Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
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Para-phenylenediamine, an oxidative hair dye ingredient, increases thymic stromal lymphopoietin and proinflammatory cytokines causing acute dermatitis

  • Lee, Jae Kwon (BK21plus Team, College of Pharmacy, The Catholic University of Korea) ;
  • Lee, Hye Eun (BK21plus Team, College of Pharmacy, The Catholic University of Korea) ;
  • Yang, Gabsik (BK21plus Team, College of Pharmacy, The Catholic University of Korea) ;
  • Kim, Kyu-Bong (College of Pharmacy, Dankook University) ;
  • Kwack, Seung Jun (Department of Bio Health Science, Changwon National University) ;
  • Lee, Joo Young (BK21plus Team, College of Pharmacy, The Catholic University of Korea)
  • Received : 2019.10.14
  • Accepted : 2020.02.08
  • Published : 2020.10.15
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Abstract

Due to high consumption of cosmetics in modern society, people are always exposed to the risk of skin damage and complications. Para-phenylenediamine (P-PD), an ingredient of hair dye, has been reported to cause allergic contact dermatitis. However, the mechanism has not been well elucidated. Here, we identify that P-PD causes dermatitis by increasing thymic stromal lymphopoietin (TSLP) and inflammatory cytokines. Topical application of P-PD to mouse ear skin in consecutive 5 days resulted in dermatitis symptoms and increased ear thickness. TSLP production in skin was upregulated by P-PD treatment alone. In addition, P-PD-induced TSLP production was potentiated by MC903, which is an in vivo TSLP inducer. P-PD increased TSLP production in keratinocytes (KCMH-1 cells and phorbol 12-myristate 13-acetate-stimulated PAM212 cells). The production of proinflammatory cytokines such as IL-1β, IL-6, IFN-γ, and CCL2, was upregulated by P-PD treatment together with MC903. The results show that repeated exposure to P-PD causes acute contact dermatitis mediated by increasing the expression of TSLP and proinflammatory cytokines.

Keywords

Acknowledgement

This work was supported by grants (18172MFDS231 and 19172MFDS221) from the Ministry of Food and Drug Safety, Korea in 2018 and 2019.

