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Chemokine expression in human 3-dimensional cultured epidermis exposed to PM2.5 collected by cyclonic separation

  • Maori, Kono (Laboratory of Advanced Cosmetic Science, Graduate School of Pharmaceutical Sciences, Osaka University) ;
  • Tomoaki, Okuda (Faculty of Science and Technology, Keio University) ;
  • Nami, Ishihara (Program of Biomedical Science, Graduate School of Integrated Sciences for Life, Hiroshima University) ;
  • Hiroyuki, Hagino (Japan Automobile Research Institute) ;
  • Yuto, Tani (School of Creative Science and Engineering, Waseda University) ;
  • Hiroshi, Okochi (School of Creative Science and Engineering, Waseda University) ;
  • Chiharu, Tokoro (School of Creative Science and Engineering, Waseda University) ;
  • Masayuki, Takaishi (Laboratory of Advanced Cosmetic Science, Graduate School of Pharmaceutical Sciences, Osaka University) ;
  • Hidefumi, Ikeda (Laboratory of Advanced Cosmetic Science, Graduate School of Pharmaceutical Sciences, Osaka University) ;
  • Yasuhiro, Ishihara (Program of Biomedical Science, Graduate School of Integrated Sciences for Life, Hiroshima University)
  • Received : 2022.05.04
  • Accepted : 2022.06.20
  • Published : 2023.01.15

Abstract

Fine particulate matter (PM2.5) exposure has a risk of inducing several health problems, especially in the respiratory tract. The skin is the largest organ of the human body and is therefore the primary target of PM2.5. In this study, we examined the effects of PM2.5 on the skin using a human 3-dimensional cultured epidermis model. PM2.5 was collected by cyclonic separation in Yokohama, Japan. Global analysis of 34 proteins released from the epidermis revealed that the chemokines, chemokine C-X-C motif ligand 1 (CXCL1) and interleukin 8 (IL-8), were significantly increased in response to PM2.5 exposure. These chemokines stimulated neutrophil chemotaxis in a C-X-C motif chemokine receptor 2-dependent manner. The oxidative stress and signal transducer and activator of transcription 3 pathways may be involved in the increased expression of CXCL1 and IL-8 in the human epidermis model. Interestingly, in the HaCaT human keratinocyte cell line, PM2.5 did not affect chemokine expression but did induce IL-6 expression, suggesting a different effect of PM2.5 between the epidermis model and HaCaT cells. Overall, PM2.5 could induce the epidermis to release chemokines, followed by neutrophil activation, which might cause an unregulated inflammatory reaction in the skin.

Keywords

Acknowledgement

The authors thank Dr. Miki Tanaka and Ms. Kaede Namba for technical assistance during the course of this study.

References

  1. Dockery DW, Pope CA 3rd, Xu X, Spengler JD, Ware JH, Fay ME, Ferris BG Jr, Speizer FE (1993) An association between air pollution and mortality in six U.S. cities. N Engl J Med 329:1753-1759. https://doi.org/10.1056/NEJM199312093292401
  2. Falcon-Rodriguez CI, Osornio-Vargas AR, Sada-Ovalle I, Segura-Medina P (2016) Aeroparticles, composition, and lung diseases. Front Immunol 7:3. https://doi.org/10.3389/fimmu.2016.00003
