Skip to main content
Log in

Adaptation to the UV-induced suppression of phagocytic activity in murine peritoneal macrophages following chronic exposure to solar simulated radiation

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

Abstract

Exposure of certain strains of mice to ultraviolet radiation (UVR) is known to suppress both local and systemic immune responses, including a reduction in the phagocytic activity of peritoneal macrophages. However, in many instances, the immunological effects have been observed following a single or a limited number of doses of UVR from sources containing a higher proportion of UVB than that emitted by the sun. The first aim of the present study was to establish whether a single exposure of C3H/HeN mice to solar simulated radiation (SSR) suppressed the ability of the peritoneal macrophages to phagocytose opsonised sheep red blood cells. The mice were irradiated with SSR from Cleo Natural lamps and a single dose of 31.9 J cm−2 was found to be the minimal dose for significant suppression of macrophage phagocytic activity. Such a dose did not modulate the surface expression of I-Ak, CD11b, CD86 or FcγRII/III (CD32/16) on the macrophages. The second aim was to assess whether repeated SSR exposures with a dose below the minimal immunosuppressive dose affected macrophage activity and, if so, to test for photoadaptation by repeated exposures followed by a single, normally immunosuppressive dose of SSR, and then assaying the macrophage activity. Groups of mice were irradiated on each of 2, 10 and 30 days with 14.9 J cm−2 SSR, followed in some instances by a single additional exposure of 31.9 J cm−2 on the same day as the last irradiation. The phagocytic activity of the peritoneal macrophages was tested 24 h later. It was reduced by 32%, 18% and 4% respectively after 2, 10 and 30 repeated exposures to SSR, and by 39%, 21% and 7% respectively after 2, 10 and 30 repeated exposures plus the additional higher dose at the end. Thus, although the macrophage activity was initially suppressed by the SSR, photoadaptation of this immune parameter occurred following repeated exposures.

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

References

  1. G. J. Clydesdale, G. W. Dandie and H. K. Muller, Ultraviolet light induced injury: immunological and inflammatory effects, Immunol. Cell Biol., 2001, 79, 547–568.

    Article  CAS  Google Scholar 

  2. B. L. Diffey, Sources and measurement of ultraviolet radiation, Methods, 2002, 28, 4–13.

    Article  CAS  Google Scholar 

  3. A. Jeevan, C. D. Bucana, Z. Dong, V. V. Dizon, S. L. Thomas, T. E. Lloyd and M. L. Kripke, Ultraviolet radiation reduces phagocytosis and intracellular killing of mycobacteria and inhibits nitric oxide production by macrophages in mice, J. Leukocyte Biol., 1995, 57, 883–890.

    Article  CAS  Google Scholar 

  4. S. Kasahara, K. Aizawa, M. Okamiya, N. Kazuno, S. Mutoh, H. Fugo, E. L. Cooper and H. Wago, UVB irradiation suppresses cytokine production and innate cellular immune functions in mice, Cytokine, 2001, 14, 104–111.

    Article  CAS  Google Scholar 

  5. K. C. Norbury, M. L. Kripke and M. B. Budmed, In vitro reactivity of macrophages and lymphocytes from ultraviolet-irradiated mice, J. Natl. Cancer Inst., 1977, 59, 1231–1235.

    Article  CAS  Google Scholar 

  6. COLIPA sun protection factor test method, European Cosmetic, Toiletry, and Perfumery Association, Brussels, 1994.

  7. J. M. Kuchel, R. St. C. Barnetson, L. Zhuang, F. M. Strickland, R. P. Pelley and G. M. Halliday, Tamarind inhibits solar-simulated ultraviolet radiation-induced suppression of recall responses in humans, Lett. Drug Des. Discovery, 2005, 2, 165–171.

    Article  CAS  Google Scholar 

  8. P. McLoone and M. Norval, Decrease in Langerhans cells and increase in lymph node dendritic cells following chronic exposure of mice to suberythemal doses of solar simulated radiation, Photochem. Photobiol., in press.

