Protective Effects of Ethanol Extract of Brazilian Green Propolis and Apigenin Against Weak Ultraviolet Ray-B-Induced Barrier Dysfunction Via Suppressing Nitric Oxide Production and Mislocalization of Claudin-1 in HaCaT Cells

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2021 Oct 13

PMID 34638666

Citations 6

Authors

Yuta Yoshino

Kana Marunaka

Mao Kobayashi

Haruka Matsunaga

Shokoku Shu

Toshiyuki Matsunaga

Akira Ikari

Affiliations

Soon will be listed here.

Abstract

Once weak ultraviolet ray-B (UVB) irradiates the skin cells, the generation of reactive nitrogen species (RNS), but not reactive oxygen species (ROS), is stimulated for the mislocalization of claudin-1 (CLDN1), an essential protein for forming tight junctions (TJs). Since our skin is constantly exposed to sunlight throughout our lives, an effective protection strategy is needed to maintain the skin barrier against weak UVB. In the present study, we investigated whether an ethanol extract of Brazilian green propolis (EBGP) and flavonoids had a protective effect against weak UVB irradiation-induced barrier dysfunction in human keratinocyte-derived HaCaT cells. A pretreatment with EBGP suppressed TJ permeability, RNS production, and the nitration level of CLDN1 in the weak UVB-exposed cells. Among the propolis components, apigenin and apigenin-like flavonoids have potent protective effects against NO production and the mislocalization of CLDN1 induced by UVB. The analyses between structures and biological function revealed that the chemically and structurally characteristic flavonoids with a hydroxyl group at the 4' position on the B-ring might contribute to its protective effect on barrier dysfunction caused by weak UVB irradiation. In conclusion, EBGP and its component apigenin protect HaCaT cells from weak UVB irradiation-induced TJ barrier dysfunction mediated by suppressing NO production.

Citing Articles

Radioprotective Effects from Propolis: A Review.

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References

Sugawara T, Iwamoto N, Akashi M, Kojima T, Hisatsune J, Sugai M . Tight junction dysfunction in the stratum granulosum leads to aberrant stratum corneum barrier function in claudin-1-deficient mice. J Dermatol Sci. 2013; 70(1):12-8. DOI: 10.1016/j.jdermsci.2013.01.002. View

Andrade J, Denadai M, de Oliveira C, Nunes M, Narain N . Evaluation of bioactive compounds potential and antioxidant activity of brown, green and red propolis from Brazilian northeast region. Food Res Int. 2017; 101:129-138. DOI: 10.1016/j.foodres.2017.08.066. View

Saric S, Sivamani R . Polyphenols and Sunburn. Int J Mol Sci. 2016; 17(9). PMC: 5037798. DOI: 10.3390/ijms17091521. View

Sae-Wong C, Matsuda H, Tewtrakul S, Tansakul P, Nakamura S, Nomura Y . Suppressive effects of methoxyflavonoids isolated from Kaempferia parviflora on inducible nitric oxide synthase (iNOS) expression in RAW 264.7 cells. J Ethnopharmacol. 2011; 136(3):488-95. DOI: 10.1016/j.jep.2011.01.013. View

Rossato M, Trevisan G, Walker C, Klafke J, de Oliveira A, Villarinho J . Eriodictyol: a flavonoid antagonist of the TRPV1 receptor with antioxidant activity. Biochem Pharmacol. 2010; 81(4):544-51. DOI: 10.1016/j.bcp.2010.11.004. View

Shahinozzaman M, Basak B, Emran R, Rozario P, Obanda D . Artepillin C: A comprehensive review of its chemistry, bioavailability, and pharmacological properties. Fitoterapia. 2020; 147:104775. DOI: 10.1016/j.fitote.2020.104775. View

Gou K, Zeng R, Ren X, Dou Q, Yang Q, Dong Y . Anti-rheumatoid arthritis effects in adjuvant-induced arthritis in rats and molecular docking studies of Polygonum orientale L. extracts. Immunol Lett. 2018; 201:59-69. DOI: 10.1016/j.imlet.2018.11.009. View

Gruber R, Bornchen C, Rose K, Daubmann A, Volksdorf T, Wladykowski E . Diverse regulation of claudin-1 and claudin-4 in atopic dermatitis. Am J Pathol. 2015; 185(10):2777-89. DOI: 10.1016/j.ajpath.2015.06.021. View

Shigetomi K, Ikenouchi J . Regulation of the epithelial barrier by post-translational modifications of tight junction membrane proteins. J Biochem. 2017; 163(4):265-272. DOI: 10.1093/jb/mvx077. View

10.

Sutter C, Rainwater H, Sutter T . Contributions of Nitric Oxide to AHR-Ligand-Mediated Keratinocyte Differentiation. Int J Mol Sci. 2020; 21(16). PMC: 7460822. DOI: 10.3390/ijms21165680. View

11.

Park C, Min S, Yu H, Kim K, Kim S, Lee H . Effects of Apigenin on RBL-2H3, RAW264.7, and HaCaT Cells: Anti-Allergic, Anti-Inflammatory, and Skin-Protective Activities. Int J Mol Sci. 2020; 21(13). PMC: 7370139. DOI: 10.3390/ijms21134620. View

12.

Pasupuleti V, Sammugam L, Ramesh N, Gan S . Honey, Propolis, and Royal Jelly: A Comprehensive Review of Their Biological Actions and Health Benefits. Oxid Med Cell Longev. 2017; 2017:1259510. PMC: 5549483. DOI: 10.1155/2017/1259510. View

13.

Franchin M, Freires I, Lazarini J, Nani B, da Cunha M, Colon D . The use of Brazilian propolis for discovery and development of novel anti-inflammatory drugs. Eur J Med Chem. 2017; 153:49-55. DOI: 10.1016/j.ejmech.2017.06.050. View

14.

Kim S, Woo E, Lee D . Apigenin promotes antibacterial activity via regulation of nitric oxide and superoxide anion production. J Basic Microbiol. 2020; 60(10):862-872. DOI: 10.1002/jobm.202000432. View

15.

Pietta P . Flavonoids as antioxidants. J Nat Prod. 2000; 63(7):1035-42. DOI: 10.1021/np9904509. View

16.

Machado J, Assuncao A, Silva M, Reis A, Costa G, Arruda D . Brazilian green propolis: anti-inflammatory property by an immunomodulatory activity. Evid Based Complement Alternat Med. 2013; 2012:157652. PMC: 3541042. DOI: 10.1155/2012/157652. View

17.

Boukamp P, Petrussevska R, Breitkreutz D, Hornung J, Markham A, Fusenig N . Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol. 1988; 106(3):761-71. PMC: 2115116. DOI: 10.1083/jcb.106.3.761. View

18.

Tsukita S, Furuse M, Itoh M . Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol. 2001; 2(4):285-93. DOI: 10.1038/35067088. View

19.

Yang B, Kotani A, Arai K, Kusu F . Estimation of the antioxidant activities of flavonoids from their oxidation potentials. Anal Sci. 2001; 17(5):599-604. DOI: 10.2116/analsci.17.599. View

20.

Marunaka K, Kobayashi M, Shu S, Matsunaga T, Ikari A . Brazilian Green Propolis Rescues Oxidative Stress-Induced Mislocalization of Claudin-1 in Human Keratinocyte-Derived HaCaT Cells. Int J Mol Sci. 2019; 20(16). PMC: 6719963. DOI: 10.3390/ijms20163869. View