Advertisement
Research Article| Volume 88, ISSUE 2, P207-215, November 2017

The effect of interaction of heat and UVB on human keratinocyte: Novel insights on UVB-induced carcinogenesis of the skin

  • Author Footnotes
    1 Lan and Wang contributed equally to this work.
    Cheng-Che E. Lan
    Footnotes
    1 Lan and Wang contributed equally to this work.
    Affiliations
    Department of Dermatology, Kaohsiung Medical University Hospital, and College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    Search for articles by this author
  • Author Footnotes
    1 Lan and Wang contributed equally to this work.
    Yeng-Tseng Wang
    Footnotes
    1 Lan and Wang contributed equally to this work.
    Affiliations
    Department of Biochemistry, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    Search for articles by this author
  • Chi-Yu Lu
    Affiliations
    Department of Biochemistry, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    Search for articles by this author
  • Ai-Hui Fang
    Affiliations
    Department of Microbiology, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
    Search for articles by this author
  • Ching-Shuang Wu
    Correspondence
    Corresponding author at: Department of Medical Laboratory Science and Biotechnology, College of Health Science, Kaohsiung Medical University, 100 Shih–Chuan 1st Rd, Kaohsiung, Taiwan.
    Affiliations
    Department of Medical Laboratory Science and Biotechnology, College of Health Science, Kaohsiung Medical University, Kaohsiung, Taiwan

    Institute of Biomedical Sciences, National Sun Yat-Sen University, Kaohsiung, Taiwan
    Search for articles by this author
  • Author Footnotes
    1 Lan and Wang contributed equally to this work.

      Highlights

      • Both UV radiation and environmental heat can induce skin aging but through different pathways.
      • UVB radiation at environment with higher temperature may possess less photocarcinogenic potential.
      • Interactions between environmental heat and UVB irradiation may provide new concepts on protection against UVB-induced DNA damage.

      Abstract

      Background

      Skin cancer is an important environmentally-related health issue. Although sun exposure is closely associated with increasing environmental heat, the effects of environmental heat on the skin, especially in the context of photocarcinogenesis, has not been carefully examined.

      Objectives

      This study aimed to explore the effects and interactions of UVB radiation and environmental heat on photocarcinogenesis of the skin using cell and animal models.

      Methods

      Cultured keratinocytes and hairless mice were exposed to different treatment conditions including UVB radiation and environmental heat. The effects of treatment on keratinocyte and mice skin were evaluated at indicated time points.

      Results

      UVB induced DNA damage was significantly lower in keratinocytes that were pretreated in an environment with slightly elevated temperature followed by UVB treatment (Heat-UVB) as compared to UVB and UVB radiation followed by exposure to equivalent increase in environmental heat (UVB-Heat) groups. Similar phenomenon was observed in terms of keratinocyte viability. In the animal model, it was found that Heat-UVB treated mice showed delayed and reduced tumor formation as compared to the UVB and UVB-Heat treated groups. Quantum simulation analyses demonstrated that the energy required for CPD formation at environment with higher temperature required considerable higher energy as compared to CPD formation at lower temperature.

