Galactomyces Ferment Filtrate Potentiates an Anti-Inflammaging System in Keratinocytes
Abstract
:1. Introduction
2. Moisturizers and Their Ingredients
3. Activation of AHR-Filaggrin Axis by GFF
4. Antioxidative Properties of GFF
5. Downregulation of Senescence by GFF
6. Enhanced Expression of Caspase-14 by GFF
7. Upregulation of Tight Junction Molecules by GFF
8. Increased Production of Antiinflammatory Cytokine IL-37 by GFF
9. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Rawlings, A.V.; Harding, C.R. Moisturization and skin barrier function. Dermatol. Ther. 2004, 17 (Suppl. S1), 43–48. [Google Scholar] [CrossRef] [PubMed]
- Candi, E.; Schmidt, R.; Melino, G. The cornified envelope: A model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 2005, 6, 328–340. [Google Scholar] [CrossRef]
- Boo, Y.C. Emerging strategies to protect the skin from ultraviolet rays using plant-derived materials. Antioxidants 2020, 9, 637. [Google Scholar] [CrossRef]
- Ryu, Y.S.; Kang, K.A.; Piao, M.J.; Ahn, M.J.; Yi, J.M.; Hyun, Y.M.; Kim, S.H.; Ko, M.K.; Park, C.O.; Hyun, J.W. Particulate matter induces inflammatory cytokine production via activation of NFκB by TLR5-NOX4-ROS signaling in human skin keratinocyte and mouse skin. Redox Biol. 2019, 21, 101080. [Google Scholar] [CrossRef]
- Tanaka, Y.; Uchi, H.; Furue, M. Antioxidant cinnamaldehyde attenuates UVB-induced photoaging. J. Dermatol. Sci. 2019, 96, 151–158. [Google Scholar] [CrossRef]
- Tanaka, Y.; Uchi, H.; Hashimoto-Hachiya, A.; Furue, M. Tryptophan photoproduct FICZ upregulates IL1A, IL1B, and IL6 expression via oxidative stress in keratinocytes. Oxid. Med. Cell Longev. 2018, 2018, 9298052. [Google Scholar] [CrossRef]
- Shive, C.; Pandiyan, P. Inflammation, immune senescence, and dysregulated immune regulation in the elderly. Front. Aging 2022, 3, 840827. [Google Scholar] [CrossRef]
- Heinze-Milne, S.D.; Banga, S.; Howlett, S.E. Frailty and cytokines in preclinical models: Comparisons with humans. Mech. Ageing Dev. 2022, 206, 111706. [Google Scholar] [CrossRef]
- Kimball, A.B.; Alora-Palli, M.B.; Tamura, M.; Mullins, L.A.; Soh, C.; Binder, R.L.; Houston, N.A.; Conley, E.D.; Tung, J.Y.; Annunziata, N.E.; et al. Age-induced and photoinduced changes in gene expression profiles in facial skin of Caucasian females across 6 decades of age. J. Am. Acad. Dermatol. 2018, 78, 29–39. [Google Scholar] [CrossRef] [PubMed]
- Furue, M.; Uchi, H.; Mitoma, C.; Hashimoto-Hachiya, A.; Chiba, T.; Ito, T.; Nakahara, T.; Tsuji, G. Antioxidants for healthy skin: The emerging role of aryl hydrocarbon receptors and nuclear factor-erythroid 2-related factor-2. Nutrients 2017, 9, 223. [Google Scholar] [CrossRef]
- Eassa, H.A.; Eltokhy, M.A.; Fayyaz, H.A.; Khalifa, M.K.A.; Shawky, S.; Helal, N.A.; Eassa, H.A.; Youssef, S.F.; Latz, I.K.; Nounou, M.I. Current topical strategies for skin-aging and inflammaging treatment: Science versus fiction. J. Cosmet. Sci. 2020, 71, 321–350. [Google Scholar]
- Elias, P.M.; Choi, E.H. Interactions among stratum corneum defensive functions. Exp. Dermatol. 2005, 14, 719–726. [Google Scholar] [CrossRef] [PubMed]
- Kypriotou, M.; Huber, M.; Hohl, D. The human epidermal differentiation complex: Cornified envelope precursors, S100 proteins and the ‘fused genes’ family. Exp. Dermatol. 2012, 21, 643–649. [Google Scholar] [CrossRef] [PubMed]
- Hoober, J.K.; Eggink, L.L. The discovery and function of filaggrin. Int. J. Mol. Sci. 2022, 23, 1455. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.; Lim, K.M. Skin barrier dysfunction and filaggrin. Arch. Pharm. Res. 2021, 44, 36–48. [Google Scholar] [PubMed]
- Eckhart, L.; Declercq, W.; Ban, J.; Rendl, M.; Lengauer, B.; Mayer, C.; Lippens, S.; Vandenabeele, P.; Tschachler, E. Terminal differentiation of human keratinocytes and stratum corneum formation is associated with caspase-14 activation. J. Investig. Dermatol. 2000, 115, 1148–1151. [Google Scholar] [CrossRef] [Green Version]
- Hoste, E.; Kemperman, P.; Devos, M.; Denecker, G.; Kezic, S.; Yau, N.; Gilbert, B.; Lippens, S.; De Groote, P.; Roelandt, R.; et al. Caspase-14 is required for filaggrin degradation to natural moisturizing factors in the skin. J. Investig. Dermatol. 2011, 131, 2233–2241. [Google Scholar] [CrossRef] [Green Version]
