Skip to main content
Log in

Heat shock antagonizes UVA-induced responses in murine melanocytes and melanoma cells: an unexpected interaction

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

The skin is under the influence of oscillatory factors such as light and temperature. This organ possesses a local system that controls several aspects in a time-dependent manner; moreover, the skin has a well-known set of opsins whose function is still unknown. We demonstrate that heat shock reduces Opn2 expression in normal Melan-a melanocytes, while the opposite effect is found in malignant B16-F10 cells. In both cell lines, UVA. radiation increases the expression of Opn4 and melanin content. Clock genes and Xpa, a DNA. repair gene, of malignant melanocytes are more responsive to UVA. radiation when compared to normal cells. Most UVA-induced effects are antagonized by heat shock, a phenomenon shown for the first time. Based on our data, the heat produced during UV. experiments should be carefully monitored since temperature represents, according to our results, an important confounding factor, and therefore it should, when possible, be dissociated from UV. radiation. The responses displayed by murine melanoma cells, if proven to also take place in human melanoma, may represent an important step in cancer development and progression

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

6-4 PP:

6,4 Photoproducts

Aqp3:

Aquaporin 3 gene

BMAL1:

Aryl hydrocarbon receptor nuclear translocator- like protein 1

Bmal1:

Aryl hydrocarbon receptor nuclear translocatorlike protein 1 gene

CLOCK.:

Circadian locomotor output cycles kaput protein

Clock:

Circadian locomotor output cycles kaput gene

CPD:

Cyclobutane pyrimidine dimers

CRY:

Cryptochrome protein

Cry:

Cryptochrome gene

DD:

Constant dark

FBS:

Fetal bovine serum

IPD:

Immediate pigment darkening

LD:

Light-dark cycle

PER:

Period protein

Per:

Period gene

PI:

Propidium iodide

Rev-Erba/β:

RAR-related orphan receptor alpha/beta gene RORalβ Nuclear receptor subfamily 1, group D, member 1/2 gene

SCNs:

Suprachiasmatic nuclei

TPA:

Phorbol 12-myristate 13-acetate

UVB:

Ultraviolet B radiation

XPA:

Xeroderma pigmentosum, complementation group A protein

Xpa:

Xeroderma pigmentosum, complementation group A. gene

ZT:

Zeitgeber time

References

  1. J. B. Hogenesch and H. R. Ueda, Understanding systems-level properties: timely stories from the study of clocks, Nat. Rev. Genet, 2011, 12, 407–416.

    Article  CAS  PubMed  Google Scholar 

  2. S. A. Brown and A. Azzi, Peripheral circadian oscillators in mammals, Handb. Exp. Pharmacol, 2013, 217, 45–66.

    Article  CAS  Google Scholar 

  3. E. D. Buhr and J. S. Takahashi, Molecular components of the Mammalian circadian clock, Handb. Exp. Pharmacol, 2013, 217, 3–27.

    Article  CAS  Google Scholar 

  4. J. A. Mohawk, C. B. Green and J. S. Takahashi, Central and peripheral circadian clocks in mammals, Annu. Rev. Neurosci., 2012, 35, 445–462.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. M. R. Ralph, R. G. Foster, F. C. Davis and M. Menaker, Transplanted suprachiasmatic nucleus determines circadian period, Science, 1990, 247, 975–978.

    Article  CAS  PubMed  Google Scholar 

  6. S. Panda, I. Provencio, D. C. Tu, S. S. Pires, M. D. Rollag, A. M. Castrucci, M. T. Pletcher, T. K. Sato, T. Wiltshire, M. Andahazy, S. A. Kay, R. N. Van Gelder and J. B. Hogenesch, Melanopsin is required for non-image-forming photic responses in blind mice, Science, 2003, 301, 525–527.

    Article  CAS  PubMed  Google Scholar 

  7. I. Provencio, M. D. Rollag and A. M. Castrucci, Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night, Nature, 2002, 415, 493.

