPH oxidase 4 protects against development of endothelial dysfunction and atherosclerosis in LDL receptor deficient mice, Eur. Heart J., 2016, vol. 37, no. 22, pp. 1753–1761. https://doi.org/10.1093/eurheartj/ehv564
29. Guo, W., Wang, P., Liu, Z., and Ye, P., Analysis of differential expression of tight junction proteins in cultured oral epithelial cells altered by Porphyromonas gingivalis, Porphyromonas gingivalis lipopolysaccharide, and extracellular adenosine triphosphate, Int. J. Oral. Sci., 2018, vol. 10, no. 1, e8. https://doi.org/10.1038/ijos.2017.51
30. De Benedetto, A., Rafaels, N.M., McGirt, L.Y., Ivanov, A.I., Georas, S.N., Cheadle, C., Berger, A.E., Zhang, K., Vidyasagar, S., Yoshida, T., Boguniewicz, M., Hata, T., Schneider, L.C., Hanifin, J.M., Gallo, R.L., Novak, N., Weidinger, S., Beaty, T.H,, Leung, D.Y., Barnes, K.C., and Beck, L.A., Tight junction defects in patients with atopic dermatitis, J. Allerg. Clin. Immun., 2011, vol. 127, pp. 773–786, e1–e7. https://doi.org/10.1016/j.jaci.2010.10.018
31. Dickel, H., Gambichler, T., Kamphowe, J., Altmeyer, P., and Skrygan, M., Standardized tape stripping prior to patch testing induces upregulation of Hsp90, Hsp70, IL-33, TNF-alpha and IL-8/CXCL8 mRNA: new insights into the involvement of ‘alarmins’, Contact Dermatitis, 2010, vol. 63, pp. 215–222. https://doi.org/10.1111/j.1600-0536.2010.01769.x
32. Berthelot, J.-M., Sellam, J., Maugars, Y., and Berenbaum, F., Cartilage-gut-microbiome axis: a new paradigm for novel therapeutic opportunities in osteoarthritis, RMD Open, 2019, vol. 5, e001037. https://doi.org/10.1136/rmdopen-2019-001037
33. Rajaiah, R., Perkins, D.J., Ireland, D.D.C., and Vogel, S.N., CD14 dependence of TLR4 endocytosis and TRIF signaling displays ligand specificity and is dissociable in endotoxin tolerance, Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, pp. 8391–8396. https://doi.org/10.1073/pnas.1424980112
34. Dana, N., Vaseghi, G., and Javanmard, S.H., Crosstalk between peroxisome proliferator-activated receptors and Toll-like receptors: a systematic review, Adv. Pharm. Bull., 2019, vol. 9, no. 1, pp. 12–21. https://doi.org/10. 15171/apb.2019.003
35. Jin, H., Kumar, L., Mathias, C., Zurakowski, D., Oettgen, H., Gorelik, L., and Geha, R., Toll-like receptor 2 is important for the T(H)1 response to cutaneous sensitization, J. Allerg. Clin. Immun., 2009, vol. 123, no. 4, pp. 875–882. https://doi.org/10.1016/j.jaci.2009.02.007
36. Nahid, M.A., Satoh, M., and Chan, E.K., Mechanistic role of microRNA-146a in endotoxin-induced differential cross-regulation of TLR signaling, J. Immunol., 2011, vol. 186, pp. 1723–1734. https://doi.org/10.4049/jimmunol.1002311
37. Ding, Y., Wang, L., Zhao, Q., Wu, Z., and Kong, L., MicroRNA-93 inhibits chondrocyte apoptosis and inflammation in osteoarthritis by targeting the TLR4/NF-kB signaling pathway, Int. J. Mol. Med., 2019, vol. 43, no. 2, pp. 779–790. https://doi.org/10.3892/ijmm.2018.4033
38. Cui, Y., Wang, X.L., Xue, J., Liu, J.Y., and Xie, M.L., Chrysanthemum morifolium extract attenuates high-fat milk-induced fatty liver through peroxisome proliferator-activated receptor alpha-mediated mechanism in mice, Nutr. Res., 2014, vol. 34, pp. 268–275. https://doi.org/10.1016/j.nutres.2013.12.010