  3. Kirrane EF, Luben TJ, Benson A, Owens EO, Sacks JD, Dutton SJ, Madden M, Nichols JL (2019) A systematic review of cardiovascular responses associated with ambient black carbon and fine particulate matter. Environ Int 127:305-316. https://doi.org/10.1016/j.envint.2019.02.027
  4. Darquenne C (2014) Aerosol deposition in the human lung in reduced gravity. J Aerosol Med Pulm Drug Deliv 27:170-177. https://doi.org/10.1089/jamp.2013.1079
  5. Nemmar A, Holme JA, Rosas I, Schwarze PE, Alfaro-Moreno E (2013) Recent advances in particulate matter and nanoparticle toxicology: a review of the in vivo and in vitro studies. Biomed Res Int 2013:279371. https://doi.org/10.1155/2013/279371
  6. Park TH, Park S, Cho MK, Kim S (2022) Associations of particulate matter with atopic dermatitis and chronic inflammatory skin diseases in South Korea. Clin Exp Dermatol 47:325-334. https://doi.org/10.1111/ced.14910
  7. Piao MJ, Ahn MJ, Kang KA, Ryu YS, Hyun YJ, Shilnikova K, Zhen AX, Jeong JW, Choi YH, Kang HK, Koh YS, Hyun JW (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
  8. Krutmann J, Liu W, Li L, Pan X, Crawford M, Sore G, Seite S (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
  9. Qiao Y, Li Q, Du HY, Wang QW, Huang Y, Liu W (2017) Airborne polycyclic aromatic hydrocarbons trigger human skin cells aging through aryl hydrocarbon receptor. Biochem Biophys Res Commun 488:445-452. https://doi.org/10.1016/j.bbrc.2017.04.160
  10. Dong L, Hu R, Yang D, Zhao J, Kan H, Tan J, Guan M, Kang Z, Xu F (2020) Fine particulate matter (PM2.5) upregulates expression of inflammasome NLRP1 via ROS/NF-kappaB signaling in HaCaT Cells. Int J Med Sci 17:2200-2206. https://doi.org/10.7150/ijms.46962
  11. Li Q, Kang Z, Jiang S, Zhao J, Yan S, Xu F, Xu J (2017) Effects of ambient fine particles PM2.5 on human HaCaT Cells. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph14010072
  12. Nagakura C, Negishi Y, Tsukimoto M, Itou S, Kondo T, Takeda K, Kojima S (2014) Involvement of P2Y11 receptor in silica nanoparticles 30-induced IL-6 production by human keratinocytes. Toxicology 322:61-68. https://doi.org/10.1016/j.tox.2014.03.010
  13. Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contam Toxicol 232:1-44. https://doi.org/10.1007/978-3-319-06746-9_1
  14. Liu L, Bridges RJ, Eyer CL (2001) Effect of cytochrome P450 1A induction on oxidative damage in rat brain. Mol Cell Biochem 223:89-94. https://doi.org/10.1023/a:1017904912654
  15. Kim DJ, Iwasaki A, Chien AL, Kang S (2022) UVB-mediated DNA damage induces matrix metalloproteinases to promote photoaging in an AhR- and SP1-dependent manner. JCI Insight. https://doi.org/10.1172/jci.insight.156344
  16. Choi MK, Kim J, Park HM, Lim CM, Pham TH, Shin HY, Kim SE, Oh DK, Yoon DY (2022) The DPA-derivative 11S, 17S-dihydroxy 7,9,13,15,19 (Z, E, Z, E, Z)-docosapentaenoic acid inhibits IL-6 production by inhibiting ROS production and ERK/NF-kappaB pathway in keratinocytes HaCaT stimulated with a fine dust PM10. Ecotoxicol Environ Saf 232:113252. https://doi.org/10.1016/j.ecoenv.2022.113252
  17. Ishihara Y, Takemoto T, Itoh K, Ishida A, Yamazaki T (2015) Dual role of superoxide dismutase 2 induced in activated microglia: oxidative stress tolerance and convergence of inflammatory responses. J Biol Chem 290:22805-22817. https://doi.org/10.1074/jbc.M115.659151
