Attenuation Effect of Radiofrequency Irradiation on UV-B-Induced Skin Pigmentation by Decreasing Melanin Synthesis and through Upregulation of Heat Shock Protein 70
Abstract
:1. Introduction
2. Results
2.1. RF Decreased Melanin Accumulation in the UV-B Radiated Skin
2.2. RF Decreased Melanin Synthesis and Formation of Stage IV Melanosome
2.3. RF Increased the Expression of HSP70 and Decreased the Expression of p53, MC1R, and MITF
2.4. HSP70 Is Involved in Decreasing Melanin Synthesis
3. Discussion
4. Materials and Methods
4.1. Skin Pigmentation Model Induced UV-B Exposure and RF Application
- (1)
- Control (no exposure to UV-B with no irradiated RF).
- (2)
- UV-B (exposure to UV-B at 200 mJ/cm2 with no irradiated RF).
- (3)
- UV-B/RF 5 W/50 ms (exposure to UV-B/irradiated RF at 2 MHz, 5 Watt for 50 ms).
- (4)
- UV-B/RF 5 W/100 ms (exposure to UV-B/irradiated RF at 2 MHz, 5 Watt for 100 ms).
- (5)
- UV-B/RF 5 W/150 ms (exposure to UV-B/irradiated RF at 2 MHz, 5 Watt for 150 ms).
- (6)
- UV-B/RF 10 W/50 ms (exposure to UV-B/irradiated RF at 2 MHz, 10 Watt for 50 ms).
- (7)
- UV-B/RF 10 W/100 ms (exposure to UV-B/irradiated RF at 2 MHz, 10 Watt for 100 ms).
- (8)
- UV-B/RF 10 W/150 ms (exposure to UV-B/irradiated RF at 2 MHz, 10 Watt for 150 ms).
- (9)
- UV-B/RF 15 W/50 ms (exposure to UV-B/irradiated RF at 2 MHz, 15 Watt for 50 ms).
- (10)
- UV-B/RF 15 W/100 ms (exposure to UV-B/irradiated RF at 2 MHz, 15 Watt for 100 ms).
- (11)
- UV-B/RF 15 W/150 ms (exposure to UV-B/irradiated RF at 2 MHz, 15 att for 150 ms).
4.2. RF Irradiation System
4.3. In Vitro Model and RF Irradiation
4.4. Overexpression and Silencing of HSP70 and Treatment of p53 Inhibitor to the HEMn
4.5. Measurement of Melanin Content in Cells
4.6. Sample Preparation
4.6.1. Extraction of RNA and cDNA Synthesis
4.6.2. Paraffin-Embedded Tissue Sectioning
4.7. Quantitative Real-Time Polymerase Chain Reaction
4.8. 3,3′-Diaminobenzidine Staining for Immunohistochemistry
4.9. Transmission Electron Microscopy
4.10. Fontana-Masson Staining
4.11. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
- Slominski, A.T.; Zmijewski, M.A.; Plonka, P.M.; Szaflarski, J.P.; Paus, R. How UV light touches the brain and endocrine system through skin, and why. Endocrinology 2018, 159, 1992–2007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Slominski, A.; Tobin, D.J.; Shibahara, S.; Wortsman, J. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 2004, 84, 1155–1228. [Google Scholar] [CrossRef]
- Slominski, A.; Zmijewski, M.A.; Pawelek, J. L-tyrosine and L-dihydroxyphenylalanine as hormone-like regulators of melanocyte functions. Pigment Cell Melanoma Res. 2012, 25, 14–27. [Google Scholar] [CrossRef] [Green Version]
- Murase, D.; Hachiya, A.; Amano, Y.; Ohuchi, A.; Kitahara, T.; Takema, Y. The essential role of p53 in hyperpigmentation of the skin via regulation of paracrine melanogenic cytokine receptor signaling. J. Biol. Chem. 2009, 284, 4343–4353. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosdahl, I.K.; Szabó, G. Mitotic activity of epidermal melanocytes in UV-irradiated mouse skin. J. Investig. Dermatol. 1978, 70, 143–148. [Google Scholar] [CrossRef] [Green Version]
