Skip to main content

Advertisement

SpringerLink
Log in

Effect of 17β-estradiol on immunosuppression induced by ultraviolet B irradiation

  • Original Paper
  • Published:
Archives of Dermatological Research Aims and scope Submit manuscript

Abstract

Background

The risk of skin cancer is lower in females than in males, and photoimmunosuppression caused by ultraviolet (UV) radiation is thought to be involved in the progression of skin cancer.

Objectives

To determine the effect of 17β-estradiol on immunosuppression and contact hypersensitivity (CHS) caused by ultraviolet B (UVB) irradiation.

Methods

Systemic immunosuppression was induced in C57BL mice that had been sensitized with 0.5% fluorescein isothiocyanate (FITC) through the skin by a single exposure to UVB (10 kJ/m2). The CHS response was assessed after applying FITC to mice treated intraperitoneally with 17β-estradiol, tamoxifen (17β-estradiol antagonist), or antiestradiol antibody. Levels of serum interleukin-10 (IL-10) were measured in treated mice and control mice using an enzyme-linked immunosorbent assay (ELISA). To assess the effect of 17β-estradiol on keratinocytes, Pam-212 cells were exposed in vitro to UVB radiation and treated for 24 h with 17β-estradiol. The IL-10 content of the supernatant was measured using an ELISA.

Results

The CHS response in UVB-irradiated mice was significantly suppressed in comparison to that in nonirradiated mice. Consecutive intraperitoneal injections of 17β-estradiol significantly reduced UVB-induced suppression of the CHS response in male mice, whereas injection of tamoxifen or antiestradiol antibody significantly promoted UVB-induced suppression in female mice. Treatment with 17β-estradiol decreased the serum IL-10 levels in CHS-suppressed male mice after UVB irradiation, but treatment with tamoxifen or antiestradiol antibody increased the serum IL-10 levels in female mice. Treatment with 17β-estradiol reduced IL-10 production by UVB-irradiated Pam-212 cells in a dose-dependent manner.

Conclusions

These results suggest that 17β-estradiol prevents UVB-induced suppression of the CHS response caused by immunosuppressive cytokines produced by keratinocytes.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Thiersch K (1875) Der Epithelialkrebs, Namentlich der ausseren. Haut, Leipzig

  2. Scotto J, Fraumeni JF Jr (1981) Skin (other than melanoma). In: Schaffenfeld D, Fraumeni JF Jr (eds) Cancer epidemiology and prevention. W.B. Saunders, Philadelphia, pp 996–1011

  3. Kripke ML (1974) Antigenicity of murine skin tumors induced by UV light. J Natl Cancer Inst 53:1333–1336

    CAS  PubMed  Google Scholar 

  4. Fisher MS, Kripke MS (1977) Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc Natl Acad Sci U S A 74:1688–1692

    CAS  PubMed  Google Scholar 

  5. Toews GB, Bergstresser PR, Streilein JW (1980) Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J Immunol 12:445–453

    Google Scholar 

  6. Jeevan A, Kripke ML (1989) Effect of a single exposure to ultraviolet radiation on Mycobacterium bovis bacillus Calmette-Guerin injection in mice. J Immunol 143:2837–2843

    CAS  PubMed  Google Scholar 

  7. Yoshikawa T, Rae V, Bruins-Slot W, Van den Berg J-W, Streilein JW (1990) Susceptibility to effects of UVB radiation on induction of contact hypersensitivity as a risk factor for skin cancer in humans. J Invest Dermatol 95:530–536

    CAS  PubMed  Google Scholar 

  8. Noonan FP, De Fabo EC, Morrison H (1988) Cis-urocannic acid, a product formed by ultraviolet B irradiation of the skin, initiates an antigen presentation defect in splenic dendritic cells in vivo. J Invest Dermatol 90:92–99

    CAS  PubMed  Google Scholar 

  9. Ullrich SE (1996) Does exposure to UV radiation induce a shift to a Th-2-like immune reaction? Photochem Photobiol 64:254–258

    CAS  PubMed  Google Scholar 

  10. Beissert S, Ullrich SE, Hosoi J, Granstein RD (1995) Supernatants from UVB radiation-exposed keratinocytes inhibit Langerhans cell presentation of tumor-associated antigen via IL-10 content. J Leukoc Biol 58:234–240

    CAS  PubMed  Google Scholar 

  11. Rivas JM, Ullrich SE (1992) Systemic suppression of delayed-type hypersensitivity by supernatants from UV-irradiated keratinocytes. An essential role for keratinocyte-derived IL-10. J Immunol 149:3865–3871

    CAS  PubMed  Google Scholar 

  12. Holman CDJ, Armstrong BK, Evans PR, Lumsden GJ, Dallimore KJ, Meehan CJ, Beagley J, Gibson IM (1984) Relationship of solar keratosis and history of skin cancer to objective measures of actinic skin damage. Br J Dermatol 110:129–138

    CAS  PubMed  Google Scholar 

  13. Harvey I, Frankel S, Marks R, Shalom D, Nolan-Farrell M (1996) Non-melanoma skin cancer and solar keratoses II analytical results of the South Wales Skin Cancer Study. Br J Cancer 74:1308–1312