  9. J. Narbutt, A. Lesiak, M. Skibinska, A. Wozniacka, H. van Loveren, A. Sysa-Jedrzejowska, I. Lewy-Trenda, A. Omulecka and M. Norval, Suppression of contact hypersensitivity after repeated exposures of humans to low doses of solar simulated radiation, Photochem. Photobiol. Sci., 2005, 4, 517–522.

    Article  CAS  Google Scholar 

  10. J. W. Streilein and P. R. Bergstresser, Genetic basis of ultraviolet-B effects on contact hypersensitivity, Immunogenetics, 1988, 27, 252–258.

    Article  CAS  Google Scholar 

  11. F. P. Noonan and H. A. Hoffman, Susceptibility to immunosuppression by ultraviolet B radiation in the mouse, Immunogenetics, 1994, 39, 29–39.

    Article  CAS  Google Scholar 

  12. T. Yoshikawa and J. W. Streilein, Genetic basis of the effects of ultraviolet light B on cutaneous immunity. Evidence that polymorphism at the Tnfα and Lps loci governs susceptibility, Immunogenetics, 1990, 32, 398–405.

    Article  CAS  Google Scholar 

  13. V. Vincek, I. Kurimoto, J. Medema, E. Prieto and J. W. Streilein, Tumour necrosis factor α polymorphism correlates with deleterious effects of ultraviolet B light on cutaneous immunity, Cancer Res., 1993, 53, 728–732.

    CAS  PubMed  Google Scholar 

  14. G. Sethi and A. Sodhi, In vitro activation of murine peritoneal macrophages by ultraviolet B radiation: upregulation of CD18, production of NO, proinflammatory cytokines and a signal transduction pathway, Mol. Immunol., 2004, 40, 1315–1323.

    Article  CAS  Google Scholar 

  15. V. Shreedhar, T. Giese, V. W. Sung and S. E. Ullrich, A cytokine cascade including prostaglandin E2, interleukin-4 and interleukin-10 is responsible for UV induced systemic immune suppression, J. Immunol., 1998, 160, 3783–3789.

    CAS  PubMed  Google Scholar 

  16. D. A. Schmitt and S. E. Ullrich, Exposure to ultraviolet radiation causes dendritic cells/macrophages to secrete immune-suppressive IL-12p40 homodimers, J. Immunol., 2000, 165, 3162–3167.

    Article  CAS  Google Scholar 

  17. J. M. Weiss, A. C. Renkl, R. W. Denfeld, R. deRoche, M. Spitzlei, M., E. Schopf and J. C. Simon, Low-dose UVB radiation perturbs the functional expression of B7.1 and B7.2 co-stimulatory molecules on human Langerhans cells, Eur. J. Immunol., 1995, 10, 2858–2862.

    Article  Google Scholar 

  18. R. W. Denfeld, J. P. Tesmann, H. Dittmar, J. M. Weiss, E. Schopf, H. U. Weltzien and J. C. Simon, Further characterization of UVB radiation effects on Langerhans cells: altered expression of the costimulatory molecules B7.1 and B7.2, Photochem. Photobiol., 1998, 67, 554–560.

    Article  CAS  Google Scholar 

  19. F.-M. Rattis, M. Concha, C. Dalbiez-Gauthier, P. Courtellemont, D. Schmitt and J. Peguet-Navarro, Effects of Ultraviolet B radiation on human Langerhans cells: functional alteration of CD86 upregulation and induction of apoptotic cell death, J. Invest. Dermatol., 1998, 111, 373–379.

    Article  CAS  Google Scholar 

  20. K. Loser, A. Scherer, M. B. W. Krummen, G. Varga, T. Higuchi, T. Schwarz, A. H. Sharpe, S. Grabbe, J. A. Bluestone and S. Beissert, An important role of CD80/CD86-CTLA-4 signaling during photocarcinogenesis in mice, J. Immunol., 2005, 174, 5298–5305.

    Article  CAS  Google Scholar 

  21. L. Leino, K. Saarinen, K. Kivisto, L. Koulu, C. T. Jansen and K. Punnonen, Systemic suppression of human peripheral blood phagocytic leukocytes after whole-body UVB irradiation, J. Leukocyte Biol., 1999, 65, 573–582.