- Imokawa, G.; Mishima, Y. Loss of melanogenic properties in tyrosinases induced by glucosylation inhibitors within malignant melanoma cells. Cancer Res. 1982, 42, 1994–2002. [Google Scholar] [PubMed]
- Mishima, Y.; Imokawa, G. Selective aberration and pigment loss in melanosomes of malignant melanoma cells in vitro by glycosylation inhibitors: Premelanosomes as glycoprotein. J. Investig. Dermatol. 1983, 81, 106–114. [Google Scholar] [CrossRef] [Green Version]
- Okazaki, K.; Uzuka, M.; Morikawa, F.; Toda, K.; Seiji, M. Transfer mechanism of melanosomes in epidermal cell culture. J. Investig. Dermatol. 1976, 67, 541–547. [Google Scholar] [CrossRef] [Green Version]
- Serre, C.; Busuttil, V.; Botto, J.M. Intrinsic and extrinsic regulation of human skin melanogenesis and pigmentation. Int. J. Cosmet. Sci. 2018, 40, 328–347. [Google Scholar] [CrossRef] [Green Version]
- Lo, J.A.; Fisher, D.E. The melanoma revolution: From UV carcinogenesis to a new era in therapeutics. Science 2014, 346, 945–949. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.J.; Fisher, D.E. Lighting a path to pigmentation: Mechanisms of MITF induction by UV. Pigment Cell Melanoma Res. 2010, 23, 741–745. [Google Scholar] [CrossRef]
- Pillaiyar, T.; Manickam, M.; Jung, S.H. Downregulation of melanogenesis: Drug discovery and therapeutic options. Drug Discov. Today 2017, 22, 282–298. [Google Scholar] [CrossRef]
- Elliott, R.J.; Szabo, M.; Wagner, M.J.; Kemp, E.H.; MacNeil, S.; Haycock, J.W. alpha-Melanocyte-stimulating hormone, MSH 11-13 KPV and adrenocorticotropic hormone signalling in human keratinocyte cells. J. Investig. Dermatol. 2004, 122, 1010–1019. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mountjoy, K.G.; Robbins, L.S.; Mortrud, M.T.; Cone, R.D. The cloning of a family of genes that encode the melanocortin receptors. Science 1992, 257, 1248–1251. [Google Scholar] [CrossRef]
- Theos, A.C.; Truschel, S.T.; Raposo, G.; Marks, M.S. The Silver locus product Pmel17/gp100/Silv/ME20: Controversial in name and in function. Pigment Cell Res. 2005, 18, 322–336. [Google Scholar] [CrossRef] [Green Version]
- Kushimoto, T.; Basrur, V.; Valencia, J.; Matsunaga, J.; Vieira, W.D.; Ferrans, V.J.; Muller, J.; Appella, E.; Hearing, V.J. A model for melanosome biogenesis based on the purification and analysis of early melanosomes. Proc. Natl. Acad. Sci. USA 2001, 98, 10698–10703. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raposo, G.; Tenza, D.; Murphy, D.M.; Berson, J.F.; Marks, M.S. Distinct protein sorting and localization to premelanosomes, melanosomes, and lysosomes in pigmented melanocytic cells. J. Cell Biol. 2001, 152, 809–824. [Google Scholar] [CrossRef] [Green Version]
- Theos, A.C.; Berson, J.F.; Theos, S.C.; Herman, K.E.; Harper, D.C.; Tenza, D.; Sviderskaya, E.V.; Lamoreux, M.L.; Bennett, D.C.; Raposo, G.; et al. Dual loss of ER export and endocytic signals with altered melanosome morphology in the silver mutation of Pmel17. Mol. Biol. Cell 2006, 17, 3598–3612. [Google Scholar] [CrossRef] [Green Version]