    Article  CAS  PubMed  Google Scholar 

  8. D. M. Berson, F. A. Dunn and M. Takao, Phototransduction by retinal ganglion cells that set the circadian clock, Science, 2002, 295, 1070–1073.

    Article  CAS  PubMed  Google Scholar 

  9. S. Hughes, M. W. Hankins, R. G. Foster and S. N. Peirson, Melanopsin phototransduction: slowly emerging from the dark, Prog. Brain Res., 2012, 199, 19–40.

    Article  CAS  PubMed  Google Scholar 

  10. K. G. Baron and K. J. Reid, Circadian misalignment and health, Int. Rev. Psychiatry, 2014, 26, 139–154.

    Article  PubMed  PubMed Central  Google Scholar 

  11. F. C. Kelleher, A. Rao and A. Maguire, Circadian molecular clocks and cancer, Cancer Lett., 2014, 342, 9–18.

    Article  CAS  PubMed  Google Scholar 

  12. C. Sawidis and M. Koutsilieris, Circadian rhythm disruption in cancer biology, Mol. Med., 2012, 18, 1249–1260.

    Article  CAS  Google Scholar 

  13. S. Kawara, R. Mydlarski, A. J. Mamelak, I. Freed, B. Wang, H. Watanabe, G. Shiyji, S. K. Tavadia, H. Suzuki, G. A. Bjarnason, R. C. Jordan and D. N. Sauder, Low-dose ultraviolet B rays alter the mRNA. expression of the circadian clock genes in cultured human keratinocytes, J. Invest. Dermatol, 2002, 119, 1220–1223.

    Article  CAS  PubMed  Google Scholar 

  14. L. V. de Assis, M. N. Moraes, S. da Silveira Cruz-Machado and A. M. Castrucci, The effect of white light on normal and malignant murine melanocytes: A. link between opsins, clock genes, and melanogenesis, Biochim. Biophys. Acta, 2016, 1863, 1119–1133.

    Article  PubMed  CAS  Google Scholar 

  15. M. O. Poletini, L. V. M. de Assis, M. N. Moraes and A. M. L. Castrucci, Estradiol Differently Affects Melanin Synthesis of Malignant and Normal Melanocytes - a Relationship With Clock and Clock Controlled Genes, Mol. Cell. Biochem., 2016, 421, 29–39.

    Article  CAS  PubMed  Google Scholar 

  16. E. D. Buhr, S. H. Yoo and J. S. Takahashi, Temperature as a universal resetting cue for mammalian circadian oscillators, Science, 2010, 330, 379–385.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. U. Abraham, A. E. Granada, P. O. Westermark, M. Heine, A. Kramer and H. Herzel, Coupling governs entrainment range of circadian clocks, Mol. Syst. Biol, 2010, 6, 438.

    Article  PubMed  PubMed Central  Google Scholar 

  18. S. A. Brown, G. Zumbrunn, F. Fleury-Olela, N. Preitner and U. Schibler, Rhythms of mammalian body temperature can sustain peripheral circadian clocks, Curr. Biol, 2002, 12, 1574–1583.

    Article  CAS  PubMed  Google Scholar 

  19. C. Saini, J. Morf, M. Stratmann, P. Gos and U. Schibler, Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators, Genes Dev., 2012, 26, 567–580.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. F. Sporl, K. Schellenberg, T. Blatt, H. Wenck, K. P. Wittern, A. Schrader and A. Kramer, A. circadian clock in HaCa T. keratinocytes,J. Invest. Dermatol, 2011, 131, 338–348.

    Article  PubMed  CAS  Google Scholar 

  21. D. Gutierrez and J. Arbesman, Circadian Dysrhythmias, Physiological Aberrations, and the Link to Skin Cancer, Int. J. Mol. Sci., 2016, 17, 621.

