Skip to main content
SpringerLink
Log in

Estrogen receptor-beta signaling protects epidermal cytokine expression and immune function from UVB-induced impairment in mice

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

Abstract

A previous study in the hairless mouse, in which the photoimmune protective properties of a topical phytoestrogen or17-ß-estradiol were abrogated by the estrogen receptor antagonist ICI 182,780, revealed that estrogen receptor (Er) signaling is involved in the regulation of the suppression of immune function by UVB (290-320 nm) radiation. Here we identify the expression of Er-ß but not Er-a mRNA in hairless mouse skin, whereas Er-a and Er-ß mRNA were present in normal haired mouse skin. This suggests that the non-classical estrogen target Er-ß is involved in the photoimmune modulation, and is consistent with Er-a being more closely associated with hair growth control, as indicated by other studies. In mice with a null mutation for Er-ß, there was a significant exacerbation of the solar simulated UV (290-400 nm)-induced suppression of contact hypersensitivity. Immunohistochemical analysis revealed that the Er-ß deficiency inhibited the normally immunoprotective upregulation by the UVA (320-400 nm) waveband of the epidermal expression of the cytokines IFN-λ and IL-12. Er-ß deficiency also significantly increased the UVB-induced expression of the immunosuppressive cytokine IL-10. Thus Er signalling via the Er-ß is evidently a major regulator of the UVA and UVB waveband interactions that determine the skin’s immune functional status, and achieves this by normalization of the cutaneous cytokine array in the UV-irradiated skin.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. S. Widyarini, D. Domanski, N. Painter, V. E. Reeve, Estrogen signalling protects against immune suppression by UV radiation exposure, Proc. Natl. Acad. Sci. USA, 2006, 103, 12837–12842.

    Article  CAS  Google Scholar 

  2. S. Widyarini, N. Spinks, A. J. Husband, V. E. Reeve, Isoflavonoid compounds from red clover (Trifolium pratense) protect from inflammation and immune suppression induced by UV radiation, Photochem. Photobiol., 2001, 74, 465–470.

    Article  CAS  Google Scholar 

  3. S. E. Ullrich, Review. Mechanisms underlying UV-induced immune suppression, Mutat. Res., 2005, 571, 185–205.

    Article  CAS  Google Scholar 

  4. M. Norval, Review. The mechanisms and consequences of ultraviolet-induced immunosuppression, Progr. Biophys. Mol. Biol., 2006, 92, 108–118.

    Article  CAS  Google Scholar 

  5. R. M. Tyrrell, V. E. Reeve, Potential protection of skin by acute UVA irradiation-From cellular to animal models, Progr. Biophys. Mol. Biol., 2006, 92, 86–91.

    Article  CAS  Google Scholar 

  6. V. E. Reeve, M. Bosnic, C. Boehm-Wilcox, N. Nishimura, R. D. Ley, Ultraviolet A radiation (320-400 nm) protects hairless mice from immunosuppression induced by ultraviolet B radiation (280-320 nm) or cis-urocanic acid, Int. Arch. Allergy Immunol., 1998, 115, 316–322.

    Article  CAS  Google Scholar 

  7. V. E. Reeve, D. Domanski, M. Slater, Radiation sources providing increased UVA/UVB ratios induce UVA dose-dependently increased photoprotection in hairless mice, Photochem. Photobiol., 2006, 82, 406–411.

    Article  CAS  Google Scholar 

  8. J. Shen, S. Bao, V. E. Reeve, Modulation of IL-10, IL-12, and IFN-λ in the epidermis of hairless mice by UVA (320-400 nm) and UVB (280-320 nm) radiation, J. Invest. Dermatol., 1999, 113, 1059–1064.

    Article  CAS  Google Scholar 

  9. U. Ohnemus, M. Uenalan, F. Conrad, B. Handjiski, L. Mecklemburg, M. Nakamura, J. Inzunza, J.-A. Gustafsson, R. Paus, Hair cycle control by estrogens: Catagen induction via estrogen receptor (ER)-α is checked by ERß signalling, Endocrinology, 2005, 146, 1214–1225.

    Article  CAS  Google Scholar 

  10. M. Allanson, V. E. Reeve, Immunoprotective UVA (320-400 nm) irradiation upregulates heme oxygenase in the dermis and epidermis of hairless mouse skin, J. Invest. Dermatol., 2004, 122, 1030–1036.

    Article  CAS  Google Scholar 

  11. V. E. Reeve, Ultraviolet radiation and the contact hypersensitivity reaction in mice, Methods, 2002, 28, 20–40.

    Article  CAS  Google Scholar 

  12. H. S. Oh, R. C. Smart, An estrogen receptor pathway regulates the telogen-anagen hair follicle transition and influences epidermal cell proliferation, Proc. Natl. Acad. Sci. USA, 1996, 93, 12525–12530.

