Enhanced expression of the soluble form of e-selectin attenuates progression of lupus nephritis and vasculitis in mrl/lpr mice

Immunity, Inflammation and Disease

Volumn 1, Issue 1, 2013, Pages 37-46

  Nakatani, Kimihiko ^a   Yoshimoto, Shuhei ^a   Asai, Osamu ^a   Sakan, Hirokazu ^a   Terada, Miho ^b   Saito, Yoshihiko ^a   Nose, Masato ^b   Iwano, Masayuki ^a,c   Konishi, Noboru ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

^b EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF FUKUI   (Japan)

Author keywords

Lupus; MRL lpr mice; Nephritis; Soluble E selectin; Vasculitis

Indexed keywords

EID: 84906316684     PISSN: None     EISSN: 20504527     Source Type: Journal    
DOI: 10.1002/iid3.6     Document Type: Article

References (55)

1. Rahman, A., and D. A. Isenberg. 2008. Systemic lupus erythematosus. N. Engl. J. Med. 358:929–939.
2. Cameron, J. S. 1999. Lupus nephritis: an historical perspective 1968–1998. J. Nephrol. 12(Suppl. 2):S29–S41.
3. Anders, H. J., V. Vielhauer, and D. Schlondorff. 2003. Chemokines and chemokine receptors are involved in the resolution or progression of renal disease. Kidney Int. 63:401– 415.
4. Kelley, V. R. and B. H. Rovin. 2003. Chemokines: therapeutic targets for autoimmune and inflammatory renal disease. Springer Semin. Immunopathol. 24:411–421.
5. Springer, T. A. 1995. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu. Rev. Physiol. 57:827–872.
6. Lasky, L. A. 1995. Selectin-carbohydrate interactions and the initiation of the inflammatory response. Annu. Rev. Biochem. 64:113–139.
7. Kansas, G. S. 1996. Selectins and their ligands: current concepts and controversies. Blood 88:3259–3287.
8. Vestweber, D. and J. E. Blanks. 1999. Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev. 79:181–213.
9. Nakatani, K., H. Fujii, H. Hasegawa, M. Terada, N. Arita, M. R. Ito, M. Ono, S. Takahashi, K. Saiga, S. Yoshimoto, et al. 2004. Endothelial adhesion molecules in glomerular lesions: association with their severity and diversity in lupus models. Kidney Int. 65:1290–1300.
10. Winchester, R., M. Wiesendanger, H. Z. Zhang, V. Steshenko, K. Peterson, L. Geraldino-Pardilla, E. Ruiz-Vazquez, and V. D’Agati. 2012. Immunologic characteristics of intrarenal T cells: trafficking of expanded CD8+ T cell beta-chain clonotypes in progressive lupus nephritis. Arthritis. Rheum. 64:1589–1600.
11. Dolff, S., W. H. Abdulahad, S. Arends, M. C. van Dijk, P. C. Limburg, C. G. Kallenberg, and M. Bijl. 2013. Urinary CD8+ T-cell counts discriminate between active and inactive lupus nephritis. Arthritis. Res. Ther. 15:R36. DOI: 10.1186/ar4189
12. Couzi, L., P. Merville, C. Deminiere, J. F. Moreau, C. Combe, J. L. Pellegrin, J. F. Viallard, and P. Blanco. 2007. Predominance of CD8+ T lymphocytes among periglomer-ular infiltrating cells and link to the prognosis of class III and class IV lupus nephritis. Arthritis. Rheum. 56:2362–2370.
13. Hirata, T., B. C. Furie, and B. Furie. 2002. P-, E-, and L-selectin mediate migration of activated CD8+ T lymphocytes into inflamed skin. J. Immunol. 169:4307–4313.
14. Biancone, L., M. Araki, K. Araki, P. Vassalli, and I. Stamenkovic. 1996. Redirection of tumor metastasis by expression of E-selectin in vivo. J. Exp. Med. 183:581–587.
15. Shimizu, S., N. Sugiyama, K. Masutani, A. Sadanaga, Y. Miyazaki, Y. Inoue, M. Akahoshi, R. Katafuchi, H. Hirakata, M. Harada, et al. 2005. Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1). J. Immunol. 175:7185–7192.
16. Miyazaki, T., M. Ono, W. M. Qu, M. C. Zhang, S. Mori, S. Nakatsuru, Y. Nakamura, T. Sawasaki, Y. Endo, and M. Nose, 2005. Implication of allelic polymorphism of osteopontin in the development of lupus nephritis in MRL/lpr mice. Eur. J. Immunol. 35:1510–1520.
