Sunlight triggers cutaneous lupus through a CSF-1-dependent mechanism in MRL-Faslpr mice

Journal of Immunology

Volumn 181, Issue 10, 2008, Pages 7367-7379

  Menke, Julia ^a   Hsu, Mei Yu ^a   Byrne, Katelyn T ^a   Lucas, Julie A ^a   Rabacal, Whitney A ^a   Croker, Byron P ^b   Zong, Xiao Hua ^c   Stanley, E Richard ^c   Kelley, Vicki Rubin ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; FAS ANTIGEN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; EX VIVO GENE TRANSFER; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; KERATINOCYTE; MACROPHAGE; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN LUPUS ERYTHEMATOSUS; SUNLIGHT; ULTRAVIOLET B RADIATION; ADOPTIVE TRANSFER; ANIMAL; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; PATHOLOGY; SKIN DISEASE; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, INBRED MRL LPR; MICE, TRANSGENIC; SKIN DISEASES; SUNLIGHT;

EID: 58149182883     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.10.7367     Document Type: Article

References (58)

1. Lin, J. H., J. P. Dutz, R. D. Sontheimer, and V. P. Werth. 2007. Pathophysiology of cutaneous lupus erythematosus. Clin. Rev. Allergy Immunol. 33: 85-106.
2. Furukawa, F., and T. Yoshimasu. 2005. Animal models of spontaneous and drug-induced cutaneous lupus erythematosus. Autoimmun. Rev. 4: 345-350. (Pubitemid 41080071)
3. Werth, V. P. 2007. Cutaneous lupus: insights into pathogenesis and disease classification. Bull. NYU Hosp. Jt. Dis. 65: 200-204.
4. Synkowski, D. R., and T. T. Provost. 1983. Characterization of the inflammatory infiltrate in lupus erythematosus lesions using monoclonal antibodies. J. Rheumatol. 10: 920-924. (Pubitemid 14156284)
5. Kanauchi, H., F. Furukawa, and S. Imamura. 1991. Characterization of cutaneous infiltrates in MRL/lpr mice monitored from onset to the full development of lupus erythematosus-like skin lesions. J. Invest. Dermatol. 96: 478-483.
6. David-Bajar, K. M., and B. M. Davis. 1997. Pathology, immunopathology, and immunohistochemistry in cutaneous lupus erythematosus. Lupus 6: 145-157. (Pubitemid 27102042)
7. Furukawa, F., H. Kanauchi, H. Wakita, Y. Tokura, T. Tachibana, Y. Horiguchi, S. Imamura, S. Ozaki, and M. Takigawa. 1996. Spontaneous autoimmune skin lesions of MRL/n mice: autoimmune disease-prone genetic background in relation to Fas-defect MRL/1pr mice. J. Invest. Dermatol. 107: 95-100.
8. Alaibac, M., E. Berti, C. Chizzolini, S. Fineschi, A. V. Marzano, B. Pigozzi, E. Riboldi, S. Sozzani, and A. Kuhn. 2006. Role of cellular immunity in the pathogenesis of autoimmune skin diseases. Clin. Exp. Rheumatol. 24: S14 -19.
9. Clark, R. A., and T. S. Kupper. 2006. Misbehaving macrophages in the pathogenesis of psoriasis. J. Clin. Invest. 116: 2084-2087.
10. Clark, R., and T. Kupper. 2005. Old meets new: the interaction between innate and adaptive immunity. J. Invest. Dermatol. 125: 629-637.
11. Dupasquier, M., P. Stoitzner, A. van Oudenaren, N. Romani, and P. J. Leenen. 2004. Macrophages and dendritic cells constitute a major subpopulation of cells in the mouse dermis. J. Invest. Dermatol. 123: 876-879. (Pubitemid 39391932)
12. Kelly, M., J. M. Hwang, and P. Kubes. 2007. Modulating leukocyte recruitment in inflammation. J. Allergy Clin. Immunol. 120: 3-10.
13. Kiekens, R. C., T. Thepen, A. J. Oosting, I. C. Bihari, J. G. Van De Winkel, C. A. Bruijnzeel-Koomen, and E. F. Knol. 2001. Heterogeneity within tissuespecific macrophage and dendritic cell populations during cutaneous inflammation in atopic dermatitis. Br. J. Dermatol. 145: 957-965.