- Furue, M.; Takahara, M.; Nakahara, T.; Uchi, H. Role of AhR/ARNT system in skin homeostasis. Arch. Dermatol. Res. 2014, 306, 769–779. [Google Scholar] [CrossRef] [Green Version]
- Furue, M.; Tsuji, G.; Mitoma, C.; Nakahara, T.; Chiba, T.; Morino-Koga, S.; Uchi, H. Gene regulation of filaggrin and other skin barrier proteins via aryl hydrocarbon receptor. J. Dermatol. Sci. 2015, 80, 83–88. [Google Scholar] [CrossRef]
- Tsuji, G.; Ito, T.; Chiba, T.; Mitoma, C.; Nakahara, T.; Uchi, H.; Furue, M. The role of the OVOL1-OVOL2 axis in normal and diseased human skin. J. Dermatol. Sci. 2018, 90, 227–231. [Google Scholar] [CrossRef] [Green Version]
- Ito, T.; Tsuji, G.; Ohno, F.; Uchi, H.; Nakahara, T.; Hashimoto-Hachiya, A.; Yoshida, Y.; Yamamoto, O.; Oda, Y.; Furue, M. Activation of the OVOL1-OVOL2 axis in the hair bulb and in pilomatricoma. Am. J. Pathol. 2016, 186, 1036–1043. [Google Scholar] [CrossRef] [PubMed]
- Wells, J.; Lee, B.; Cai, A.Q.; Karapetyan, A.; Lee, W.J.; Rugg, E.; Sinha, S.; Nie, Q.; Dai, X. Ovol2 suppresses cell cycling and terminal differentiation of keratinocytes by directly repressing c-Myc and Notch1. J. Biol. Chem. 2009, 284, 29125–29135. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nair, M.; Teng, A.; Bilanchone, V.; Agrawal, A.; Li, B.; Dai, X. Ovol1 regulates the growth arrest of embryonic epidermal progenitor cells and represses c-myc transcription. J. Cell Biol. 2006, 173, 253–264. [Google Scholar] [CrossRef]
- Melnik, B.C. The potential role of impaired Notch signalling in atopic dermatitis. Acta Derm. Venereol. 2015, 95, 5–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lopez, R.G.; Garcia-Silva, S.; Moore, S.J.; Bereshchenko, O.; Martinez-Cruz, A.B.; Ermakova, O.; Kurz, E.; Paramio, J.M.; Nerlov, C. C/EBPalpha and beta couple interfollicular keratinocyte proliferation arrest to commitment and terminal differentiation. Nat. Cell Biol. 2009, 11, 1181–1190. [Google Scholar] [CrossRef] [PubMed]
- House, J.S.; Zhu, S.; Ranjan, R.; Linder, K.; Smart, R.C. C/EBPalpha and C/EBPbeta are required for Sebocyte differentiation and stratified squamous differentiation in adult mouse skin. PLoS ONE 2010, 5, e9837. [Google Scholar] [CrossRef] [Green Version]
- Yan, Y.; Furumura, M.; Numata, S.; Teye, K.; Karashima, T.; Ohyama, B.; Tanida, N.; Hashimoto, T. Various peroxisome proliferator-activated receptor (PPAR)-γ agonists differently induce differentiation of cultured human keratinocytes. Exp. Dermatol. 2015, 24, 62–65. [Google Scholar] [CrossRef] [PubMed]
- Yang, R.; Chowdhury, S.; Choudhary, V.; Chen, X.; Bollag, W.B. Keratinocyte aquaporin-3 expression induced by histone deacetylase inhibitors is mediated in part by peroxisome proliferator-activated receptors (PPARs). Exp. Dermatol. 2020, 29, 380–386. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Furue, M. Regulation of filaggrin, loricrin, and involucrin by IL-4, IL-13, IL-17A, IL-22, AHR, and NRF2: Pathogenic implications in atopic dermatitis. Int. J. Mol. Sci. 2020, 21, 5382. [Google Scholar] [CrossRef] [PubMed]
- Furue, M. Regulation of skin barrier function via competition between AHR axis versus IL-13/IL-4-JAK-STAT6/STAT3 axis: Pathogenic and therapeutic implications in atopic dermatitis. J. Clin. Med. 2020, 9, 3741. [Google Scholar] [CrossRef]
- Furue, K.; Ito, T.; Tsuji, G.; Ulzii, D.; Vu, Y.H.; Kido-Nakahara, M.; Nakahara, T.; Furue, M. The IL-13-OVOL1-FLG axis in atopic dermatitis. Immunology 2019, 158, 281–286. [Google Scholar] [CrossRef]
- Naher, L.; Kiyoshima, T.; Kobayashi, I.; Wada, H.; Nagata, K.; Fujiwara, H.; Ookuma, Y.F.; Ozeki, S.; Nakamura, S.; Sakai, H. STAT3 signal transduction through interleukin-22 in oral squamous cell carcinoma. Int. J. Oncol. 2012, 41, 1577–1586. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swindell, W.R.; Bojanowski, K.; Chaudhuri, R.K. A zingerone analog, acetyl zingerone, bolsters matrisome synthesis, inhibits matrix metallopeptidases, and represses IL-17A target gene expression. J. Investig. Dermatol. 2020, 140, 602–614. [Google Scholar] [CrossRef]