17. Qu, W. M., T. Miyazaki, M. Terada, L. M. Lu, M. Nishihara, A. Yamada, S. Mori, Y. Nakamura, H. Ogasawara, C. Yazawa, et al. 2000. Genetic dissection of vasculitis in MRL/lpr lupus mice: a novel susceptibility locus involving the CD72c allele. Eur. J. Immunol. 30:2027–2037.
18. Yoshimoto, S., K. Nakatani, M. Iwano, O. Asai, K. Samejima, H. Sakan, M. Terada, K. Harada, Y. Akai, H. Shiiki, et al. 2007. Elevated levels of fractalkine expression and accumulation of CD16+ monocytes in glomeruli of active lupus nephritis. Am. J. Kidney Dis. 50:47–58.
19. Azuma, A., S. Takahashi, M. Nose, K. Araki, M. Araki, T. Takahashi, M. Hirose, H. Kawashima, M. Miyasaka, and S. Kudoh, 2000. Role of E-selectin in bleomycin induced lung fibrosis in mice. Thorax. 55:147–152.
20. Chen, X., Q. Xu, and L. Tang. 1995. Expression of intercellular adhesion molecule-1 and vascular adhesion molecule-1 in kidney of patients with lupus nephritis and membranopro-liferative glomerulonephritis. Zhonghua Bing Li Xue Za Zhi 24:149–151.
21. Zheng, L., R. Sinniah, and S. I. Hsu. 2006. In situ glomerular expression of activated NF-kappaB in human lupus nephritis and other non-proliferative proteinuric glomerulopathy. Virchows. Arch. 448:172–183.
22. Yokoyama, H., M. Takaeda, T. Wada, S. Ohta, Y. Hisada, C. Segawa, K. Furuichi, and K. Kobayashi. 1997. Glomerular ICAM-1 expression related to circulating TNF-alpha in human glomerulonephritis. Nephron. 76:425–433.
23. Lhotta, K., H. P. Neumayer, M. Joannidis, D. Geissler, and P. Konig. 1991. Renal expression of intercellular adhesion molecule-1 in different forms of glomerulonephritis. Clin. Sci. (Lond) 81:477–481.
24. Wuthrich, R. P. 1992. Vascular cell adhesion molecule-1 (VCAM-1) expression in murine lupus nephritis. Kidney Int. 42:903–914.
25. Seron, D., J. S. Cameron, and D. O. Haskard. 1991. Expression of VCAM-1 in the normal and diseased kidney. Nephrol. Dial. Transplant. 6:917–922.
26. Singh, S., T. Wu, C. Xie, K. Vanarsa, J. Han, T. Mahajan, H. B. Oei, C. Ahn, X. J. Zhou, C. Putterman, et al. 2012. Urine VCAM-1 as a marker of renal pathology activity index in lupus nephritis. Arthritis. Res. Ther. 14:R164. DOI: 10.1186/ar3912
27. Spronk, P. E., H. Bootsma, M. G. Huitema, P. C. Limburg, and C. G. Kallenberg. 1994. Levels of soluble VCAM-1, soluble ICAM-1, and soluble E-selectin during disease exacerbations in patients with systemic lupus erythematosus (SLE); a long term prospective study. Clin. Exp. Immunol. 97:439–444.
28. Molad, Y., E. Miroshnik, J. Sulkes, S. Pitlik, A. Weinberger, and Y. Monselise. 2002. Urinary soluble VCAM-1 in systemic lupus erythematosus: a clinical marker for monitoring disease activity and damage. Clin. Exp. Rheumatol. 20:403–406.
29. Tesar, V., Z. Masek, I. Rychlik, M. Merta, J. Bartunkova, A. Stejskalova, J. Zabka, I. Janatkova, T. Fucikova, C. Dostal, et al. 1998. Cytokines and adhesion molecules in renal vasculitis and lupus nephritis. Nephrol. Dial. Transplant. 13:1662–1667.
30. Ikeda, Y., T. Fujimoto, M. Ameno, H. Shiiki, and K. Dohi. 1998. Relationship between lupus nephritis activity and the serum level of soluble VCAM-1. Lupus. 7:347–354.
31. Bevilacqua, M. P., J. S. Pober, D. L. Mendrick, R. S. Cotran, and M. A. Gimbrone Jr. 1987. Identification of an inducible endothelial-leukocyte adhesion molecule. Proc. Narl. Acad. Sci. 84:9238–9242.
32. Bevilacqua, M. P., S. Stengelin, M. A. Gimbrone, Jr. and B. Seed. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 1989. 243:1160–1165.
33. Gearing, A. J. and W. Newman. 1993. Circulating adhesion molecules in disease. Immunol. Today 14:506–512.