14. Wang, H., T. Peters, D. Kess, A. Sindrilaru, T. Oreshkova, N. Van Rooijen, A. Stratis, A. C. Renkl, C. Sunderkotter, M. Wlaschek, et al. 2006. Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation. J. Clin. Invest. 116: 2105-2114. (Pubitemid 44162319)
15. Stratis, A., M. Pasparakis, R. A. Rupec, D. Markur, K. Hartmann, K. Scharffetter-Kochanek, T. Peters, N. van Rooijen, T. Krieg, and I. Haase. 2006. Pathogenic role for skin macrophages in a mouse model of keratinocyte- induced psoriasis-like skin inflammation. J. Clin. Invest. 116: 2094-2104. (Pubitemid 44162318)
16. Tesch, G. H., A. Schwarting, K. Kinoshita, H. Y. Lan, B. J. Rollins, and V. R. Kelley. 1999. Monocyte chemoattractant protein-1 promotes macrophage-mediated tubular injury, but not glomerular injury, in nephrotoxic serum nephritis. J. Clin. Invest. 103: 73-80.
17. Cecchini, M. G., M. G. Dominguez, S. Mocci, A. Wetterwald, R. Felix, H. Fleisch, O. Chisholm, W. Hofstetter, J. W. Pollard, and E. R. Stanley. 1994. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120: 1357-1372.
18. Pixley, F. J., and E. R. Stanley. 2004. CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol. 14: 628-638.
19. Ginhoux, F., F. Tacke, V. Angeli, M. Bogunovic, M. Loubeau, X. M. Dai, E. R. Stanley, G. J. Randolph, and M. Merad. 2006. Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7: 265-273.
20. Yui, M. A., W. H. Brissette, D. C. Brennan, R. P. Wuthrich, and V. E. Rubin-Kelley. 1991. Increased macrophage colony-stimulating factor in neonatal and adult autoimmune MRL-lpr mice. Am. J. Pathol. 139: 255-261.
21. Bloom, R. D., S. Florquin, G. G. Singer, D. C. Brennan, and V. R. Kelley. 1993. Colony stimulating factor-1 in the induction of lupus nephritis. Kidney Int. 43: 1000-1009.
22. Lenda, D. M., E. R. Stanley, and V. R. Kelley. 2004. Negative role of colony-stimulating factor-1 in macrophage, T cell, and B cell mediated autoimmune disease in MRL-Faslpr mice. J. Immunol. 173: 4744-4754.
23. Lenda, D. M., E. Kikawada, E. R. Stanley, and V. R. Kelley. 2003. Reduced macrophage recruitment, proliferation, and activation in colony-stimulating factor- 1-deficient mice results in decreased tubular apoptosis during renal inflammation. J. Immunol. 170: 3254-3262.
24. Sasmono, R. T., D. Oceandy, J. W. Pollard, W. Tong, P. Pavli, B. J. Wainwright, M. C. Ostrowski, S. R. Himes, and D. A. Hume. 2003. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101: 1155-1163.
25. Ryan, G. R., X. M. Dai, M. G. Dominguez, W. Tong, F. Chuan, O. Chisholm, R. G. Russell, J. W. Pollard, and E. R. Stanley. 2001. Rescue of the colony-stimulating factor 1 (CSF-1)-nullizygous mouse (Csf1op/Csf1op phenotype with a CSF-1 transgene and identification of sites of local CSF-1 synthesis. Blood 98: 74-84.
26. Faust, J., J. Menke, J. Kriegsmann, V. R. Kelley, W. J. Mayet, P. R. Galle, and A. Schwarting. 2002. Correlation of renal tubular epithelial cell-derived interleukin- 18 up- regulation with disease activity in MRL-Faslpr mice with autoimmune lupus nephritis. Arthritis Rheum. 46: 3083-3095. (Pubitemid 35315904)
27. Menke, J., J. A. Lucas, G. C. Zeller, M. E. Keir, X. R. Huang, N. Tsuboi, T. N. Mayadas, H. Y. Lan, A. H. Sharpe, and V. R. Kelley. 2007. Programmed death 1 ligand (PD-L) 1 and PD-L2 limit autoimmune kidney disease: distinct roles. J. Immunol. 179: 7466-7477.