- Kawakami, A.; Sakane, F.; Imai, S.I.; Yasuda, S.; Kai, M.; Kanoh, H.; Jin, H.Y.; Hirosaki, K.; Yamashita, T.; Fisher, D.E.; et al. Rab7 regulates maturation of melanosomal matrix protein gp100/Pmel17/Silv. J. Investig. Dermatol. 2008, 128, 143–150. [Google Scholar] [CrossRef] [Green Version]
- Hida, T.; Sohma, H.; Kokai, Y.; Kawakami, A.; Hirosaki, K.; Okura, M.; Tosa, N.; Yamashita, T.; Jimbow, K. Rab7 is a critical mediator in vesicular transport of tyrosinase-related protein 1 in melanocytes. J. Dermatol. 2011, 38, 432–441. [Google Scholar] [CrossRef] [PubMed]
- Miyamura, Y.; Coelho, S.G.; Wolber, R.; Miller, S.A.; Wakamatsu, K.; Zmudzka, B.Z.; Ito, S.; Smuda, C.; Passeron, T.; Choi, W.; et al. Regulation of human skin pigmentation and responses to ultraviolet radiation. Pigment Cell Res. 2007, 20, 2–13. [Google Scholar] [CrossRef]
- Yamaguchi, Y.; Brenner, M.; Hearing, V.J. The regulation of skin pigmentation. J. Biol. Chem. 2007, 282, 27557–27561. [Google Scholar] [CrossRef] [Green Version]
- Bultema, J.J.; Di Pietro, S.M. Cell type-specific Rab32 and Rab38 cooperate with the ubiquitous lysosome biogenesis machinery to synthesize specialized lysosome-related organelles. Small GTPases 2013, 4, 16–21. [Google Scholar] [CrossRef] [Green Version]
- Chiaverini, C.; Beuret, L.; Flori, E.; Busca, R.; Abbe, P.; Bille, K.; Bahadoran, P.; Ortonne, J.-P.; Bertolotto, C.; Ballotti, R. Microphthalmia-associated transcription factor regulates RAB27A gene expression and controls melanosome transport. J. Biol. Chem. 2008, 283, 12635–12642. [Google Scholar] [CrossRef] [Green Version]
- Hoek, K.S.; Schlegel, N.C.; Eichhoff, O.M.; Widmer, D.S.; Praetorius, C.; Einarsson, S.O.; Valgeirsdottir, S.; Bergsteinsdottir, K.; Schepsky, A.; Dummer, R.; et al. Novel MITF targets identified using a two-step DNA microarray strategy. Pigment Cell Melanoma Res. 2008, 21, 665–676. [Google Scholar] [CrossRef] [PubMed]
- Morimoto, R.I.; Santoro, M.G. Stress-inducible responses and heat shock proteins: New pharmacologic targets for cytoprotection. Nat. Biotechnol. 1998, 16, 833–838. [Google Scholar] [CrossRef]
- Matsuda, M.; Hoshino, T.; Yamashita, Y.; Tanaka, K.-I.; Maji, D.; Sato, K.; Adachi, H.; Sobue, G.; Ihn, H.; Funasaka, Y.; et al. Prevention of UVB radiation-induced epidermal damage by expression of heat shock protein 70. J. Biol. Chem. 2010, 285, 5848–5858. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matsuda, M.; Hoshino, T.; Yamakawa, N.; Tahara, K.; Adachi, H.; Sobue, G.; Maji, D.; Ihn, H.; Mizushima, T. Suppression of UV-induced wrinkle formation by induction of HSP70 expression in mice. J. Investig. Dermatol. 2013, 133, 919–928. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoshino, T.; Matsuda, M.; Yamashita, Y.; Takehara, M.; Fukuya, M.; Mineda, K.; Maji, D.; Ihn, H.; Adachi, H.; Sobue, G.; et al. Suppression of melanin production by expression of HSP70. J. Biol. Chem. 2010, 285, 13254–13263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cui, R.; Widlund, H.R.; Feige, E.; Lin, J.Y.; Wilensky, D.L.; Igras, V.E.; D’Orazio, J.; Fung, C.Y.; Schanbacher, C.F.; Granter, S.R.; et al. Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell 2007, 128, 853–864. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wawrzynow, B.; Zylicz, A.; Zylicz, M. Chaperoning the guardian of the genome. The two-faced role of molecular chaperones in p53 tumor suppressor action. Biochim. Biophys. Acta Rev. Cancer 2018, 1869, 161–174. [Google Scholar] [CrossRef] [PubMed]
- Hansen, S.; Hupp, T.R.; Lane, D.P. Allosteric regulation of the thermostability and DNA binding activity of human p53 by specific interacting proteins. CRC Cell Transformation Group. J. Biol. Chem. 1996, 271, 3917–3924. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hupp, T.R.; Meek, D.W.; Midgley, C.A.; Lane, D.P. Regulation of the specific DNA binding function of p53. Cell 1992, 71, 875–886. [Google Scholar] [CrossRef]
- Walerych, D.; Olszewski, M.B.; Gutkowska, M.; Helwak, A.; Zylicz, M.; Zylicz, A. Hsp70 molecular chaperones are required to support p53 tumor suppressor activity under stress conditions. Oncogene 2009, 28, 4284–4294. [Google Scholar] [CrossRef] [Green Version]
- Akakura, S.; Yoshida, M.; Yoneda, Y.; Horinouchi, S. A role for Hsc70 in regulating nucleocytoplasmic transport of a temperature-sensitive p53 (p53Val-135). J. Biol. Chem. 2001, 276, 14649–14657. [Google Scholar] [CrossRef] [Green Version]
- Rohde, M.; Daugaard, M.; Jensen, M.H.; Helin, K.; Nylandsted, J.; Jäättelä, M. Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev. 2005, 19, 570–582. [Google Scholar] [CrossRef] [Green Version]
- Wiech, M.; Olszewski, M.B.; Tracz-Gaszewska, Z.; Wawrzynow, B.; Zylicz, M.; Zylicz, A. Molecular mechanism of mutant p53 stabilization: The role of HSP70 and MDM2. PLoS ONE 2012, 7, e51426. [Google Scholar]
- Kim, H.-B.; Lee, S.-H.; Um, J.-H.; Oh, W.K.; Kim, D.-W.; Kang, C.-D.; Kim, S.-H. Sensitization of multidrug-resistant human cancer cells to Hsp90 inhibitors by down-regulation of SIRT1. Oncotarget 2015, 6, 36202–36218. [Google Scholar] [CrossRef]
- Buckley, N.E.; D’Costa, Z.; Kaminska, M.; Mullan, P.B. S100A2 is a BRCA1/p63 coregulated tumour suppressor gene with roles in the regulation of mutant p53 stability. Cell Death Dis. 2014, 5, e1070. [Google Scholar] [CrossRef] [Green Version]
- Kim, H.M.; Oh, S.; Yoon, J.H.; Kang, D.; Son, M.; Byun, K. Radiofrequency Irradiation Attenuates High-Mobility Group Box 1 and Toll-like Receptor Activation in Ultraviolet B-Induced Skin Inflammation. Molecules 2021, 26, 1297. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.M.; Oh, S.; Yang, J.Y.; Sun, H.J.; Jang, M.; Kang, D.; Son, K.H.; Byun, K. Evaluating Whether Radiofrequency Irradiation Attenuated UV-B-Induced Skin Pigmentation by Increasing Melanosomal Autophagy and Decreasing Melanin Synthesis. Int. J. Mol. Sci. 2021, 22, 10724. [Google Scholar] [CrossRef]