    Article  PubMed Central  CAS  Google Scholar 

  22. A. J. Luber, S. H. Ensanyat and J. A. Zeichner, Therapeutic implications of the circadian clock on skin function, J. Drugs Dermatol, 2014, 13, 130–134.

    PubMed  Google Scholar 

  23. M. S. Matsui, E. Pelle, K. Dong and N. Pernodet, Biological Rhythms in the Skin, Int. J. Mol. Sci., 2016, 17, 801.

    Article  PubMed Central  CAS  Google Scholar 

  24. M. V. Plikus, E. N. Van Spyk, K. Pham, M. Geyfman, V. Kumar, J. S. Takahashi and B. Andersen, The circadian clock in skin: implications for adult stem cells, tissue regeneration, cancer, aging, and immunity, J. Biol Rhythms, 2015, 30, 163–182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. C. Sandu, M. Dumas, A. Malan, D. Sambakhe, C. Marteau, C. Nizard, S. Schnebert, E. Perrier, E. Challet, P. Pevet and M. P. Felder-Schmittbuhl, Human skin keratinocytes, melanocytes, and fibroblasts contain distinct circadian clock machineries, Cell Mol Life Scl, 2012, 69, 3329–3339.

    Article  CAS  Google Scholar 

  26. G. Yosipovitch, L. Sackett-Lundeen, A. Goon, C. Yiong Huak, C. Leok Goh and E. Haus, Circadian and ultradian (12 h) variations of skin blood flow and barrier function in non-irritated and irritated skin-effect of topical corticosteroids, J. Invest. Dermatol, 2004, 122, 824–829.

    Article  CAS  PubMed  Google Scholar 

  27. I. Le Fur, A. Reinberg, S. Lopez, F. Morizot, M. Mechkouri and E. Tschachler, Analysis of circadian and ultradian rhythms of skin surface properties of face and forearm of healthy women, J. Invest. Dermatol, 2001, 117, 718–724.

    Article  PubMed  Google Scholar 

  28. G. Yosipovitch, G. L. Xiong, E. Haus, L. Sackett-Lundeen, I. Ashkenazi and H. I. Maibach, Time-dependent variations of the skin barrier function in humans: transepidermal water loss, stratum corneum hydration, skin surface pH, and skin temperature, J. Invest. Dermatol, 1998, 110, 20–23.

    Article  CAS  PubMed  Google Scholar 

  29. N. Matsunaga, K. Itcho, K. Hamamura, E. Ikeda, H. Ikeyama, Y. Furuichi, M. Watanabe, S. Koyanagi and S. Ohdo, 24-hour rhythm of aquaporin-3 function in the epidermis is regulated by molecular clocks, J. Invest. Dermatol, 2014, 134, 1636–1644.

    Article  CAS  PubMed  Google Scholar 

  30. S. Gaddameedhi, C. P. Selby, W. K. Kaufmann, R. C. Smart and A. Sancar, Control of skin cancer by the circadian rhythm, Proc. Natl Acad. Sci. U. S. A, 2011, 108, 18790–18795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. M. Geyfman, V. Kumar, Q. Liu, R. Ruiz, W. Gordon, F. Espitia, E. Cam, S. E. Millar, P. Smyth, A. Ihler, J. S. Takahashi and B. Andersen, Brain and muscle Arntlike protein-1 (BMALl) controls circadian cell proliferation and susceptibility to UVB-induced DNA. damage in the epidermis, Proc. Natl Acad. Sci. U. S. A., 2012, 109, 11758–11763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. J. A. Hardman, D. J. Tobin, I. S. Haslam, N. Farjo, B. Farjo, Y. Al-Nuaimi, B. Grimaldi and R. Paus, The peripheral clock regulates human pigmentation, J. Invest. Dermatol, 2015, 135, 1053–1064.

    Article  CAS  PubMed  Google Scholar 

  33. M. Tanioka, H. Yamada, M. Doi, H. Bando, Y. Yamaguchi, C. Nishigori and H. Okamura, Molecular clocks in mouse skin, J. Invest. Dermatol, 2009, 129, 1225–1231.