  18. Chowdhury PH, Okano H, Honda A, Kudou H, Kitamura G, Ito S, Ueda K, Takano H (2018) Aqueous and organic extract of PM2.5 collected in different seasons and cities of Japan differently affect respiratory and immune systems. Environ Pollut 235:223-234. https://doi.org/10.1016/j.envpol.2017.12.040
  19. Honda A, Okuda T, Nagao M, Miyasaka N, Tanaka M, Takano H (2021) PM2.5 collected using cyclonic separation causes stronger biological responses than that collected using a conventional filtration method. Environ Res 198:110490. https://doi.org/10.1016/j.envres.2020.110490
  20. Ishihara N, Okuda T, Hagino H, Oguro A, Tani Y, Okochi H, Tokoro C, Fujii-Kuriyama Y, Itoh K, Vogel CFA, Ishihara Y (2022) Involvement of polycyclic aromatic hydrocarbons and endotoxin in macrophage expression of interleukin-33 induced by exposure to particulate matter. J Toxicol Sci 47:201-210. https://doi.org/10.2131/jts.47.201
  21. Ishihara Y, Itoh K, Ishida A, Yamazaki T (2015) Selective estrogen-receptor modulators suppress microglial activation and neuronal cell death via an estrogen receptor-dependent pathway. J Steroid Biochem Mol Biol 145:85-93. https://doi.org/10.1016/j.jsbmb.2014.10.002
  22. Ishihara Y, Kawami T, Ishida A, Yamazaki T (2012) Tributyltin induces oxidative stress and neuronal injury by inhibiting glutathione S-transferase in rat organotypic hippocampal slice cultures. Neurochem Int 60:782-790. https://doi.org/10.1016/j.neuint.2012.03.004
  23. Cho AK, Sioutas C, Miguel AH, Kumagai Y, Schmitz DA, Singh M, Eiguren-Fernandez A, Froines JR (2005) Redox activity of airborne particulate matter at different sites in the Los Angeles Basin. Environ Res 99:40-47. https://doi.org/10.1016/j.envres.2005.01.003
  24. Kumagai Y, Koide S, Taguchi K, Endo A, Nakai Y, Yoshikawa T, Shimojo N (2002) Oxidation of proximal protein sulfhydryls by phenanthraquinone, a component of diesel exhaust particles. Chem Res Toxicol 15:483-489. https://doi.org/10.1021/tx0100993
  25. Inami Y, Andoh T, Sasaki A, Kuraishi Y (2013) Topical surfactant-induced pruritus: involvement of histamine released from epidermal keratinocytes. J Pharmacol Exp Ther 344:459-466. https://doi.org/10.1124/jpet.112.200063
  26. Kojima H, Katoh M, Shinoda S, Hagiwara S, Suzuki T, Izumi R, Yamaguchi Y, Nakamura M, Kasahawa T, Shibai A (2014) A catch-up validation study of an in vitro skin irritation test method using reconstructed human epidermis LabCyte EPI-MODEL24. J Appl Toxicol 34:766-774. https://doi.org/10.1002/jat.2937
  27. Saito K, Takenouchi O, Nukada Y, Miyazawa M, Sakaguchi H (2017) An in vitro skin sensitization assay termed EpiSensA for broad sets of chemicals including lipophilic chemicals and pre/pro-haptens. Toxicol In Vitro 40:11-25. https://doi.org/10.1016/j.tiv.2016.12.005
  28. Feng S, Gao D, Liao F, Zhou F, Wang X (2016) The health effects of ambient PM2.5 and potential mechanisms. Ecotoxicol Environ Saf 128:67-74. https://doi.org/10.1016/j.ecoenv.2016.01.030
  29. Phillipson M, Kubes P (2019) The healing power of neutrophils. Trends Immunol 40:635-647. https://doi.org/10.1016/j.it.2019.05.001