- Chiricozzi, A.; Nograles, K.E.; Johnson-Huang, L.M.; Fuentes-Duculan, J.; Cardinale, I.; Bonifacio, K.M.; Gulati, N.; Mitsui, H.; Guttman-Yassky, E.; Suárez-Fariñas, M.; et al. IL-17 induces an expanded range of downstream genes in reconstituted human epidermis model. PLoS ONE 2014, 9, e90284. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di, T.; Zhai, C.; Zhao, J.; Wang, Y.; Chen, Z.; Li, P. Taxifolin inhibits keratinocyte proliferation and ameliorates imiquimod-induced psoriasis-like mouse model via regulating cytoplasmic phospholipase A2 and PPAR-γ pathway. Int. Immunopharmacol. 2021, 99, 107900. [Google Scholar] [CrossRef]
- Lee, J.; Kim, H.J.; Yi, J.Y. A secretome analysis reveals that PPARα is upregulated by fractionated-dose γ-irradiation in three-dimensional keratinocyte cultures. Biochem. Biophys. Res. Commun. 2017, 482, 270–276. [Google Scholar] [CrossRef] [PubMed]
- Furue, M.; Hashimoto-Hachiya, A.; Tsuji, G. Antioxidative phytochemicals accelerate epidermal terminal differentiation via the AHR-OVOL1 pathway: Implications for atopic dermatitis. Acta Derm. Venereol. 2018, 98, 918–923. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Furue, M.; Uchi, H.; Mitoma, C.; Hashimoto-Hachiya, A.; Tanaka, Y.; Ito, T.; Tsuji, G. Implications of tryptophan photoproduct FICZ in oxidative stress and terminal differentiation of keratinocytes. G. Ital. Dermatol. Venereol. 2019, 154, 37–41. [Google Scholar] [CrossRef]
- Montero-Vilchez, T.; Segura-Fernández-Nogueras, M.V.; Pérez-Rodríguez, I.; Soler-Gongora, M.; Martinez-Lopez, A.; Fernández-González, A.; Molina-Leyva, A.; Arias-Santiago, S. Skin barrier function in psoriasis and atopic dermatitis: Transepidermal water loss and temperature as useful tools to assess disease severity. J. Clin. Med. 2021, 10, 359. [Google Scholar] [CrossRef]
- Maroto-Morales, D.; Montero-Vilchez, T.; Arias-Santiago, S. Study of skin barrier function in psoriasis: The impact of emollients. Life 2021, 11, 651. [Google Scholar] [CrossRef]
- Katoh, N.; Ohya, Y.; Ikeda, M.; Ebihara, T.; Katayama, I.; Saeki, H.; Shimojo, N.; Tanaka, A.; Nakahara, T.; Nagao, M.; et al. Japanese guidelines for atopic dermatitis 2020. Allergol. Int. 2020, 69, 356–369. [Google Scholar] [CrossRef] [PubMed]
- Salvati, L.; Cosmi, L.; Annunziato, F. From emollients to biologicals: Targeting atopic dermatitis. Int. J. Mol. Sci. 2021, 22, 10381. [Google Scholar] [CrossRef]
- Lueangarun, S.; Tragulplaingam, P.; Sugkraroek, S.; Tempark, T. The 24-hr, 28-day, and 7-day post-moisturizing efficacy of ceramides 1, 3, 6-II containing moisturizing cream compared with hydrophilic cream on skin dryness and barrier disruption in senile xerosis treatment. Dermatol. Ther. 2019, 32, e13090. [Google Scholar] [CrossRef] [PubMed]
- Hebert, A.A.; Rippke, F.; Weber, T.M.; Nicol, N.H. Efficacy of nonprescription moisturizers for atopic dermatitis: An updated review of clinical evidence. Am. J. Clin. Dermatol. 2020, 21, 641–655. [Google Scholar] [CrossRef] [PubMed]
- Miyamoto, K.; Inoue, Y.; Hsueh, K.; Liang, Z.; Yan, X.; Yoshii, T.; Furue, M. Characterization of comprehensive appearances of skin ageing: An 11-year longitudinal study on facial skin ageing in Japanese females at Akita. J. Dermatol. Sci. 2011, 64, 229–236. [Google Scholar] [CrossRef]
- Miyamoto, K.; Dissanayake, B.; Omotezako, T.; Takemura, M.; Tsuji, G.; Furue, M. Daily fluctuation of facial pore area, roughness and redness among young Japanese women; Beneficial effects of Galactomyces ferment filtrate containing antioxidative skin care formula. J. Clin. Med. 2021, 10, 2502. [Google Scholar] [CrossRef] [PubMed]
- Iino, H.; Fujii, M.; Fujino, M.; Kohara, S.; Hashizaki, K.; Kira, H.; Koizumi, N.; Watanabe, Y.; Utoguchi, N. Influence of characteristics of oily vehicle on skin penetration of ufenamate. Biol. Pharm. Bull. 2017, 40, 220–226. [Google Scholar] [CrossRef] [Green Version]
- Harding, C.R.; Watkinson, A.; Rawlings, A.V.; Scott, I.R. Dry skin, moisturization and corneodesmolysis. Int. J. Cosmet. Sci. 2000, 22, 21–52. [Google Scholar] [CrossRef] [PubMed]
- Loden, M. Role of topical emollients and moisturizers in the treatment of dry skin barrier disorders. Am. J. Clin. Dermatol. 2003, 4, 771–788. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.; Bajor, J.; Moaddel, T.; Subramanian, V.; Lee, J.M.; Marrero, D.; Rocha, S.; Tharp, M.D. Principles of moisturizer product design. J. Drugs Dermatol. 2019, 18, s89–s95. [Google Scholar] [PubMed]