- Beasley, K.L.; Weiss, R.A. Radiofrequency in cosmetic dermatology. Dermatol. Clin. 2014, 32, 79–90. [Google Scholar] [CrossRef]
- Dierickx, C.C. The role of deep heating for noninvasive skin rejuvenation. Lasers Surg. Med. 2006, 38, 799–807. [Google Scholar] [CrossRef] [PubMed]
- Zelickson, B.D.; Kist, D.; Bernstein, E.; Brown, D.B.; Ksenzenko, S.; Burns, J.; Kilmer, S.; Mehregan, D.; Pope, K. Histological and ultrastructural evaluation of the effects of a radiofrequency-based nonablative dermal remodeling device: A pilot study. Arch. Dermatol. 2004, 140, 204–209. [Google Scholar] [CrossRef] [Green Version]
- Hantash, B.M.; Ubeid, A.A.; Chang, H.; Kafi, R.; Renton, B. Bipolar fractional radiofrequency treatment induces neoelastogenesis and neocollagenesis. Lasers Surg. Med. 2009, 41, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Pathak, M.A.; Fanselow, D.L. Photobiology of melanin pigmentation: Dose/response of skin to sunlight and its contents. J. Am. Acad. Dermatol. 1983, 9, 724–733. [Google Scholar] [CrossRef]
- Riley, P.A. Melanin. Int. J. Biochem. Cell Biol. 1997, 29, 1235–1239. [Google Scholar] [CrossRef]
- Costin, G.E.; Hearing, V.J. Human skin pigmentation: Melanocytes modulate skin color in response to stress. FASEB J. 2007, 21, 976–994. [Google Scholar] [CrossRef]
- Simon, J.D.; Peles, D.; Wakamatsu, K.; Ito, S. Current challenges in understanding melanogenesis: Bridging chemistry, biological control, morphology, and function. Pigment Cell Melanoma Res. 2009, 22, 563–579. [Google Scholar] [CrossRef] [PubMed]
- Park, H.Y.; Kosmadaki, M.; Yaar, M.; Gilchrest, B.A. Cellular mechanisms regulating human melanogenesis. Cell Mol. Life Sci. 2009, 66, 1493–1506. [Google Scholar] [CrossRef]
- Pawelek, J.M. After dopachrome? Pigment Cell Res. 1991, 4, 53–62. [Google Scholar] [CrossRef]
- Ito, S.; Wakamatsu, K. Chemistry of mixed melanogenesis--pivotal roles of dopaquinone. Photochem. Photobiol. 2008, 84, 582–592. [Google Scholar] [CrossRef]
- Del Marmol, V.; Beermann, F. Tyrosinase and related proteins in mammalian pigmentation. FEBS Lett. 1996, 381, 165–168. [Google Scholar] [CrossRef]
- Abdel-Malek, Z.; Swope, V.B.; Suzuki, I.; Akcali, C.; Harriger, M.D.; Boyce, S.T.; Urabe, K.; Hearing, V.J. Mitogenic and melanogenic stimulation of normal human melanocytes by melanotropic peptides. Proc. Natl. Acad. Sci. USA 1995, 92, 1789–1793. [Google Scholar] [CrossRef] [Green Version]
- García-Borrón, J.C.; Abdel-Malek, Z.; Jiménez-Cervantes, C. MC1R, the cAMP pathway, and the response to solar UV: Extending the horizon beyond pigmentation. Pigment Cell Melanoma Res. 2014, 27, 699–720. [Google Scholar] [CrossRef] [PubMed]
- Swope, V.B.; Abdel-Malek, Z.A. Significance of the Melanocortin 1 and Endothelin B Receptors in Melanocyte Homeostasis and Prevention of Sun-Induced Genotoxicity. Front. Genet. 2016, 7, 146. [Google Scholar] [CrossRef] [Green Version]
- Wolf Horrell, E.M.; Boulanger, M.C.; D’Orazio, J.A. Melanocortin 1 Receptor: Structure, Function, and Regulation. Front. Genet. 2016, 7, 95. [Google Scholar] [CrossRef] [Green Version]