References

  1. Chen X, Sullivan DA, Sullivan AG, Kam WR, Liu Y (2018) Toxicity of cosmetic preservatives on human ocular surface and adnexal cells. Exp Eye Res 170:188-197. https://doi.org/10.1016/j.exer.2018.02.020
  2. Nohynek GJ, Fautz R, Benech-Kieffer F, Toutain H (2004) Toxicity and human health risk of hair dyes. Food Chem Toxicol Int J Publ Br Ind Biol Res Assoc 42:517-543. https://doi.org/10.1016/j.fct.2003.11.003
  3. McFadden JP, White IR, Frosch PJ, Sosted H, Johansen JD, Menne T (2007) Allergy to hair dye. BMJ 334:220. https://doi.org/10.1136/bmj.39042.643206.BE
  4. McFadden JP, Yeo L, White JL (2011) Clinical and experimental aspects of allergic contact dermatitis to para-phenylenediamine. Clin Dermatol 29:316-324. https://doi.org/10.1016/j.clindermatol.2010.11.011
  5. Oakes T, Popple AL, Williams J, Best K, Heather JM, Ismail M, Maxwell G, Gellatly N, Dearman RJ, Kimber I, Chain B (2017) The T cell response to the contact sensitizer paraphenylenediamine is characterized by a polyclonal diverse repertoire of antigen-specific receptors. Front Immunol 8:162. https://doi.org/10.3389/fimmu.2017.00162
  6. Vogel TA, Coenraads PJ, Bijkersma LM, Vermeulen KM, Schuttelaar ML (2015) p-Phenylenediamine exposure in real life-a case-control study on sensitization rate, mode and elicitation reactions in the northern Netherlands. Contact Dermat 72:355-361. https://doi.org/10.1111/cod.12354
  7. Basketter DA, Goodwin BF (1988) Investigation of the prohapten concept. Cross reactions between 1,4-substituted benzene derivatives in the guinea pig. Contact Dermat 19:248-253 https://doi.org/10.1111/j.1600-0536.1988.tb02921.x
  8. Nacaroglu HT, Yavuz S, Basman E, Bahceci S, Tasdemir M, Yigit O, Can D (2015) The clinical spectrum of reactions developed based on paraphenylenediamine hypersensitivity two pediatric cases. Postepy dermatologii i alergologii 32:393-395. https://doi.org/10.5114/pdia.2015.52738
  9. Mukkanna KS, Stone NM, Ingram JR (2017) Para-phenylenediamine allergy: current perspectives on diagnosis and management. J Asthma Allergy 10:9-15. https://doi.org/10.2147/jaa.S90265
  10. Thyssen JP, White JM (2008) Epidemiological data on consumer allergy to p-phenylenediamine. Contact Dermat 59:327-343. https://doi.org/10.1111/j.1600-0536.2008.01427.x
  11. Sharma VK, Chakrabarti A (1998) Common contact sensitizers in Chandigarh, India. A study of 200 patients with the European standard series. Contact Dermat 38:127-131 https://doi.org/10.1111/j.1600-0536.1998.tb05677.x
  12. Ziegler SF (2012) Thymic stromal lymphopoietin and allergic disease. J Allergy Clin Immunol 130:845-852. https://doi.org/10.1016/j.jaci.2012.07.010
  13. Leyva-Castillo JM, Hener P, Michea P, Karasuyama H, Chan S, Soumelis V, Li M (2013) Skin thymic stromal lymphopoietin initiates Th2 responses through an orchestrated immune cascade. Nat Commun 4:2847. https://doi.org/10.1038/ncomms3847
  14. Wong CK, Hu S, Cheung PF, Lam CW (2010) Thymic stromal lymphopoietin induces chemotactic and prosurvival effects in eosinophils: implications in allergic inflammation. Am J Respir Cell Mol Biol 43:305-315. https://doi.org/10.1165/rcmb.2009-0168OC
  15. Segawa R, Yamashita S, Mizuno N, Shiraki M, Hatayama T, Satou N, Hiratsuka M, Hide M, Hirasawa N (2014) Identification of a cell line producing high levels of TSLP: advantages for screening of anti-allergic drugs. J Immunol Methods 402:9-14. https://doi.org/10.1016/j.jim.2013.10.012
  16. Yuspa SH, Hawley-Nelson P, Koehler B, Stanley JR (1980) A survey of transformation markers in differentiating epidermal cell lines in culture. Cancer Res 40:4694-4703
  17. Yang G, Lee HE, Lim KM, Choi YK, Kim KB, Lee BM, Lee JY (2018) Potentiation of skin TSLP production by a cosmetic colorant leads to aggravation of dermatitis symptoms. Chem Biol Interact 284:41-47. https://doi.org/10.1016/j.cbi.2018.02.020