- Elias, P.M.; Wakefield, J.S.; Man, M.Q. Moisturizers versus current and next-generation barrier repair therapy for the management of atopic dermatitis. Skin Pharmacol. Physiol. 2019, 32, 1–7. [Google Scholar] [CrossRef]
- Schleusener, J.; Salazar, A.; von Hagen, J.; Lademann, J.; Darvin, M.E. Retaining skin barrier function properties of the stratum corneum with components of the natural moisturizing factor—A randomized, placebo-controlled double-blind in vivo study. Molecules 2021, 26, 1649. [Google Scholar] [CrossRef]
- Spada, F.; Harrison, I.P.; Barnes, T.M.; Greive, K.A.; Daniels, D.; Townley, J.P.; Mostafa, N.; Fong, A.T.; Tong, P.L.; Shumack, S. A daily regimen of a ceramide-dominant moisturizing cream and cleanser restores the skin permeability barrier in adults with moderate eczema: A randomized trial. Dermatol. Ther. 2021, 34, e14970. [Google Scholar] [CrossRef] [PubMed]
- Miyamoto, K.; Munakata, Y.; Yan, X.; Tsuji, G.; Furue, M. Enhanced fluctuations in facial pore size, redness, and TEWL caused by mask usage are normalized by the application of a moisturizer. J. Clin. Med. 2022, 11, 2121. [Google Scholar] [CrossRef]
- Takei, K.; Mitoma, C.; Hashimoto-Hachiya, A.; Takahara, M.; Tsuji, G.; Nakahara, T.; Furue, M. Galactomyces fermentation filtrate prevents T helper 2-mediated reduction of filaggrin in an aryl hydrocarbon receptor-dependent manner. Clin. Exp. Dermatol. 2015, 40, 786–793. [Google Scholar] [CrossRef]
- Hashimoto-Hachiya, A.; Tsuji, G.; Furue, M. Antioxidants cinnamaldehyde and Galactomyces fermentation filtrate downregulate senescence marker CDKN2A/p16INK4A via NRF2 activation in keratinocytes. J. Dermatol. Sci. 2019, 96, 53–56. [Google Scholar] [CrossRef] [Green Version]
- Howell, M.D.; Kim, B.E.; Gao, P.; Grant, A.V.; Boguniewicz, M.; Debenedetto, A.; Schneider, L.; Beck, L.A.; Barnes, K.C.; Leung, D.Y. Cytokine modulation of atopic dermatitis filaggrin skin expression. J. Allergy Clin. Immunol. 2007, 120, 150–155. [Google Scholar] [CrossRef] [Green Version]
- Kobayashi, J.; Inai, T.; Morita, K.; Moroi, Y.; Urabe, K.; Shibata, Y.; Furue, M. Reciprocal regulation of permeability through a cultured keratinocyte sheet by IFN-gamma and IL-4. Cytokine 2004, 28, 186–189. [Google Scholar] [CrossRef] [PubMed]
- Dębińska, A. New treatments for atopic dermatitis targeting skin barrier repair via the regulation of FLG expression. J. Clin. Med. 2021, 10, 2506. [Google Scholar] [CrossRef]
- Doi, K.; Mitoma, C.; Nakahara, T.; Uchi, H.; Hashimoto-Hachiya, A.; Takahara, M.; Tsuji, G.; Nakahara, T.; Furue, M. Antioxidant Houttuynia cordata extract upregulates filaggrin expression in an aryl hydrocarbon-dependent manner. Fukuoka Igaku Zasshi 2014, 105, 205–213. [Google Scholar] [PubMed]
- Nakahara, T.; Mitoma, C.; Hashimoto-Hachiya, A.; Takahara, M.; Tsuji, G.; Uchi, H.; Yan, X.; Hachisuka, J.; Chiba, T.; Esaki, H.; et al. Antioxidant Opuntia ficus-indica extract activates AHR-NRF2 signaling and upregulates filaggrin and loricrin expression in human keratinocytes. J. Med. Food 2015, 18, 1143–1149. [Google Scholar] [CrossRef]
- Hirano, A.; Goto, M.; Mitsui, T.; Hashimoto-Hachiya, A.; Tsuji, G.; Furue, M. Antioxidant Artemisia princeps extract enhances the expression of filaggrin and loricrin via the AHR/OVOL1 pathway. Int. J. Mol. Sci. 2017, 18, 1948. [Google Scholar] [CrossRef]
- van den Bogaard, E.H.; Bergboer, J.G.; Vonk-Bergers, M.; van Vlijmen-Willems, I.M.; Hato, S.V.; van der Valk, P.G.; Schröder, J.M.; Joosten, I.; Zeeuwen, P.L.; Schalkwijk, J. Coal tar induces AHR-dependent skin barrier repair in atopic dermatitis. J. Clin. Investig. 2013, 123, 917–927. [Google Scholar] [CrossRef] [Green Version]
- Takei, K.; Mitoma, C.; Hashimoto-Hachiya, A.; Uchi, H.; Takahara, M.; Tsuji, G.; Kido-Nakahara, M.; Nakahara, T.; Furue, M. Antioxidant soybean tar Glyteer rescues T-helper-mediated downregulation of filaggrin expression via aryl hydrocarbon receptor. J. Dermatol. 2015, 42, 171–180. [Google Scholar] [CrossRef] [Green Version]