  30. Su Y, Richmond A (2015) Chemokine regulation of neutrophil infiltration of skin wounds. Adv Wound Care (New Rochelle) 4:631-640. https://doi.org/10.1089/wound.2014.0559
  31. Xing YF, Xu YH, Shi MH, Lian YX (2016) The impact of PM2.5 on the human respiratory system. J Thorac Dis 8:E69-E74. https://doi.org/10.3978/j.issn.2072-1439.2016.01.19
  32. Ejaz S, Ashraf M, Nawaz M, Lim CW (2009) Total particulate matter and wound healing: an in vivo study with histological insights. Biomed Environ Sci 22:278-287. https://doi.org/10.1016/S0895-3988(09)60057-X
  33. Vierkotter A, Schikowski T, Ranft U, Sugiri D, Matsui M, Kramer U, Krutmann J (2010) Airborne particle exposure and extrinsic skin aging. J Invest Dermatol 130:2719-2726. https://doi.org/10.1038/jid.2010.204
  34. Devalaraja RM, Nanney LB, Du J, Qian Q, Yu Y, Devalaraja MN, Richmond A (2000) Delayed wound healing in CXCR2 knockout mice. J Invest Dermatol 115:234-244. https://doi.org/10.1046/j.1523-1747.2000.00034.x
  35. Addison CL, Daniel TO, Burdick MD, Liu H, Ehlert JE, Xue YY, Buechi L, Walz A, Richmond A, Strieter RM (2000) The CXC chemokine receptor 2, CXCR2, is the putative receptor for ELR+ CXC chemokine-induced angiogenic activity. J Immunol 165:5269-5277. https://doi.org/10.4049/jimmunol.165.9.5269
  36. Heidemann J, Ogawa H, Dwinell MB, Rafiee P, Maaser C, Gockel HR, Otterson MF, Ota DM, Lugering N, Domschke W, Binion DG (2003) Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. J Biol Chem 278:8508-8515. https://doi.org/10.1074/jbc.M208231200
  37. Carreira EU, Carregaro V, Teixeira MM, Moriconi A, Aramini A, Verri WA Jr, Ferreira SH, Cunha FQ, Cunha TM (2013) Neutrophils recruited by CXCR1/2 signalling mediate post-incisional pain. Eur J Pain 17:654-663. https://doi.org/10.1002/j.1532-2149.2012.00240.x
  38. Levine JD, Khasar SG, Green PG (2006) Neurogenic inflammation and arthritis. Ann N Y Acad Sci 1069:155-167. https://doi.org/10.1196/annals.1351.014
  39. Sumida H, Yanagida K, Kita Y, Abe J, Matsushima K, Nakamura M, Ishii S, Sato S, Shimizu T (2014) Interplay between CXCR2 and BLT1 facilitates neutrophil infiltration and resultant keratinocyte activation in a murine model of imiquimod-induced psoriasis. J Immunol 192:4361-4369. https://doi.org/10.4049/jimmunol.1302959
  40. Walsh CM, Hill RZ, Schwendinger-Schreck J, Deguine J, Brock EC, Kucirek N, Rifi Z, Wei J, Gronert K, Brem RB, Barton GM, Bautista DM (2019) Neutrophils promote CXCR3-dependent itch in the development of atopic dermatitis. Elife. https://doi.org/10.7554/eLife.48448
  41. Jin SP, Li Z, Choi EK, Lee S, Kim YK, Seo EY, Chung JH, Cho S (2018) Urban particulate matter in air pollution penetrates into the barrier-disrupted skin and produces ROS-dependent cutaneous inflammatory response in vivo. J Dermatol Sci. https://doi.org/10.1016/j.jdermsci.2018.04.015
  42. Sawada N, Nakaya T, Kashima S, Yorifuji T, Hanibuchi T, Charvat H, Yamaji T, Iwasaki M, Inoue M, Iso H, Tsugane S (2022) Long-term exposure to fine particle matter and all-cause mortality and cause-specific mortality in Japan: the JPHC Study. BMC Public Health 22:466. https://doi.org/10.1186/s12889-022-12829-2