    Article  CAS  PubMed  Google Scholar 

  34. B. Iyengar, The melanocyte photosensory system in the human skin, SpringerPlus, 2013, 2, 158.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. G. J. Lopes, C. C. Gois, L. H. Lima and A. M. Castrucci, Modulation of rhodopsin gene expression and signaling mechanisms evoked by endothelins in goldfish and murine pigment cell lines, Braz.J. Med. Biol. Res., 2010, 43, 828–836.

    Article  CAS  PubMed  Google Scholar 

  36. Y. Miyashita, T. Moriya, T. Kubota, K. Yamada and K. Asami, Expression of opsin molecule in cultured murine melanocyte, J. Invest. Dermatol. Symp. Proc, 2001, 6, 54–57.

    Article  CAS  Google Scholar 

  37. M. Tsutsumi, K. Ikeyama, S. Denda, J. Nakanishi, S. Fuziwara, H. Aoki and M. Denda, Expressions of rod and cone photoreceptor-like proteins in human epidermis, Exp. Dermatol, 2009, 18, 567–570.

    Article  CAS  PubMed  Google Scholar 

  38. K. Haltaufderhyde, R. N. Ozdeslik, N. L. Wicks, J. A. Najera and E. Oancea, Opsin expression in human epidermal skin, Photochem. Photobiol, 2015, 91, 117–123.

    Article  CAS  PubMed  Google Scholar 

  39. N. W. Bellono, L. G. Kammel, A. L. Zimmerman and E. Oancea, UV. light phototransduction activates transient receptor potential Al ion channels in human melanocytes, Proc. Natl Acad. Sci. U. S. A, 2013, 110, 2383–2388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. H. J. Kim, E. D. Son, J. Y. Jung, H. Choi, T. R. Lee and D. W. Shin, Violet light down-regulates the expression of specific differentiation markers through Rhodopsin in normal human epidermal keratinocytes, PLoS. One, 2013, 8, e73678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. N. L. Wicks, J. W. Chan, J. A. Najera, J. M. Ciriello and E. Oancea, UVA. phototransduction drives early melanin synthesis in human melanocytes, Curr. Biol, 2011, 21, 1906–1911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. E. Dupont, J. Gomez and D. Bilodeau, Beyond UV radiation: a skin under challenge, Int. J. Cosmet. Sci., 2013, 35, 224–232.

    Article  CAS  PubMed  Google Scholar 

  43. L. R. Sklar, F. Almutawa, H. W. Lim and I. Hamzavi, Effects of ultraviolet radiation, visible light, and infrared radiation on erythema and pigmentation: a review, Photochem. Photobiol Sci., 2013, 12, 54–64.

    Article  CAS  PubMed  Google Scholar 

  44. C. Fortes and E. de Vries, Nonsolar occupational risk factors for cutaneous melanoma, Int. J. Dermatol, 2008, 47, 319–328.

    Article  PubMed  Google Scholar 

  45. H. S. Lee, D. H. Lee, S. Cho and J. H. Chung, Minimal heating dose: a novel biological unit to measure infrared irradiation, Photo dermatol, Photoimmunol Photomed., 2006, 22, 148–152.

    Article  Google Scholar 

  46. L. Calapre, E. S. Gray and M. Ziman, Heat stress: a risk factor for skin carcinogenesis, Cancer Lett, 2013, 337, 35–40.

    Article  CAS  PubMed  Google Scholar 

  47. J. S. Dover, T. J. Phillips and K. A. Arndt, Cutaneous effects and therapeutic uses of heat with emphasis on infrared radiation, J. Am. Acad. Dermatol, 1989, 20, 278–286.

    Article  CAS  PubMed  Google Scholar 

  48. L. H. Kligman, Intensification of ultraviolet-induced dermal damage by infrared radiation, Arch. Dermatol. Res., 1982, 272, 229–238.