- Smith, S.H.; Jayawickreme, C.; Rickard, D.J.; Nicodeme, E.; Bui, T.; Simmons, C.; Coquery, C.M.; Neil, J.; Pryor, W.M.; Mayhew, D.; et al. Tapinarof is a natural AhR agonist that resolves skin inflammation in mice and humans. J. Investig. Dermatol. 2017, 137, 2110–2119. [Google Scholar] [CrossRef] [Green Version]
- Furue, M.; Nakahara, T. Revival of AHR agonist for the treatment of atopic dermatitis: Tapinarof. Curr. Treat. Options Allergy 2020, 7, 414–421. [Google Scholar] [CrossRef]
- Paller, A.S.; Stein Gold, L.; Soung, J.; Tallman, A.M.; Rubenstein, D.S.; Gooderham, M. Efficacy and patient-reported outcomes from a phase 2b, randomized clinical trial of tapinarof cream for the treatment of adolescents and adults with atopic dermatitis. J. Am. Acad. Dermatol. 2021, 84, 632–638. [Google Scholar] [CrossRef]
- Lebwohl, M.G.; Stein Gold, L.; Strober, B.; Papp, K.A.; Armstrong, A.W.; Bagel, J.; Kircik, L.; Ehst, B.; Hong, H.C.; Soung, J.; et al. Phase 3 trials of tapinarof cream for plaque psoriasis. N. Engl. J. Med. 2021, 385, 2219–2229. [Google Scholar] [CrossRef]
- Bissonnette, R.; Stein Gold, L.; Rubenstein, D.S.; Tallman, A.M.; Armstrong, A. Tapinarof in the treatment of psoriasis: A review of the unique mechanism of action of a novel therapeutic aryl hydrocarbon receptor-modulating agent. J. Am. Acad. Dermatol. 2021, 84, 1059–1067. [Google Scholar] [CrossRef]
- Chen, J.; Liu, Y.; Zhao, Z.; Qiu, J. Oxidative stress in the skin: Impact and related protection. Int. J. Cosmet. Sci. 2021, 43, 495–509. [Google Scholar] [CrossRef]
- Tsuji, G.; Takahara, M.; Uchi, H.; Takeuchi, S.; Mitoma, C.; Moroi, Y.; Furue, M. An environmental contaminant, benzo(a)pyrene, induces oxidative stress-mediated interleukin-8 production in human keratinocytes via the aryl hydrocarbon receptor signaling pathway. J. Dermatol. Sci. 2011, 62, 42–49. [Google Scholar] [CrossRef]
- Takei, K.; Hashimoto-Hachiya, A.; Takahara, M.; Tsuji, G.; Nakahara, T.; Furue, M. Cynaropicrin attenuates UVB-induced oxidative stress via the AhR-Nrf2-Nqo1 pathway. Toxicol. Lett. 2015, 234, 74–80. [Google Scholar] [CrossRef]
- Bak, D.H.; Lee, E.; Lee, B.C.; Choi, M.J.; Kwon, T.R.; Hong, J.; Mun, S.K.; Lee, K.; Kim, S.; Na, J.; et al. Therapeutic potential of topically administered γ-AlOOH on 2,4-dinitrochlorobenzene-induced atopic dermatitis-like lesions in Balb/c mice. Exp. Dermatol. 2019, 28, 169–176. [Google Scholar] [CrossRef]
- Fuyuno, Y.; Uchi, H.; Yasumatsu, M.; Morino-Koga, S.; Tanaka, Y.; Mitoma, C.; Furue, M. Perillaldehyde inhibits AHR signaling and activates NRF2 antioxidant pathway in human keratinocytes. Oxid. Med. Cell Longev. 2018, 2018, 9524657. [Google Scholar] [CrossRef]
- Walshe, J.; Serewko-Auret, M.M.; Teakle, N.; Cameron, S.; Minto, K.; Smith, L.; Burcham, P.C.; Russell, T.; Strutton, G.; Griffin, A.; et al. Inactivation of glutathione peroxidase activity contributes to UV-induced squamous cell carcinoma formation. Cancer Res. 2007, 67, 4751–4758. [Google Scholar] [CrossRef] [Green Version]
- Takei, K.; Takahara, M.; Hachiya, A.; Inoue, K.; Yan, X.; Tsuji, G.; Nakahara, T.; Furue, M. Galactomyces ferment filtrate (Pitera) inhibits UVB-induced ROS production by Ahr/NRrf2/Nqo1 signaling, Aesthet. Dermatol. 2014, 24, 342–350. (In Japanese) [Google Scholar]
- Cooper, J.K.W.; Koshoffer, A.; Kadekaro, A.L.; Hakozaki, T.; Boissy, R.E. Galactomyces ferment filtrate suppresses reactive oxygen species generation and promotes cellular redox balance in human melanocytes via Nrf2-ARE pathway. J. Clin. Cosmet. Dermatol. 2019, 3, 1. [Google Scholar] [CrossRef] [Green Version]
- Mitamura, Y.; Murai, M.; Mitoma, C.; Furue, M. NRF2 activation inhibits both TGF-β1- and IL-13-mediated periostin expression in fibroblasts: Benefit of cinnamaldehyde for antifibrotic treatment. Oxid. Med. Cell Longev. 2018, 2018, 2475047. [Google Scholar] [CrossRef] [Green Version]
- Schäfer, M.; Farwanah, H.; Willrodt, A.H.; Huebner, A.J.; Sandhoff, K.; Roop, D.; Hohl, D.; Bloch, W.; Werner, S. Nrf2 links epidermal barrier function with antioxidant defense. EMBO Mol. Med. 2012, 4, 364–379. [Google Scholar] [CrossRef]
- Skeate, J.G.; Porras, T.B.; Woodham, A.W.; Jang, J.K.; Taylor, J.R.; Brand, H.E.; Kelly, T.J.; Jung, J.U.; Da Silva, D.M.; Yuan, W.; et al. Herpes simplex virus downregulation of secretory leukocyte protease inhibitor enhances human papillomavirus type 16 infection. J. Gen. Virol. 2016, 97, 422–434. [Google Scholar] [CrossRef]