    CAS  PubMed  Google Scholar 

  14. Yuspa ST, Hawley-Nelson P, Koehler B, Stanley JR (1980) A survey of transformation markers in differentiating epidermal cell lines in culture. Cancer Res 40:4694–4703

    CAS  PubMed  Google Scholar 

  15. Naganuma M, Yagi E, Yamase Y, Fukuda H (1995) High ultraviolet sensitivity in males. Jpn J Dermatol 105:1427–1430

    Google Scholar 

  16. Robertson B, Gahring L, Newton R, Daynes RA (1987) In vivo administration of IL-1 to normal mice depresses their capacity to elicit contact hypersensitivity responses: prostaglandins are involved in this modification of immune function. J Invest Dermatol 88:380–387

    CAS  PubMed  Google Scholar 

  17. Vermeer M, Streilein JW (1990) Ultraviolet B light-induced alterations in epidermal Langerhans cells are mediated in part by tumor necrosis factor-alpha. Photodermatol Photoimmunol Photomed 7:258–265

    CAS  PubMed  Google Scholar 

  18. Rivas JM, Ullrich SE (1994) The role of IL-4, IL-10, and TNF-a in the immune suppression induced by ultraviolet radiation. J Leukoc Biol 56:769–775

    CAS  PubMed  Google Scholar 

  19. Byeon SW, Pelley RP, Ullrich SE, Waller TA, Bucana CD, Strickland FM (1998) Aloe barbadensis extracts reduce the production of interleukin-10 after exposure to ultraviolet radiation. J Invest Dermatol 110:811–817

    Article  CAS  PubMed  Google Scholar 

  20. Kurimoto I, Kitazawa T, Streilein JW (2000) Studies of delayed systemic effects of ultraviolet B radiation (UVR) on the induction of contact hypersensitivity, 2. Evidence that interleukin-10 from UVR-treated epidermis is the critical mediator. Immunology 99:134–140

    Article  CAS  PubMed  Google Scholar 

  21. Kitazawa T, Streilein JW (2000) Studies on delayed systemic effects of ultraviolet B radiation on the induction of contact hypersensitivity, 3. Dendritic cells from secondary lymphoid organs are deficient in interleukin-12 production and capacity to promote activation and differentiation of T helper type 1 cells. Immunology 99:296–304

    Article  CAS  PubMed  Google Scholar 

  22. Kang K, Gilliam AC, Chen G, Tootell E, Cooper KD (1998) In human skin, UVB initiates early induction of IL-10 over IL-12 preferentially in the expanding dermal monocytic/macrophagic population. J Invest Dermatol 111:31–38

    Article  CAS  PubMed  Google Scholar 

  23. Shreedhar VK, Pride MW, Sun Y, Kripke ML, Strickland FM (1998) Origin and characteristics of ultraviolet-B radiation-induced suppressor T lymphocytes. J Immunol 161:1327–1335

    CAS  PubMed  Google Scholar 

  24. Streilein JW, Alard P, Niizeki H (1999) Neural influences on induction of contact hypersensitivity. Ann N Y Acad Sci 885:196–208

    CAS  PubMed  Google Scholar 

  25. Carruba G, D’Agostino P, Miele M, Calabro M, Barbera C, Bella GD, Milano S, Ferlazzo V, Caruso R, Rosa ML, Cocciadiferro L, Campisi I, Castagnetta L, Cillari E (2003) Estrogen regulates cytokine production and apoptosis in PMA-differentiated, macrophage-like U937 cells. J Cell Biochem 90:187–196

    Article  CAS  PubMed  Google Scholar 

  26. Malabarba MG, Rui H, Deutsch HH, Chung J, Kaithoff FS, Farrar WL, Kirken RA (1996) Interleukin-13 is a potent activator of JAK 3 and STAT6 in cells expressing interlukin-2 receptor-gamma and interleukin-4 receptor alpha. Biochem J 329:865–872

    Google Scholar 

  27. Schmitt DA, Owen-Schaub L, Ullrich SE (1995) Effect of IL-12 on immune suppression and suppressor cell induction by ultraviolet radiation. J Immunol 154:5114–5120

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Pathology, Osaka City University Medical School, 1-4-3 Asahimachi, Abeno-ku, 545-8585, Osaka City, Osaka, Japan

    Keiichi Hiramoto, Eisuke F. Sato & Masayasu Inoue

  2. Research Laboratory, Nihon Menard Cosmetic Co. Ltd., 4-6 Trimi, Nishi-ku, 451-0071, Nagoya City, Aichi, Japan

    Hiroshi Tanaka

  3. Department of Ophthalmology, Osaka City Juso Hospital, 2-12-27 Nonakakita, Yodogawa-ku, 532-0034, Osaka City, Osaka, Japan

    Nobuyo Yanagihara

Authors
  1. Keiichi Hiramoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroshi Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nobuyo Yanagihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eisuke F. Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masayasu Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keiichi Hiramoto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hiramoto, K., Tanaka, H., Yanagihara, N. et al. Effect of 17β-estradiol on immunosuppression induced by ultraviolet B irradiation. Arch Dermatol Res 295, 307–311 (2004). https://doi.org/10.1007/s00403-003-0437-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00403-003-0437-0

Keywords

Search

Navigation