    Article  CAS  PubMed  Google Scholar 

  49. L. H. Kligman and A. M. Kligman, Reflections on heat, Br. J. Dermatol, 1984, 110, 369–375.

    Article  CAS  PubMed  Google Scholar 

  50. D. C. Bennett, P. J. Cooper and I. R. Hart, A line of non-tumorigenic mouse melanocytes, syngeneic with the B16 melanoma and requiring a tumour promoter for growth, Int. J. Cancer, 1987, 39, 414–418.

    Article  CAS  PubMed  Google Scholar 

  51. C. Riccardi and I. Nicoletti, Analysis of apoptosis by propi-dium iodide staining and flow cytometry, Nat. Protoc, 2006, 1, 1458–1461.

    Article  CAS  PubMed  Google Scholar 

  52. K. J. Livak and T. D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR. and the 2(-DeIta Delta C(T)) Method, Methods, 2001, 25, 402–408.

    Article  CAS  PubMed  Google Scholar 

  53. M. Kajstura, H. D. Halicka, J. Pryjma and Z. Darzynkiewicz, Discontinuous fragmentation of nuclear DNA. during apoptosis revealed by discrete “sub-G1” peaks on DNA. content histograms, Cytometry, Part A, 2007, 71, 125–131.

    Article  CAS  Google Scholar 

  54. E. D. Buhr, W. W. Yue, X. Ren, Z. Jiang, H. W. Liao, X. Mei, S. Vemaraju, M. T. Nguyen, R. R. Reed, R. A. Lang, K. W. Yau and R. N. Van Gelder, Neuropsin (OPN5)-mediated photoentrainment of local circadian oscillators in mammalian retina and cornea, Proc. Natl Acad. Sci. U. S. A., 2015, 112, 13093–13098.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. D. Kojima, S. Mori, M. Torii, A. Wada, R. Morishita and Y. Fukada, UV-sensitive photoreceptor protein OPN5 in humans and mice, PLoS. One, 2011, 6, e26388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Y. J. Hwang, H. J. Park, H. J. Hahn, J. Y. Kim, J. H. Ko, Y. W. Lee, Y. B. Choe and K. J. Ahn, Immediate pigment darkening and persistent pigment darkening as means of measuring the ultraviolet A. protection factor in vivo: a comparative study, Br. J. Dermatol, 2011, 164, 1356–1361.

    Article  CAS  PubMed  Google Scholar 

  57. S. D. McAlear, T. W. Kraft and A. K. Gross, 1 rhodopsin mutations in congenital night blindness, Adv. Exp. Med. Biol, 2010, 664, 263–272.

    Article  CAS  PubMed  Google Scholar 

  58. M. C. Isoldi, M. D. Rollag, A. M. Castrucci and I. Provencio, Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin, Proc. Natl Acad. Sci. U. S. A., 2005, 102, 1217–1221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. M. N. Moraes, L. H. Lima, B. C. Ramos, M. O. Poletini and A. M. Castrucci, Endothelin modulates the circadian expression of non-visual opsins, Gen. Comp. Endocrinol, 2014, 205, 279–286.

    Article  CAS  PubMed  Google Scholar 

  60. I. Provencio, G. Jiang, W. J. De Grip, W. P. Hayes and M. D. Rollag, Melanopsin: An opsin in melanophores, brain, and eye, Proc. Natl Acad. Sci. U. S. A., 1998, 95, 340–345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. G. Sikka, G. P. Hussmann, D. Pandey, S. Cao, D. Hori, J. T. Park, J. Steppan, J. H. Kim, V. Barodka, A. C. Myers, L. Santhanam, D. Nyhan, M. K. Halushka, R. C. Koehler, S. H. Snyder, L. A. Shimoda and D. E. Berkowitz, Melanopsin mediates light-dependent relaxation in blood vessels, Proc. Natl Acad. Sci. U. S. A., 2014, 111, 17977–17982.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. H. Imai, V. Kefalov, K. Sakurai, O. Chisaka, Y. Ueda, A. Onishi, T. Morizumi, Y. Fu, K. Ichikawa, K. Nakatani, Y. Honda, J. Chen, K. W. Yau and Y. Shichida, Molecular properties of rhodopsin and rod function, J. Biol Chem., 2007, 282, 6677–6684.