- Nakajima, A.; Sakae, N.; Yan, X.; Hakozaki, T.; Zhao, W.; Laughlin, T.; Furue, M. Transcriptomic analysis of human keratinocytes treated with Galactomyces ferment filtrate, a beneficial cosmetic ingredient. J. Clin. Med. 2022, 11, 4645. [Google Scholar] [CrossRef]
- Walker, K.A.; Basisty, N.; Wilson, D.M., 3rd; Ferrucci, L. Connecting aging biology and inflammation in the omics era. J. Clin. Investig. 2022, 132, e158448. [Google Scholar] [CrossRef]
- Abbadie, C.; Pluquet, O.; Pourtier, A. Epithelial cell senescence: An adaptive response to pre-carcinogenic stresses? Cell. Mol. Life Sci. 2017, 74, 4471–4509. [Google Scholar] [CrossRef]
- Adamus, J.; Aho, S.; Meldrum, H.; Bosko, C.; Lee, J.M. p16INK4A influences the aging phenotype in the living skin equivalent. J. Investig. Dermatol. 2014, 134, 1131–1133. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.Y.; Souroullas, G.P.; Diekman, B.O.; Krishnamurthy, J.; Hall, B.M.; Sorrentino, J.A.; Parker, J.S.; Sessions, G.A.; Gudkov, A.V.; Sharpless, N.E. Cells exhibiting strong p16INK4a promoter activation in vivo display features of senescence. Proc. Natl. Acad. Sci. USA 2019, 116, 2603–2611. [Google Scholar] [CrossRef] [Green Version]
- Tsai, H.H.; Chen, Y.C.; Lee, W.R.; Hu, C.H.; Hakozaki, T.; Yoshii, T.; Shen, S.C. Inhibition of inflammatory nitric oxide production and epidermis damages by Saccharomycopsis ferment filtrate. J. Dermatol Sci. 2006, 42, 249–257. [Google Scholar] [CrossRef]
- Tsuji, G.; Takahara, M.; Uchi, H.; Matsuda, T.; Chiba, T.; Takeuchi, S.; Yasukawa, F.; Moroi, Y.; Furue, M. Identification of ketoconazole as an AhR-Nrf2 activator in cultured human keratinocytes: The basis of its anti-inflammatory effect. J. Investig. Dermatol. 2012, 132, 59–68. [Google Scholar] [CrossRef] [Green Version]
- Haarmann-Stemmann, T.; Abel, J.; Fritsche, E.; Krutmann, J. The AhR-Nrf2 pathway in keratinocytes: On the road to chemoprevention? J. Investig. Dermatol. 2012, 132, 7–9. [Google Scholar] [CrossRef] [Green Version]
- Hvid, M.; Johansen, C.; Deleuran, B.; Kemp, K.; Deleuran, M.; Vestergaard, C. Regulation of caspase 14 expression in keratinocytes by inflammatory cytokines—A possible link between reduced skin barrier function and inflammation? Exp. Dermatol. 2011, 20, 633–636. [Google Scholar] [CrossRef]
- Denecker, G.; Hoste, E.; Gilbert, B.; Hochepied, T.; Ovaere, P.; Lippens, S.; Van den Broecke, C.; Van Damme, P.; D’Herde, K.; Hachem, J.P.; et al. Caspase-14 protects against epidermal UVB photodamage and water loss. Nat. Cell Biol. 2007, 9, 666–674. [Google Scholar] [CrossRef]
- Kataoka, S.; Hattori, K.; Date, A.; Tamura, H. Human keratinocyte caspase-14 expression is altered in human epidermal 3D models by dexamethasone and by natural products used in cosmetics. Arch. Dermatol. Res. 2013, 305, 683–689. [Google Scholar] [CrossRef]
- Ding, W.; Fan, L.; Tian, Y.; He, C. Study of the protective effects of cosmetic ingredients on the skin barrier, based on the expression of barrier-related genes and cytokines. Mol. Biol. Rep. 2022, 49, 989–995. [Google Scholar] [CrossRef]
- Chamcheu, J.C.; Siddiqui, I.A.; Adhami, V.M.; Esnault, S.; Bharali, D.J.; Babatunde, A.S.; Adame, S.; Massey, R.J.; Wood, G.S.; Longley, B.J.; et al. Chitosan-based nanoformulated (-)-epigallocatechin-3-gallate (EGCG) modulates human keratinocyte-induced responses and alleviates imiquimod-induced murine psoriasiform dermatitis. Int. J. Nanomed. 2018, 13, 4189–4206. [Google Scholar] [CrossRef] [Green Version]
- Lee, Y.; Lim, H.W.; Ryu, I.W.; Huang, Y.H.; Park, M.; Chi, Y.; Lim, C.J. Anti-inflammatory, barrier-protective, and antiwrinkle properties of Agastache rugosa Kuntze in human epidermal keratinocytes. Biomed. Res. Int. 2020, 2020, 1759067. [Google Scholar] [CrossRef]
- Denecker, G.; Ovaere, P.; Vandenabeele, P.; Declercq, W. Caspase-14 reveals its secrets. J. Cell Biol. 2008, 180, 451–458. [Google Scholar] [CrossRef] [Green Version]
- Markiewicz, A.; Sigorski, D.; Markiewicz, M.; Owczarczyk-Saczonek, A.; Placek, W. Caspase-14—From biomolecular basics to clinical approach. A review of available data. Int. J. Mol. Sci. 2021, 22, 5575. [Google Scholar] [CrossRef]