- Buscà, R.; Ballotti, R. Cyclic AMP a key messenger in the regulation of skin pigmentation. Pigment Cell Res. 2000, 13, 60–69. [Google Scholar] [CrossRef] [PubMed]
- Cheli, Y.; Ohanna, M.; Ballotti, R.; Bertolotto, C. Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res. 2010, 23, 27–40. [Google Scholar] [CrossRef] [PubMed]
- Barnetson, R.S.; Ooi, T.K.; Zhuang, L.; Halliday, G.M.; Reid, C.M.; Walker, P.C.; Humphrey, S.M.; Kleinig, M.J. [Nle4-D-Phe7]-alpha-melanocyte-stimulating hormone significantly increased pigmentation and decreased UV damage in fair-skinned Caucasian volunteers. J. Investig. Dermatol. 2006, 126, 1869–1878. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.-J.; Hseu, Y.-C.; Gowrisankar, Y.V.; Chung, Y.-T.; Zhang, Y.-Z.; Way, T.-D.; Yang, H.-L. The anti-melanogenic effects of 3-O-ethyl ascorbic acid via Nrf2-mediated α-MSH inhibition in UVA-irradiated keratinocytes and autophagy induction in melanocytes. Free Radic. Biol. Med. 2021, 173, 151–169. [Google Scholar] [CrossRef] [PubMed]
- Wilson, N.; McArdle, A.; Guerin, D.; Tasker, H.; Wareing, P.; Foster, C.S.; Jackson, M.J.; Rhodes, L.E. Hyperthermia to normal human skin in vivo upregulates heat shock proteins 27, 60, 72i and 90. J. Cutan. Pathol. 2000, 27, 176–182. [Google Scholar] [CrossRef]
- Morris, S.D. Heat shock proteins and the skin. Clin. Exp. Dermatol. 2002, 27, 220–224. [Google Scholar] [CrossRef] [PubMed]
- Jonak, C.; Klosner, G.; Trautinger, F. Heat shock proteins in the skin. Int. J. Cosmet. Sci. 2006, 28, 233–241. [Google Scholar] [CrossRef] [PubMed]
- Trautinger, F.; Kokesch, C.; Klosner, G.; Knobler, R.M.; Kindas-Mügge, I. Expression of the 72-kD heat shock protein is induced by ultraviolet A radiation in a human fibrosarcoma cell line. Exp. Dermatol. 1999, 8, 187–192. [Google Scholar] [CrossRef]
- Allanson, M.; Reeve, V.E. Immunoprotective UVA (320–400 nm) irradiation upregulates heme oxygenase-1 in the dermis and epidermis of hairless mouse skin. J. Investig. Dermatol. 2004, 122, 1030–1036. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trautinger, F. Heat shock proteins in the photobiology of human skin. J. Photochem. Photobiol. B 2001, 63, 70–77. [Google Scholar] [CrossRef]
- Trautinger, F.; Kindås-Mügge, I.; Barlan, B.; Neuner, P.; Knobler, R.M. 72-kD heat shock protein is a mediator of resistance to ultraviolet B light. J. Investig. Dermatol. 1995, 105, 160–162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, K.-C.; Kim, D.-S.; Choi, H.-O.; Kim, K.-H.; Chung, J.-H.; Eun, H.-C.; Lee, J.-S.; Seo, J.-S. Overexpression of HSP70 prevents ultraviolet B-induced apoptosis of a human melanoma cell line. Arch. Dermatol. Res. 2000, 292, 482–487. [Google Scholar] [CrossRef]
- Maytin, E.V.; Wimberlym, J.M.; Kanem, K.S. Heat shock modulates UVB-induced cell death in human epidermal keratinocytes: Evidence for a hyperthermia-inducible protective response. J. Investig. Dermatol. 1994, 103, 547–553. [Google Scholar] [CrossRef] [Green Version]