    Article  CAS  PubMed  Google Scholar 

  63. M. Brenner and V. J. Hearing, The protective role of melanin against UV. damage in human skin, Photochem. Photobiol, 2008, 84, 539–549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. C. F. M. Menck and V. Munford, DNA. repair diseases: What do they tell us about cancer and aging?, Genet. Mol Biol, 2014, 37, 220–233.

    Article  CAS  PubMed  Google Scholar 

  65. S. Cho, M. H. Shin, Y. K. Kim, J. E. Seo, Y. M. Lee, C. H. Park and J. H. Chung, Effects of infrared radiation and heat on human skin aging in vivo, J. Invest. Dermatol Symp. Proc, 2009, 14, 15–19.

    Article  CAS  Google Scholar 

  66. V. Cavallari, R. Cicciarello, V. Torre, M. E. Gagliardi, F. Albiero, R. Palazzo, M. Siragusa and C. Schipis, Chronic heat-induced skin lesions (erythema ab Igne): ultrastructural studies, Ultrastruct. Pathol, 2001, 25, 93–97.

    Article  CAS  PubMed  Google Scholar 

  67. L. Calapre, E. S. Gray, S. Kurdykowski, A. David, P. Hart, P. Descargues and M. Ziman, Heat-mediated reduction of apoptosis in UVB-damaged keratinocytes in vitro and in human skin ex vivo, BMC. Dermatol., 2016, 16, 6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. J. C. van der Leun, R. D. Piacentini and F. R. de GruijI, Climate change and human skin cancer, Photochem. Photobiol. Sci., 2008, 7, 730–733.

    Article  PubMed  CAS  Google Scholar 

  69. R. Jeronimo, M. N. Moraes, L. V. M. de Assis, B. C. Ramos, T. C. Rocha and A. M. L. Castrucci, Thermal Stress in Danio rerio: a Link between Temperature, Light, Thermo-TRP. Channels, and Clock Genes, J. Therm. Biol, 2016, Accepted manuscript.

    Google Scholar 

  70. N. Hamilton, N. Diaz-de-Cerio and D. Whitmore, Impaired light detection of the circadian clock in a zebrafish melanoma model, Cell Cycle, 2015, 14, 1232–1241.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Z. Lengyel, C. Lovig, S. Kommedal, R. Keszthelyi, G. Szekeres, Z. Battyani, V. Csernus and A. D. Nagy, Altered expression patterns of clock gene mRNAs and clock proteins in human skin tumors, Tumour Biol, 2013, 34, 811–819.

    Article  CAS  PubMed  Google Scholar 

  72. D. Hanahan and R. A. Weinberg, The hallmarks of cancer, Cell, 2000, 100, 57–70.

    Article  CAS  PubMed  Google Scholar 

  73. D. Hanahan and R. A. Weinberg, Hallmarks of cancer: the next generation, Cell, 2011, 144, 646–674.

    Article  CAS  PubMed  Google Scholar 

  74. T. H. Kang, L. A. Lindsey-Boltz, J. T. Reardon and A. Sancar, Circadian control of XPA. and excision repair of cisplatin-DNA. damage by cryptochrome and HERC2 ubiquitin ligase, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 4890–4895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. T. H. Kang, J. T. Reardon, M. Kemp and A. Sancar, Circadian oscillation of nucleotide excision repair in mammalian brain, Proc. Natl. Acad. Sci. U. S. A., 2009, 106, 2864–2870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. S. Gaddameedhi, C. P. Selby, M. G. Kemp, R. Ye and A. Sancar, The circadian clock controls sunburn apoptosis and erythema in mouse skin, J. Invest. Dermatol, 2015, 135, 1119–1127.