- Kirschner, N.; Houdek, P.; Fromm, M.; Moll, I.; Brandner, J.M. Tight junctions form a barrier in human epidermis. Eur. J. Cell Biol. 2010, 89, 839–842. [Google Scholar] [CrossRef]
- Yuki, T.; Haratake, A.; Koishikawa, H.; Morita, K.; Miyachi, Y.; Inoue, S. Tight junction proteins in keratinocytes: Localization and contribution to barrier function. Exp. Dermatol. 2007, 16, 324–330. [Google Scholar] [CrossRef]
- Furuse, M.; Hata, M.; Furuse, K.; Yoshida, Y.; Haratake, A.; Sugitani, Y.; Noda, T.; Kubo, A.; Tsukita, S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: A lesson from claudin-1-deficient mice. J. Cell Biol. 2002, 156, 1099–1111. [Google Scholar] [CrossRef]
- Wong, W.R.; Hakozaki, T.; Yoshii, T.; Chen, T.Y.; Pan, J.H.S. Up-regulation of tight junction-related proteins and increase of human epidermal keratinocytes barrier function by Saccharomycosis ferment filtrate. J. Cosm. Dermatol. Sci. Appl. 2011, 1, 15–24. [Google Scholar]
- Bergmann, S.; von Buenau, B.; Vidal-Y-Sy, S.; Haftek, M.; Wladykowski, E.; Houdek, P.; Lezius, S.; Duplan, H.; Bäsler, K.; Dähnhardt-Pfeiffer, S.; et al. Claudin-1 decrease impacts epidermal barrier function in atopic dermatitis lesions dose-dependently. Sci. Rep. 2020, 10, 2024. [Google Scholar] [CrossRef] [Green Version]
- Hadj-Rabia, S.; Baala, L.; Vabres, P.; Hamel-Teillac, D.; Jacquemin, E.; Fabre, M.; Lyonnet, S.; De Prost, Y.; Munnich, A.; Hadchouel, M.; et al. Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: A tight junction disease. Gastroenterology 2004, 127, 1386–1390. [Google Scholar] [CrossRef]
- Macleod, T.; Berekmeri, A.; Bridgewood, C.; Stacey, M.; McGonagle, D.; Wittmann, M. The immunological impact of IL-1 family cytokines on the epidermal barrier. Front. Immunol. 2021, 12, 808012. [Google Scholar] [CrossRef]
- Li, B.; Tsoi, L.C.; Swindell, W.R.; Gudjonsson, J.E.; Tejasvi, T.; Johnston, A.; Ding, J.; Stuart, P.E.; Xing, X.; Kochkodan, J.J.; et al. Transcriptome analysis of psoriasis in a large case-control sample: RNA-seq provides insights into disease mechanisms. J. Investig. Dermatol. 2014, 134, 1828–1838. [Google Scholar] [CrossRef] [Green Version]
- Teng, X.; Hu, Z.; Wei, X.; Wang, Z.; Guan, T.; Liu, N.; Liu, X.; Ye, N.; Deng, G.; Luo, C.; et al. IL-37 ameliorates the inflammatory process in psoriasis by suppressing proinflammatory cytokine production. J. Immunol. 2014, 192, 1815–1823. [Google Scholar] [CrossRef] [Green Version]
- Dickel, H.; Gambichler, T.; Kamphowe, J.; Altmeyer, P.; Skrygan, M. Standardized tape stripping prior to patch testing induces upregulation of Hsp90, Hsp70, IL-33, TNF-α and IL-8/CXCL8 mRNA: New insights into the involvement of ‘alarmins’. Contact Dermat. 2010, 63, 215–222. [Google Scholar] [CrossRef]
- Halim, T.Y.F.; Rana, B.M.J.; Walker, J.A.; Kerscher, B.; Knolle, M.D.; Jolin, H.E.; Serrao, E.M.; Haim-Vilmovsky, L.; Teichmann, S.A.; Rodewald, H.R.; et al. Tissue-restricted adaptive type 2 immunity is orchestrated by expression of the costimulatory molecule OX40L on group 2 innate lymphoid cells. Immunity 2018, 48, 1195–1207. [Google Scholar] [CrossRef] [Green Version]
- Nechama, M.; Kwon, J.; Wei, S.; Kyi, A.T.; Welner, R.S.; Ben-Dov, I.Z.; Arredouani, M.S.; Asara, J.M.; Chen, C.H.; Tsai, C.Y.; et al. The IL-33-PIN1-IRAK-M axis is critical for type 2 immunity in IL-33-induced allergic airway inflammation. Nat. Commun. 2018, 9, 1603. [Google Scholar] [CrossRef] [Green Version]
- Jang, Y.H.; Choi, J.K.; Jin, M.; Choi, Y.A.; Ryoo, Z.Y.; Lee, H.S.; Park, P.H.; Kim, S.U.; Kwon, T.K.; Jang, M.H.; et al. House dust mite increases pro-Th2 cytokines IL-25 and IL-33 via the activation of TLR1/6 signaling. J. Investig. Dermatol. 2017, 137, 2354–2361. [Google Scholar] [CrossRef] [Green Version]
- Cayrol, C.; Duval, A.; Schmitt, P.; Roga, S.; Camus, M.; Stella, A.; Burlet-Schiltz, O.; Gonzalez-de-Peredo, A.; Girard, J.P. Environmental allergens induce allergic inflammation through proteolytic maturation of IL-33. Nat. Immunol. 2018, 19, 375–385. [Google Scholar] [CrossRef]
- Nold, M.F.; Nold-Petry, C.A.; Zepp, J.A.; Palmer, B.E.; Bufler, P.; Dinarello, C.A. IL-37 is a fundamental inhibitor of innate immunity. Nat. Immunol. 2010, 11, 1014–1022. [Google Scholar] [CrossRef] [Green Version]