    Article  CAS  Google Scholar 

  13. S. Chanda, C. L. Robinette, J. F. Couse, R. C. Smart, 17ß-estradiol and ICI-182780 regulate the hair follicle cycle in mice through an estrogen receptor-a pathway, Am. J. Physiol. Endocrin. Metab., 2000, 278, E202–210.

    Article  CAS  Google Scholar 

  14. M. J. Thornton, A. H. Taylor, K. Mulligan, F. All-Azzawi, C. C. Lyon, J. O’Driscoll, A. G. Messenger, Oestrogen receptor beta is the predominant oestrogen receptor in human scalp, Exp. Dermatol., 2003, 12, 181–190.

    Article  CAS  Google Scholar 

  15. M. J. Thornton, A. H. Taylor, K. Mulligan, F. All-Azzawi, C. C. Lyon, J. O’Driscoll, A. G. Messenger, The distribution of estrogen receptor beta is distinct to that of estrogen receptor alpha and the androgen receptor in human skin, J. Invest. Dermatol. Symp. Proc., 2003, 8, 100–103.

    Article  CAS  Google Scholar 

  16. G. Pelletier, L. Ren, Localization of sex steroid receptors in human skin (Review), Histol. Histopath., 2004, 19, 629–636.

    CAS  Google Scholar 

  17. F. Hildebrand, W. J. Hubbard, M. A. Choudry, B. M. Thobe, H. C. Pape, I. H. Chaudry, Are the protective effects of 17beta-estradiol on splenic macrophages and splenocytes after trauma-hemorrhage mediated via estrogen-receptor (ER)-alpha or ER-beta?, J. Leukocyte Biol., 2006, 79, 1173–1180.

    Article  CAS  Google Scholar 

  18. T. Suzuki, T. Shimizu, H. P. Yu, Y. C. Hsieh, M. A. Chaudry, M. G. Schwacha, I. H. Chaudry, Tissue compartment-specific role of estrogen receptor subtypes in immune cell cytokine production following trauma-hemorrhage, J. Appl. Physiol., 2007, 102, 163–168.

    Article  CAS  Google Scholar 

  19. V. E. Reeve, R. M. Tyrrell, Heme oxygenase induction mediates the photoimmunoprotective activity of UVA radiation in the mouse, Proc. Natl. Acad. Sci. USA, 1999, 96, 9317–9321.

    Article  CAS  Google Scholar 

  20. T. Nakamura, G. Xi, R. F. Keep, M. Wang, S. Nagao, J. T. Hoff, Y. Hua, Effects of endogenous and exogenous estrogen on intracerebral hemorrhage-induced brain damage in rats, Acta Neurochirurgica-Suppl., 2006, 96, 218–221.

    Article  CAS  Google Scholar 

  21. H. P. Yu, T. Shimizu, Y. C. Hsieh, T. Suzuki, M. A. Choudry, M. G. Schwacha, I. H. Chaudry, Mechanism of the salutary effects of flutamide on intestinal myeloperoxidase activity following trauma-hemorrhage: upregulation of estrogen receptor-beta-dependent HO-1, J. Leukocyte Biol., 2006, 79, 963–970.

    Article  CAS  Google Scholar 

  22. M. Allanson, D. Domanski, V. E. Reeve, Photoimmunoprotection by UVA (320-400 nm) radiation is determined by UVA dose and is associated with cutaneous cyclic guanosine monophosphate, J. Invest. Dermatol., 2006, 126, 191–197.

    Article  CAS  Google Scholar 

  23. S. Y. Lee, T. Andoh, D. L. Murphy, C. C. Chiueh, 17beta-estradiol activates ICI 182,780-sensitive estrogen receptors and cyclic GMP-dependent thioredoxin expression for neuroprotection, FASEB J., 2003, 17, 947–948.

    CAS  PubMed  Google Scholar 

  24. M. M. Montano, B. S. Katzenellenbogen, The quinone reductase gene: a unique estrogen receptor-regulated gene that is activated by antiestrogens, Proc. Natl. Acad. Sci. USA, 1997, 94, 2581–2586.

    Article  CAS  Google Scholar 

  25. M. M. Montano, H. Deng, M. Liu, X. Sun, R. Singal, Transcriptional regulation by the estrogen receptor of antioxidative stress enzymes and its functional implications, Oncogene, 2004, 23, 2442–2453.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Veterinary Science, University of Sydney, Sydney, New South Wales, Australia

    Jun-Lae Cho, Munif Allanson, Diane Domanski, Sondur J. Arun & Vivienne E. Reeve

Authors
  1. Jun-Lae Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Munif Allanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Diane Domanski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sondur J. Arun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vivienne E. Reeve
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cho, JL., Allanson, M., Domanski, D. et al. Estrogen receptor-beta signaling protects epidermal cytokine expression and immune function from UVB-induced impairment in mice. Photochem Photobiol Sci 7, 120–125 (2008). https://doi.org/10.1039/b709856a

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b709856a

Search

Navigation