- Kwon, S.B.; Young, C.; Kim, D.S.; Choi, H.O.; Kim, K.H.; Chung, J.H.; Eun, H.C.; Park, K.C.; Oh, C.K.; Seo, J.S. Impaired repair ability of hsp70.1 KO mouse after UVB irradiation. J. Dermatol. Sci. 2002, 28, 144–151. [Google Scholar] [CrossRef]
- Kim, D.S.; Park, S.H.; Kwon, S.B.; Youn, S.W.; Park, E.S.; Park, K.C. Heat treatment decreases melanin synthesis via protein phosphatase 2A inactivation. Cell Signal. 2005, 17, 1023–1031. [Google Scholar] [CrossRef]
- Kim, D.S.; Park, S.H.; Kwon, S.B.; Na, J.I.; Huh, C.H.; Park, K.C. Additive effects of heat and p38 MAPK inhibitor treatment on melanin synthesis. Arch. Pharm. Res. 2007, 30, 581–586. [Google Scholar] [CrossRef] [PubMed]
- Usui, K.; Ikeda, T.; Horibe, Y.; Nakao, M.; Hoshino, T.; Mizushima, T. Identification of HSP70-inducing activity in Arnica montana extract and purification and characterization of HSP70-inducers. J. Dermatol. Sci. 2015, 78, 67–75. [Google Scholar] [CrossRef] [Green Version]
- Yaglom, J.A.; Gabai, V.L.; Sherman, M.Y. High levels of heat shock protein Hsp72 in cancer cells suppress default senescence pathways. Cancer Res. 2007, 67, 2373–2381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gabai, V.L.; Yaglom, J.A.; Waldman, T.; Sherman, M.Y. Heat shock protein Hsp72 controls oncogene-induced senescence pathways in cancer cells. Mol. Cell. Biol. 2009, 29, 559–569. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gabai, V.L.; Meriin, A.B.; Mosser, D.D.; Caron, A.W.; Rits, S.; Shifrin, V.I.; Sherman, M.Y. Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol. Chem. 1997, 272, 18033–18037. [Google Scholar] [CrossRef] [Green Version]
- Mosser, D.D.; Caron, A.W.; Bourget, L.; Denis-Larose, C.; Massie, B. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 1997, 17, 5317–5327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fuchs, S.Y.; Adler, V.; Pincus, M.R.; Ronai, Z. MEKK1/JNK signaling stabilizes and activates p53. Proc. Natl. Acad. Sci. USA 1998, 95, 10541–10546. [Google Scholar] [CrossRef] [Green Version]
- Beltrán-Frutos, E.; Ferrer, C.; Seco-Rovira, V.; Martínez-Hernández, J.; Serrano-Sánchez, M.I.; Pastor, L.M. Differences in the response in the dermis of the tails of young and old SD rats to treatment with bipolar RF. J. Cosmet. Dermatol. 2021, 20, 2519–2526. [Google Scholar] [CrossRef]
- El-Abaseri, T.B.; Putta, S.; Hansen, L.A. Ultraviolet irradiation induces keratinocyte proliferation and epidermal hyperplasia through the activation of the epidermal growth factor receptor. Carcinogenesis 2006, 27, 225–231. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stierner, U.; Rosdahl, I.; Augustsson, A.; Kågedal, B. UVB irradiation induces melanocyte increase in both exposed and shielded human skin. J. Investig. Dermatol. 1989, 92, 561–564. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.; Lockey, R. Dermatology for the allergist. World Allergy Organ. J. 2010, 3, 202–215. [Google Scholar] [CrossRef] [Green Version]
- Levy, L.L.; Emer, J.J. Emotional benefit of cosmetic camouflage in the treatment of facial skin conditions: Personal experience and review. Clin. Cosmet. Investig. Dermatol. 2012, 5, 173–182. [Google Scholar]