    Article  CAS  PubMed  Google Scholar 

  77. A. R. Muotri, M. C. N. Marchetto, M. F. Suzuki, K. Okazaki, C. F. P. Lotfi, G. Brumatti, G. P. Amarante-Mendes and C. F. M. Menck, Low amounts of the DNA. repair XPA. protein are sufficient to recover UV-resistance, Carcinogenesis, 2002, 23, 1039–1046.

    Article  CAS  PubMed  Google Scholar 

  78. A. Daponte, P. A. Ascierto, A. Gravina, M. Melucci, S. Scala, A. Ottaiano, E. Simeone, G. Palmieris and G. Cornelia, Temozolomide and cisplatin in avdanced malignant melanoma, Anticancer Res., 2005, 25, 1441–1447.

    CAS  PubMed  Google Scholar 

  79. H. Helmbach, E. Rossmann, M. A. Kern and D. Schadendorf, Drug-resistance in human melanoma, Int. J. Cancer, 2001, 93, 617–622.

    Article  CAS  PubMed  Google Scholar 

  80. A. Slominski, D. J. Tobin, S. Shibahara and J. Wortsman, Melanin pigmentation in mammalian skin and its hormonal regulation, Physiol. Rev., 2004, 84, 1155–1228.

    Article  CAS  PubMed  Google Scholar 

  81. J. Y. Lin and D. E. Fisher, Melanocyte biology and skin pigmentation, Nature, 2007, 445, 843–850.

    Article  CAS  PubMed  Google Scholar 

  82. G. H. Findlay and L. W. Van der Merwe, The Meirowsky phenomenon. Colour changes in melanin according to temperature and redox potential, Br. J. Dermatol, 1966, 78, 572–576.

    Article  CAS  PubMed  Google Scholar 

  83. K. Maeda and M. Hatao, Involvement of photooxidation of melanogenic precursors in prolonged pigmentation induced by ultraviolet A. J. Invest. Dermatol, 2004, 122, 503–509.

    Article  CAS  PubMed  Google Scholar 

  84. K. Nakazawa, F. Sahuc, O. Damour, C. Collombel and H. Nakazawa, Regulatory effects of heat on normal human melanocyte growth and melanogenesis: comparative study with UVB, J. Invest. Dermatol, 1998, 110, 972–977.

    Article  CAS  PubMed  Google Scholar 

  85. T. B. Fitzpatrick and G. Szabo, Part III: General Considerations of Skin Pigmentation: The Melanocyte: Cytology and Cytochemistryl, J. Invest. Dermatol, 1959, 32, 197–206.

    Article  CAS  PubMed  Google Scholar 

  86. S. H. Kidson and B. C. Fabian, The effect of temperature on tyrosinase activity in Himalayan mouse skin, J. Exp. Zool, 1981, 215, 91–97.

    Article  CAS  PubMed  Google Scholar 

  87. F. G. Benedict, W. R. Miles and A. Johnson, The Temperature of the Human Skin, Proc. Natl Acad. Sci. U. S.A., 1919, 5, 218–222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. D. S. Kim, S. H. Park, S. B. Kwon, Y. H. Joo, S. W. Youn, U. D. Sohn and K. C. Park, Temperature regulates melanin synthesis in melanocytes, Arch. Pharmacol Res., 2003, 26, 840–845.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Electronic supplementary information (ESI) available. See DOI: 10.1039/C6pp00330c

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Assis, L.V.M., Moraes, M.N. & de Lauro Castrucci, A.M. Heat shock antagonizes UVA-induced responses in murine melanocytes and melanoma cells: an unexpected interaction. Photochem Photobiol Sci 16, 633–648 (2017). https://doi.org/10.1039/c6pp00330c

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c6pp00330c

Navigation