  43. D'Orazio J, Jarrett S, Amaro-Ortiz A, Scott T (2013) UV radiation and the skin. Int J Mol Sci 14:12222-12248. https://doi.org/10.3390/ijms140612222
  44. Mokrzynski K, Krzysztynska-Kuleta O, Zawrotniak M, Sarna M, Sarna T (2021) Fine particulate matter-induced oxidative stress mediated by UVA-visible light leads to keratinocyte damage. Int J Mol Sci. https://doi.org/10.3390/ijms221910645
  45. von Koschembahr A, Youssef A, Beal D, Gudimard L, Giot JP, Douki T (2020) Toxicity and DNA repair in normal human keratinocytes co-exposed to benzo[a]pyrene and sunlight. Toxicol In Vitro 63:104744. https://doi.org/10.1016/j.tiv.2019.104744
  46. Ishihara Y, Shiba D, Shimamoto N (2006) Enhancement of DMNQ-induced hepatocyte toxicity by cytochrome P450 inhibition. Toxicol Appl Pharmacol 214:109-117. https://doi.org/10.1016/j.taap.2005.12.003
  47. Hagio-Izaki K, Yasunaga M, Yamaguchi M, Kajiya H, Morita H, Yoneda M, Hirofuji T, Ohno J (2018) Lipopolysaccharide induces bacterial autophagy in epithelial keratinocytes of the gingival sulcus. BMC Cell Biol 19:18. https://doi.org/10.1186/s12860-018-0168-x
  48. Menden HL, Xia S, Mabry SM, Navarro A, Nyp MF, Sampath V (2016) Nicotinamide adenine dinucleotide phosphate oxidase 2 regulates LPS-induced inflammation and alveolar remodeling in the developing lung. Am J Respir Cell Mol Biol 55:767-778. https://doi.org/10.1165/rcmb.2016-0006OC
  49. Bae HC, Jeong SH, Kim JH, Lee H, Ryu WI, Kim MG, Son ED, Lee TR, Son SW (2018) RIP4 upregulates CCL20 expression through STAT3 signalling in cultured keratinocytes. Exp Dermatol 27:1126-1133. https://doi.org/10.1111/exd.13750
  50. Li H, Li H, Huo R, Wu P, Shen Z, Xu H, Shen B, Li N (2017) Cyr61/CCN1 induces CCL20 production by keratinocyte via activating p38 and JNK/AP-1 pathway in psoriasis. J Dermatol Sci 88:46-56. https://doi.org/10.1016/j.jdermsci.2017.05.018
  51. Park JH, Lee KY, Park B, Yoon J (2015) Suppression of Th2 chemokines by crocin via blocking of ERK-MAPK/NF-kappaB/STAT1 signalling pathways in TNF-alpha/IFN-gamma-stimulated human epidermal keratinocytes. Exp Dermatol 24:634-636. https://doi.org/10.1111/exd.12726
  52. Rinna A, Forman HJ (2008) SHP-1 inhibition by 4-hydroxynonenal activates Jun N-terminal kinase and glutamate cysteine ligase. Am J Respir Cell Mol Biol 39:97-104. https://doi.org/10.1165/rcmb.2007-0371OC
  53. Alicea-Velazquez NL, Jakoncic J, Boggon TJ (2013) Structure-guided studies of the SHP-1/JAK1 interaction provide new insights into phosphatase catalytic domain substrate recognition. J Struct Biol 181:243-251. https://doi.org/10.1016/j.jsb.2012.12.009
  54. Carballo M, Conde M, El Bekay R, Martin-Nieto J, Camacho MJ, Monteseirin J, Conde J, Bedoya FJ, Sobrino F (1999) Oxidative stress triggers STAT3 tyrosine phosphorylation and nuclear translocation in human lymphocytes. J Biol Chem 274:17580-17586. https://doi.org/10.1074/jbc.274.25.17580
  55. Qu Y, Oyan AM, Liu R, Hua Y, Zhang J, Hovland R, Popa M, Liu X, Brokstad KA, Simon R, Molven A, Lin B, Zhang WD, McCormack E, Kalland KH, Ke XS (2013) Generation of prostate tumor-initiating cells is associated with elevation of reactive oxygen species and IL-6/STAT3 signaling. Cancer Res 73:7090-7100. https://doi.org/10.1158/0008-5472.CAN-13-1560