      Conclusion

      Taken together, our results demonstrated that with equivalent UVB exposure, higher temperature environment may protect cells against subsequent UVB-induced DNA damages.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Dermatological Science
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Schieke S.M.
        • Schroeder P.
        • Krutmann J.
        Cutaneous effects of infrared radiation: from clinical observations to molecular response mechanisms.
        Photodermatol. Photoimmunol. Photomed. 2003; 19: 228-234
        • Bowden G.T.
        Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling.
        Nat. Rev. Cancer. 2004; 4: 23-35
        • Rigel D.S.
        Cutaneous ultraviolet exposure and its relationship to the development of skin cancer.
        J. Am. Acad. Dermatol. 2008; 58: S129-S132
        • Shin M.H.
        • Seo J.E.
        • Kim Y.K.
        • Kim K.H.
        • Chung J.H.
        Chronic heat treatment causes skin wrinkle formation and oxidative damage in hairless mice.
        Mech. Ageing Dev. 2012; 133: 92-98
        • Mayes A.E.
        • Holyoak C.D.
        Repeat mild heat shock increases dermal fibroblast activity and collagen production.
        Rejuvenation Res. 2008; 11: 461-465
        • Lan C.C.
        • Wu C.S.
        • Yu H.S.
        Solar-simulated radiation and heat treatment induced metalloproteinase-1 expression in cultured dermal fibroblasts via distinct pathways: implications on reduction of sun-associated aging.
        J. Dermatol. Sci. 2013; 72: 290-295
        • Searchinger T.
        • Heimlich R.
        • Houghton R.A.
        • Dong F.
        • Elobeid A.
        • Fabiosa J.
        • Tokgoz S.
        • Hayes D.
        • Yu T.H.
        Use of U.S. croplands for biofuels increases greenhouse gases through emissions from land-use change.
        Science. 2008; 319: 1238-1240
        • Schellnhuber H.J.
        Global warming: stop worrying start panicking?.
        Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 14239-14240
        • Weston D.
        Policy on global warming: fiddling while the globe burns?.
        Aust. N. Z. J. Public Health. 2009; 33: 307-311
        • Ling H.
        • Boudsocq F.
        • Plosky B.S.
        • Woodgate R.
        • Yang W.
        Replication of a cis–syn thymine dimer at atomic resolution.
        Nature. 2003; 424: 1083-1087
        • Jorgensen W.L.
        • Chandrasekhar J.
        • Madura J.D.
        • Impey R.W.
        • Klein M.L.
        Comparison of simple potential functions for simulating liquid water.
        J. Chem. Phys. 1983; 79: 926-935
        • Ryckaert J.-P.
        • Ciccotti G.
        • Berendsen H.J.
        Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes.
        J. Comput. Phys. 1977; 23: 327-341
        • Kim K.
        • Jordan K.
        Particle mesh Ewald: an N [center-dot] log (N) method for Ewald sums in large systems.
        J. Chem. Phys. 1994; 98: 10089-10092
        • Becke A.D.
        Density-functional thermochemistry. III. The role of exact exchange.
        J. Chem. Phys. 1993; 98: 5648-5652
        • Valiev M.
        • Bylaska E.J.
        • Govind N.
        • Kowalski K.
        • Straatsma T.P.
        • Van Dam H.J.
        • Wang D.
        • Nieplocha J.
        • Apra E.
        • Windus T.L.
        NWChem: a comprehensive and scalable open-source solution for large scale molecular simulations.
        Comput. Phys. Commun. 2010; 181: 1477-1489
        • Jans J.
        • Schul W.
        • Sert Y.-G.
        • Rijksen Y.
        • Rebel H.
        • Eker A.P.
        • Nakajima S.
        • van Steeg H.
        • de Gruijl F.R.
        • Yasui A.
        Powerful skin cancer protection by a CPD-photolyase transgene.
        Curr. Biol. 2005; 15: 105-115
        • Benjamin C.L.
        • Ullrich S.E.
        • Kripke M.L.
        • Ananthaswamy H.N.
        p53 tumor suppressor gene: a critical molecular target for UV induction and prevention of skin cancer.
        Photochem. Photobiol. 2008; 84: 55-62
        • Gannon J.
        • Greaves R.
        • Iggo R.
        • Lane D.
        Activating mutations in p53 produce a common conformational effect. A monoclonal antibody specific for the mutant form.
        EMBO. J. 1990; 9: 1595-1602
        • Maytin E.V.
        • Murphy L.A.
        • Merrill M.A.
        Hyperthermia induces resistance to ultraviolet light B in primary and immortalized epidermal keratinocytes.
        Cancer Res. 1993; 53: 4952-4959
        • Maytin E.V.
        • Wimberly J.M.
        • Kane K.S.
        Heat shock modulates UVB-induced cell death in human epidermal keratinocytes: evidence for a hyperthermia-inducible protective response.
        J. Invest. Dermatol. 1994; 103: 547-553
        • Simon M.M.
        • Reikerstorfer A.
        • Schwarz A.
        • Krone C.
        • Luger T.A.
        • Jäättelä M.
        • Schwarz T.
        Heat shock protein 70 overexpression affects the response to ultraviolet light in murine fibroblasts. Evidence for increased cell viability and suppression of cytokine release.
        J. Clin. Invest. 1995; 95: 926-933
        • Calapre L.
        • Gray E.S.
        • Ziman M.
        Heat stress: a risk for skin carcinogenesis.
        Cancer Lett. 2013; 337: 35-40
        • Fisher M.S.
        • Kripke M.L.
        Suppressor T lymphocytes control the development of primary skin cancers in ultraviolet-irradiated mice.
        Science. 1982; 216: 1133-1134
        • Law Y.K.
        • Azadi J.
        • Crespo-Hernández C.E.
        • Olmon E.
        • Kohler B.
        Predicting thymine dimerization yields from molecular dynamics simulations.
        Biophys. J. 2008; 94: 3590-3600
        • Barbatti M.
        Computational reference data for the photochemistry of cyclobutane pyrimidine dimers.
        Chem. Phys. Chem. 2014; 15: 3342-3354
        • Miyazawa Y.
        • Nishioka H.
        • Yura K.
        • Yamato T.
        Discrimination of class I cyclobutane pyrimidine dimer photolyase from blue light photoreceptors by single methionine residue.
        Biophys. J. 2008; 94: 2194-2203
        • Mendieta-Moreno J.I.s.
        • Trabada D.G.
        • Mendieta J.s.
        • Lewis J.P.
        • Gómez-Puertas P.
        • Ortega J.
        Quantum mechanics/molecular mechanics free energy maps and nonadiabatic simulations for a photochemical reaction in DNA: cyclobutane thymine dimer.
        J. Phys. Chem. Lett. 2016; 7: 4391-4397