  18. Lee HE, Yang G, Han SH, Lee JH, An TJ, Jang JK, Lee JY (2018) Anti-obesity potential of Glycyrrhiza uralensis and licochalcone A through induction of adipocyte browning. Biochem Biophys Res Commun 503:2117-2123. https://doi.org/10.1016/j.bbrc.2018.07.168
  19. Yang G, Koo JE, Lee HE, Shin SW, Um SH, Lee JY (2019) Immunostimulatory activity of Y-shaped DNA nanostructures mediated through the activation of TLR9. Biomed Pharmacother 112:108657. https://doi.org/10.1016/j.biopha.2019.108657
  20. Li M, Hener P, Zhang Z, Kato S, Metzger D, Chambon P (2006) Topical vitamin D3 and low-calcemic analogs induce thymic stromal lymphopoietin in mouse keratinocytes and trigger an atopic dermatitis. Proc Natl Acad Sci USA 103:11736-11741. https://doi.org/10.1073/pnas.0604575103
  21. Jang HY, Koo JH, Lee SM, Park BH (2018) Atopic dermatitis-like skin lesions are suppressed in fat-1 transgenic mice through the inhibition of inflammasomes. Exp Mol Med 50:73. https://doi.org/10.1038/s12276-018-0104-3
  22. Dai J, Choo MK, Park JM, Fisher DE (2017) Topical ROR inverse agonists suppress inflammation in mouse models of atopic dermatitis and acute irritant dermatitis. J Investig Dermatol 137:2523-2531. https://doi.org/10.1016/j.jid.2017.07.819
  23. Lee HC, Ziegler SF (2007) Inducible expression of the proallergic cytokine thymic stromal lymphopoietin in airway epithelial cells is controlled by NFkappaB. Proc Natl Acad Sci USA 104:914-919. https://doi.org/10.1073/pnas.0607305104
  24. Divekar R, Kita H (2015) Recent advances in epithelium-derived cytokines (IL-33, IL-25, and thymic stromal lymphopoietin) and allergic inflammation. Curr Opin Allergy Clin Immunol 15:98-103. https://doi.org/10.1097/aci.0000000000000133
  25. Klonowska J, Glen J, Nowicki RJ, Trzeciak M (2018) New cytokines in the pathogenesis of atopic dermatitis-new therapeutic targets. Int J Mol Sci. https://doi.org/10.3390/ijms19103086
  26. Reena K, Ng KY, Koh RY, Gnanajothy P, Chye SM (2017) Para-phenylenediamine induces apoptosis through activation of reactive oxygen species-mediated mitochondrial pathway, and inhibition of the NF-kappaB, mTOR, and Wnt pathways in human urothelial cells. Environ Toxicol 32:265-277. https://doi.org/10.1002/tox.22233
  27. Zaid Y, Marhoume F, Senhaji N, Kojok K, Boufous H, Naya A, Oudghiri M, Darif Y, Habti N, Zouine S, Mohamed F, Chait A, Bagri A (2016) Paraphenylene diamine exacerbates platelet aggregation and thrombus formation in response to a low dose of collagen. J Toxicol Sci 41:123-128. https://doi.org/10.2131/jts.41.123
  28. Oyoshi MK, He R, Kumar L, Yoon J, Geha RS (2009) Cellular and molecular mechanisms in atopic dermatitis. Adv Immunol 102:135-226. https://doi.org/10.1016/s0065-2776(09)01203-6
  29. Noske K (2018) Secreted immunoregulatory proteins in the skin. J Dermatol Sci 89:3-10. https://doi.org/10.1016/j.jdermsci.2017.10.008
  30. Johnson-Huang LM, Suarez-Farinas M, Pierson KC, Fuentes-Duculan J, Cueto I, Lentini T, Sullivan-Whalen M, Gilleaudeau P, Krueger JG, Haider AS, Lowes MA (2012) A single intradermal injection of IFN-gamma induces an inflammatory state in both non-lesional psoriatic and healthy skin. J Investig Dermatol 132:1177-1187. https://doi.org/10.1038/jid.2011.458
  31. Giustizieri ML, Mascia F, Frezzolini A, De Pita O, Chinni LM, Giannetti A, Girolomoni G, Pastore S (2001) Keratinocytes from patients with atopic dermatitis and psoriasis show a distinct chemokine production profile in response to T cell-derived cytokines. J Allergy Clin Immunol 107:871-877. https://doi.org/10.1067/mai.2001.114707
  32. Kasi RA, Moi CS, Kien YW, Yian KR, Chin NW, Yen NK, Ponnudurai G, Fong SH (2015) Para-phenylenediamine-induces apoptosis via a pathway dependent on PTK-Ras-Raf-JNK activation but independent of the PI3K/Akt pathway in NRK-52E cells. Mol Med Rep 11:2262-2268. https://doi.org/10.3892/mmr.2014.2979

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