    Article  CAS  Google Scholar 

  22. S. Gorman, J. W.-Y. Tan, J. A. Thomas, S. L. Townley, P. A. Stumbles, J. J. Finlay-Jones and P. H. Hart, Primary defect in UVB-induced systemic immunomodulation does not relate to immature or functionally impaired APCs in regional lymph nodes, J. Immunol., 2005, 174, 6677–6685.

    Article  CAS  Google Scholar 

  23. S. N. Bryme and G. M. Halliday, B cells activated in lymph nodes in response to ultraviolet irradiation or by interleukin-10 inhibit dendritic cell induction of immunity, J. Invest. Dermatol., 2005, 124, 570–578.

    Article  Google Scholar 

  24. M. L. Kripke, J. S. Lofgreen, J. Beard, J. M. Jessup and M. S. Fisher, In vivo immune responses of mice during carcinogenesis by ultraviolet radiation, J. Natl. Cancer Inst., 1977, 59, 1227–1230.

    Article  CAS  Google Scholar 

  25. M. F. Gurish, D. H. Lynch and R. A. Daynes, Changes in antigen-presenting cell function in the spleen and lymph nodes of ultraviolet irradiated mice, Transplantation, 1982, 33, 280–284.

    Article  CAS  Google Scholar 

  26. D. L. Damian, G. M. Halliday, C. A. Taylor and R. St. C. Barnetson, Ultraviolet radiation induced suppression of Mantoux reactions in humans, J. Invest. Dermatol., 1998, 110, 824–827.

    Article  CAS  Google Scholar 

  27. D. L. Damian, R. St. C. Barnetson and G. M. Halliday, Low dose UVA and UVB have different time courses for suppression of contact hypersensitivity to a recall antigen in humans, J. Invest. Dermatol., 1999, 112, 939–944.

    Article  CAS  Google Scholar 

  28. V. E. Reeve, M. Bosnic, C. Boehm-Wilcox, N. Nishimura and 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 

  29. R. W. Gange, A. Blackell, E. A. Matzinger, B. M. Sutherland and I. E. Kochevar, Comparative protection efficiency of UVA- and UVB-induced tans against erythema and formation of endonuclease sensitive sites in DNA by UVB in human skin, J. Invest. Dermatol., 1985, 85, 362–364.

    Article  CAS  Google Scholar 

  30. B. Chaqour, S. Seite, K. Coutant, A. Fourtanier, J.-P. Borel and G. Bellon, Chronic UVB and all- trans retinoic-acid-induced qualitative and quantitative changes in hairless mouse skin, J. Photochem. Photobiol., B, 1995, 28, 125–135.

    Article  CAS  Google Scholar 

  31. J. Ruegemer, B. Schuetz, K. Hermann, R. Hein, J. Ring and D. Abeck, UV-induced skin changes due to regular use of commercial sunbeds, Photodermatol. Photoimmunol. Photomed., 2002, 18, 223–227.

    Article  CAS  Google Scholar 

  32. T. Gambichler, K. Sauermann, M. A. Altintas, V. Paech, A. Kreuter, P. Altmeyer and K. Hoffman, Effects of repeated sunbed exposures on the human skin. In vivo measurements with confocal microscopy, Photodermatol. Photoimmunol. Photomed., 2004, 20, 27–32.

    Article  CAS  Google Scholar 

  33. N. Bech-Thomsen, B. Munch-Peterson, K. Lundgren, T. Poulsen and H. C. Wulf, UV-induced alterations in skin and lymphocytes during a one week holiday in the Canary Islands in May, Acta Derm. Venereol., 1993, 73, 422–425.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary Norval.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McLoone, P., Norval, M. Adaptation to the UV-induced suppression of phagocytic activity in murine peritoneal macrophages following chronic exposure to solar simulated radiation. Photochem Photobiol Sci 4, 792–797 (2005). https://doi.org/10.1039/b503094c

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b503094c

Navigation