28. Moore, K. J., K. Yeh, T. Naito, and V. R. Kelley. 1996. TNF-α enhances colony-stimulating factor-1-induced macrophage accumulation in autoimmune renal disease. J. Immunol. 157: 427-432.
29. Mee, J. B., C. Antonopoulos, S. Poole, T. S. Kupper, and R. W. Groves. 2005. Counter-regulation of interleukin-1α (IL-1α) and IL-1 receptor antagonist in murine keratinocytes. J. Invest. Dermatol. 124: 1267-1274.
30. Dlugosz, A. A., A. B. Glick, T. Tennenbaum, W. C. Weinberg, and S. H. Yuspa. 1995. Isolation and utilization of epidermal keratinocytes for oncogene research. Methods Enzymol. 254: 3-20.
31. Rogers, K. M., D. H. Black, and R. Eberle. 2007. Primary mouse dermal fibroblast cell cultures as an in vitro model system for the differential pathogenicity of cross-species Herpesvirus papio 2 infections. Arch. Virol. 152: 543-552.
32. Wuthrich, R. P., L. H. Glimcher, M. A. Yui, A. M. Jevnikar, S. E. Dumas, and V. E. Kelley. 1990. MHC class II, antigen presentation and tumor necrosis factor in renal tubular epithelial cells. Kidney Int. 37: 783-792.
33. Danos, O., and R. C. Mulligan. 1988. Safe and efficient generation of recombinant retroviruses with amphotropic and ecotropic host ranges. Proc. Natl. Acad. Sci. USA 85: 6460-6464. (Pubitemid 18219183)
34. Keir, M. E., S. C. Liang, I. Guleria, Y. E. Latchman, A. Qipo, L. A. Albacker, M. Koulmanda, G. J. Freeman, M. H. Sayegh, and A. H. Sharpe. 2006. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203: 883-895.
35. Merad, M., M. G. Manz, H. Karsunky, A. Wagers, W. Peters, I. Charo, I. L. Weissman, J. G. Cyster, and E. G. Engleman. 2002. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3: 1135-1141. (Pubitemid 35469697)
36. Vermes, I., C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger. 1995. A novel assay for apoptosis: flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J. Immunol. Methods 184: 39-51.
37. Blaszczyk, M., S. Jablonska, T. P. Chorzelski, M. Jarzabek-Chorzelska, E. H. Beutner, and V. Kumar. 1992. Clinical relevance of immunologic findings in cutaneous lupus erythematosus. Clin. Dermatol. 10: 399-406. (Pubitemid 23129999)
38. Theofilopoulos, A. N., and F. J. Dixon. 1985. Murine models of systemic lupus erythematosus. Adv. Immunol. 37: 269-390. (Pubitemid 15093080)
39. Schuhmachers, G., K. Ariizumi, T. Kitajima, D. Edelbaum, S. Xu, R. K. Shadduck, G. L. Gilmore, R. S. Taylor, P. R. Bergstresser, and A. Takashima. 1996. UVB radiation interrupts cytokine-mediated support of an epidermal-derived dendritic cell line (XS52) by a dual mechanism. J. Invest. Dermatol. 106: 1023-1029. (Pubitemid 26155096)
40. Chodakewitz, J. A., J. Lacy, S. E. Edwards, N. Birchall, and D. L. Coleman. 1990. Macrophage colony-stimulating factor production by murine and human keratinocytes: enhancement by bacterial lipopolysaccharide. J. Immunol. 144: 2190-2196.
41. Furukawa, F., H. Tanaka, K. Sekita, T. Nakamura, Y. Horiguchi, and Y. Hamashima. 1984. Dermatopathological studies on skin lesions of MRL mice. Arch. Dermatol. Res. 276: 186-194. (Pubitemid 14107771)
42. Hasan, T., F. Nyberg, E. Stephansson, P. Puska, M. Hakkinen, S. Sarna, A. M. Ros, and A. Ranki. 1997. Photosensitivity in lupus erythematosus, UV photoprovocation results compared with history of photosensitivity and clinical findings. Br. J. Dermatol. 136: 699-705. (Pubitemid 27278077)
43. Moore, K. J., T. Naito, C. Martin, and V. R. Kelley. 1996. Enhanced response of macrophages to CSF-1 in autoimmune mice: a gene transfer strategy. J. Immunol. 157: 433-440.