- Saxena, S.; Andersen, R.M.; Maibach, H.I. Pitfalls in clinical trials reveal need for well tolerated, more effective depigmenting agents. J. Dermatol. Treat. 2015, 26, 440–450. [Google Scholar] [CrossRef]
- Pavlic, V.; Brkic, Z.; Marin, S.; Cicmil, S.; Gojkov-Vukelic, M.; Aoki, A. Gingival melanin depigmentation by Er:YAG laser: A literature review. J. Cosmet. Laser Ther. 2018, 20, 85–90. [Google Scholar] [CrossRef] [PubMed]
- Jow, T.; Hantash, B.M. Hydroquinone-induced depigmentation: Case report and review of the literature. Dermatitis 2014, 25, e1–e5. [Google Scholar] [CrossRef]
- Jegal, J.; Chung, K.W.; Chung, H.Y.; Jeong, E.J.; Yang, M.H. The standardized extract of juniperus communis alleviates hyperpigmentation in vivo HRM-2 hairless mice and in vitro murine B16 melanoma cells. Biol. Pharm. Bull. 2017, 40, 1381–1388. [Google Scholar] [CrossRef] [Green Version]
- Yun, C.Y.; You, S.T.; Kim, J.H.; Chung, J.H.; Han, S.B.; Shin, E.Y.; Kim, E.G. p21-activated kinase 4 critically regulates melanogenesis via activation of the CREB/MITF and β-catenin/MITF pathways. J. Investig. Dermatol. 2015, 135, 1385–1394. [Google Scholar] [CrossRef] [Green Version]
- Lee, B.; Moon, K.M.; Kim, S.J.; Kim, S.H.; Kim, D.H.; An, H.J.; Jeong, J.W.; Kim, Y.R.; Son, S.; Kim, M.J.; et al. (Z)-5-(2,4-Dihydroxybenzylidene)thiazolidine-2,4-dione prevents UVB-induced melanogenesis and wrinkle formation through suppressing oxidative stress in HRM-2 hairless mice. Oxid. Med. Cell. Longev. 2016, 2016, 2761463. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chung, K.W.; Jeong, H.O.; Jang, E.J.; Choi, Y.J.; Kim, D.H.; Kim, S.R.; Lee, K.J.; Lee, H.J.; Chun, P.; Byun, Y.; et al. Characterization of a small molecule inhibitor of melanogenesis that inhibits tyrosinase activity and scavenges nitric oxide (NO). Biochim. Biophys. Acta 2013, 1830, 4752–4761. [Google Scholar] [CrossRef] [PubMed]
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Kim, H.M.; Oh, S.; Choi, C.H.; Yang, J.Y.; Kim, S.; Kang, D.; Son, K.H.; Byun, K. Attenuation Effect of Radiofrequency Irradiation on UV-B-Induced Skin Pigmentation by Decreasing Melanin Synthesis and through Upregulation of Heat Shock Protein 70. Molecules 2021, 26, 7648. https://0-doi-org.brum.beds.ac.uk/10.3390/molecules26247648
Kim HM, Oh S, Choi CH, Yang JY, Kim S, Kang D, Son KH, Byun K. Attenuation Effect of Radiofrequency Irradiation on UV-B-Induced Skin Pigmentation by Decreasing Melanin Synthesis and through Upregulation of Heat Shock Protein 70. Molecules. 2021; 26(24):7648. https://0-doi-org.brum.beds.ac.uk/10.3390/molecules26247648
Chicago/Turabian StyleKim, Hyoung Moon, Seyeon Oh, Chang Hu Choi, Jin Young Yang, Sunggeun Kim, Donghwan Kang, Kuk Hui Son, and Kyunghee Byun. 2021. "Attenuation Effect of Radiofrequency Irradiation on UV-B-Induced Skin Pigmentation by Decreasing Melanin Synthesis and through Upregulation of Heat Shock Protein 70" Molecules 26, no. 24: 7648. https://0-doi-org.brum.beds.ac.uk/10.3390/molecules26247648