- Dinarello, C.A.; Bufler, P. Interleukin-37. Semin. Immunol. 2013, 25, 466–468. [Google Scholar] [CrossRef]
- Dinarello, C.A. The IL-1 family of cytokines and receptors in rheumatic diseases. Nat. Rev. Rheumatol. 2019, 15, 612–632. [Google Scholar] [CrossRef]
- Newman, T.L.; Tuzun, E.; Morrison, V.A.; Hayden, K.E.; Ventura, M.; McGrath, S.D.; Rocchi, M.; Eichler, E.E. A genome-wide survey of structural variation between human and chimpanzee. Genome Res. 2005, 15, 1344–1356. [Google Scholar] [CrossRef] [Green Version]
- Dinarello, C.A.; Nold-Petry, C.; Nold, M.; Fujita, M.; Li, S.; Kim, S.; Bufler, P. Suppression of innate inflammation and immunity by interleukin-37. Eur. J. Immunol. 2016, 46, 1067–1081. [Google Scholar] [CrossRef] [Green Version]
- Tsuji, G.; Hashimoto-Hachiya, A.; Matsuda-Taniguchi, T.; Takai-Yumine, A.; Takemura, M.; Furue, M.; Nakahara, T. Natural compounds tapinarof and Galactomyces ferment filtrate downregulate IL-33 via the AHR/IL-37 axis in human keratinocytes. Front. Immunol. 2022, 13, 745997. [Google Scholar] [CrossRef]
- Tsuji, G.; Hashimoto-Hachiya, A.; Yen, V.H.; Miake, S.; Takemura, M.; Mitamura, Y.; Ito, T.; Murata, M.; Furue, M.; Nakahara, T. Aryl hydrocarbon receptor activation downregulates IL-33 expression in keratinocytes via Ovo-Like 1. J. Clin. Med. 2020, 9, 891. [Google Scholar] [CrossRef] [Green Version]
- Ryu, W.I.; Lee, H.; Bae, H.C.; Jeon, J.; Ryu, H.J.; Kim, J.; Kim, J.H.; Son, J.W.; Kim, J.; Imai, Y.; et al. IL-33 down-regulates CLDN1 expression through the ERK/STAT3 pathway in keratinocytes. J. Dermatol. Sci. 2018, 90, 313–322. [Google Scholar] [CrossRef] [Green Version]
- Lu, J.; Chatterjee, M.; Schmid, H.; Beck, S.; Gawaz, M. CXCL14 as an emerging immune and inflammatory modulator. J. Inflamm. 2016, 13, 1. [Google Scholar] [CrossRef] [Green Version]
- Hasegawa, T.; Feng, Z.; Yan, Z.; Ngo, K.H.; Hosoi, J.; Demehri, S. Reduction in human epidermal Langerhans cells with age is associated with decline in CXCL14-mediated recruitment of CD14+ monocytes. J. Investig. Dermatol. 2020, 140, 1327–1334. [Google Scholar] [CrossRef]
- Kawamura, T.; Tomari, H.; Onoyama, I.; Araki, H.; Yasunaga, M.; Lin, C.; Kawamura, K.; Yokota, N.; Yoshida, S.; Yagi, H.; et al. Identification of genes associated with endometrial cell ageing. Mol. Hum. Reprod. 2021, 27, gaaa078. [Google Scholar] [CrossRef]
- Sturmlechner, I.; Zhang, C.; Sine, C.C.; van Deursen, E.J.; Jeganathan, K.B.; Hamada, N.; Grasic, J.; Friedman, D.; Stutchman, J.T.; Can, I.; et al. p21 produces a bioactive secretome that places stressed cells under immunosurveillance. Science 2021, 374, eabb3420. [Google Scholar] [CrossRef]
- Engelhart, K.; El Hindi, T.; Biesalski, H.K.; Pfitzner, I. In vitro reproduction of clinical hallmarks of eczematous dermatitis in organotypic skin models. Arch. Dermatol. Res. 2005, 297, 1–9. [Google Scholar] [CrossRef]
- Jett, J.E.; McLaughlin, M.; Lee, M.S.; Parish, L.C.; DuBois, J.; Raoof, T.J.; Tabolt, G.; Wilson, T.; Somerville, M.C.; DellaMaestra, W.; et al. Tapinarof cream 1% for extensive plaque psoriasis: A maximal use trial on safety, tolerability, and pharmacokinetics. Am. J. Clin. Dermatol. 2022, 23, 83–91. [Google Scholar] [CrossRef]
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Yan, X.; Tsuji, G.; Hashimoto-Hachiya, A.; Furue, M. Galactomyces Ferment Filtrate Potentiates an Anti-Inflammaging System in Keratinocytes. J. Clin. Med. 2022, 11, 6338. https://doi.org/10.3390/jcm11216338
Yan X, Tsuji G, Hashimoto-Hachiya A, Furue M. Galactomyces Ferment Filtrate Potentiates an Anti-Inflammaging System in Keratinocytes. Journal of Clinical Medicine. 2022; 11(21):6338. https://doi.org/10.3390/jcm11216338
Chicago/Turabian StyleYan, Xianghong, Gaku Tsuji, Akiko Hashimoto-Hachiya, and Masutaka Furue. 2022. "Galactomyces Ferment Filtrate Potentiates an Anti-Inflammaging System in Keratinocytes" Journal of Clinical Medicine 11, no. 21: 6338. https://doi.org/10.3390/jcm11216338
APA StyleYan, X., Tsuji, G., Hashimoto-Hachiya, A., & Furue, M. (2022). Galactomyces Ferment Filtrate Potentiates an Anti-Inflammaging System in Keratinocytes. Journal of Clinical Medicine, 11(21), 6338. https://doi.org/10.3390/jcm11216338