44. Koh, D. R., A. Ho, A. Rahemtulla, W. P. Fung-Leung, H. Griesser, and T. W. Mak. 1995. Murine lupus in MRL/lpr mice lacking CD4 or CD8 T cells. Eur. J. Immunol. 25: 2558-2562.
45. Yang, J.-Q., V. Saxena, H. Xu, L. Van Kaer, C.-R. Wang, and R. R. Singh. 2003. Repeated α-galactosylceramide administration results in expansion of NK T cells and alleviates inflammatory dermatitis in MRL-lpr/lpr mice. J. Immunol. 171: 4439-4446.
46. Yang, J.-Q., T. Chun, H. Liu, S. Hong, H. Bui, L. Van Kaer, C.-R. Wang, and R. R. Singh. 2004. CD1d deficiency exacerbates inflammatory dermatitis in MRL-lpr/lpr mice. Eur. J. Immunol. 34: 1723-1732.
47. 2-microglobulin, but not CD1, accelerates spontaneous lupus skin disease while inhibiting nephritis in MRL-faslpr mice: an example of disease regulation at the organ level. J. Immunol. 167: 2985-2990.
48. Scordi, I. A., and V. Vincek. 2000. Timecourse study of UVB-induced cytokine induction in whole mouse skin. Photodermatol. Photoimmunol. Photomed. 16: 67-73.
49. Van Laethem, A., S. Claerhout, M. Garmyn, and P. Agostinis. 2005. The sunburn cell: regulation of death and survival of the keratinocyte. Int. J. Biochem. Cell Biol. 37: 1547-1553. (Pubitemid 40719633)
50. Bijl, M., E. Reefman, P. C. Limburg, and C. G. Kallenberg. 2007. Inflammatory clearance of apoptotic cells after UVB challenge. Autoimmunity 40: 244-248. (Pubitemid 46845515)
51. Reefman, E., M. C. de Jong, H. Kuiper, M. F. Jonkman, P. C. Limburg, C. G. Kallenberg, and M. Bijl. 2006. Is disturbed clearance of apoptotic keratinocytes responsible for UVB-induced inflammatory skin lesions in systemic lupus erythematosus? Arthritis Res. Ther. 8: R156.
52. Takahashi, H., A. Ishida-Yamamoto, and H. Iizuka. 2001. Ultraviolet B irradiation induces apoptosis of keratinocytes by direct activation of Fas antigen. J. Invest. Dermatol. Symp. Proc. 6: 64-68. (Pubitemid 33758607)
53. Zhuang, L., B. Wang, and D. N. Sauder. 2000. Molecular mechanism of ultraviolet- induced keratinocyte apoptosis. J. Interferon Cytokine Res. 20: 445-454. (Pubitemid 30414226)
54. Zhuang, L., B. Wang, G. A. Shinder, G. M. Shivji, T. W. Mak, and D. N. Sauder. 1999. TNF receptor p55 plays a pivotal role in murine keratinocyte apoptosis induced by ultraviolet B irradiation. J. Immunol. 162: 1440-1447. (Pubitemid 29307016)
55. Gaipl, U. S., A. Kuhn, A. Sheriff, L. E. Munoz, S. Franz, R. E. Voll, J. R. Kalden, and M. Herrmann. 2006. Clearance of apoptotic cells in human SLE. Curr. Dir. Autoimmun. 9: 173-187.
56. Licht, R., J. W. Dieker, C. W. Jacobs, W. J. Tax, and J. H. Berden. 2004. Decreased phagocytosis of apoptotic cells in diseased SLE mice. J. Autoimmun. 22: 139-145. (Pubitemid 38252970)
57. Potter, P. K., J. Cortes-Hernandez, P. Quartier, M. Botto, and M. J. Walport. 2003. Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J. Immunol. 170: 3223-3232.
58. Gaipl, U. S., L. E. Munoz, G. Grossmayer, K. Lauber, S. Franz, K. Sarter, R. E. Voll, T. Winkler, A. Kuhn, J. Kalden, et al. 2007. Clearance deficiency and systemic lupus erythematosus (SLE). J. Autoimmun. 28: 114-121. (Pubitemid 46680499)