34. Subramaniam, M., J. A. Koedam, and D. D. Wagner. 1993. Divergent fates of P-and E-selectins after their expression on the plasma membrane. Mol. Biol. Cell 4:791–801.
35. Mebius, R. E. and S. R. Watson. 1993. L-and E-selectin can recognize the same naturally occurring ligands on high endothelial venules. J. Immunol. 151:3252–3260.
36. McEver, R. P. 2005. A sulfated address for lymphocyte homing. Nat. Immunol. 6:1067–1069.
37. Foster, M. H. and V. R. Kelley. 1999. Lupus nephritis: update on pathogenesis and disease mechanisms. Semin. Nephrol. 19:173–181.
38. Weyand, C. M. and J. J. Goronzy. 2003. Medium-and large-vessel vasculitis. N. Engl. J. Med. 349:160–169.
39. Tipping, P. G. and S. R. Holdsworth. 2006. T cells in crescentic glomerulonephritis. J. Am. Soc. Nephrol. 17:1253–1263.
40. Wang, Y. M., G. Y. Zhang, M. Hu, T. Polhill, A. Sawyer, J. J. Zhou, M. Saito, D. Watson, H. Wu, Y. Wang, et al. 2012. CD8+ regulatory T cells induced by T cell vaccination protect against autoimmune nephritis. J. Am. Soc. Nephrol. 23:1058–1067.
41. Hopfer, H., J. Holzer, S. Hunemorder, H. J. Paust, M. Sachs, C. Meyer-Schwesinger, J. E. Turner, U. Panzer, and H. W. Mittrucker, 2012. Characterization of the renal CD4+ T-cell response in experimental autoimmune glomerulonephritis. Kidney Int. 82:60–71.
42. Winchester, R., M. Wiesendanger, H. Z. Zhang, V. Steshenko, K Peterson, L. Geraldino-Pardilla, E. Ruiz-Vazquez, and V. D’Agati. 2012. Immunologic characteristics of intrarenal T cells: trafficking of expanded CD8+ T cell β-chain clonotypes in progressive lupus nephritis. Arthritis. Rheum. 64:1589–1600.
43. Wang, Y., S. Ito, Y. Chino, K. Iwanami, T. Yasukochi, D. Goto, I. Matsumoto, T. Hayashi, K. Uchida, and T. Sumida, 2008. Use of laser microdissection in the analysis of renal-infiltrating T cells in MRL/lpr mice. Mod. Rheumatol. 18:385–393.
44. Couzi, L., P. Merville, C. DeminiÒre, J. F. Moreau, C. Combe, J. L. Pellegrin, J. F. Viallard, and P. Blanco. 2007. Predominance of CD8+ T lymphocytes among periglomer-ular infiltrating cells and link to the prognosis of class III and class IV lupus nephritis. Arthritis. Rheum. 56:2362–2370.
45. Masutani, K., M. Akahoshi, K. Tsuruya, M. Tokumoto, T. Ninomiya, T. Kohsaka, K. Fukuda, H. Kanai, H. Nakashima, T. Otsuka, et al. 2001. Predominance of Th1 immune response in diffuse proliferative lupus nephritis. Arthritis. Rheum. 44:2097–2106.
46. Austrup, F., D. Vestweber, E. Borges, M. Lohning, R. Brauer, U. Herz, H. Renz, R. Hallmann, A. Scheffold, A. Radbruch, et al. 1997. P-and E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflammed tissues. Nature 385:81–83.
47. Borges, E., W. Tietz, M. Steegmaier, T. Moll, R. Hallmann, A. Hamann, and D. Vestweber. 1997. P-selectin glycoprotein ligand-1 (PSGL-1) on T helper 1 but not on T helper 2 cells binds to P-selectin and supports migration into inflamed skin. J. Exp. Med. 185:573–578.
48. Lim, Y. C., L. Henault, A. J. Wagers, G. S. Kansas, F. W. Luscinskas, and A. H. Lichtman. 1999. Expression of functional selectin ligands on Th cells is differentially regulated by IL-12 and IL-4. J. Immunol. 162:3193–3201.
49. Takahashi, S., M. Nose, J. Sasaki, T. Yamamoto, and M. Kyogoku. 1991. IgG3 production in MRL/lpr mice is responsible for development of lupus nephritis. J. Immunol. 147:515–519.
50. Arbones, M. L., D. C. Ord, K. Ley, H. Ratech, C. Maynard-Curry, G. Otten, D. J. Capon, and T. F. Tedder 1994. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity. 1:247–260.
51. Baldwin, D. S. 1982. Clinical usefulness of the morphological classification of lupus nephritis. Am. J. Kidney Dis. 2:142– 149.
52. Nossent, H. C., S. C. Henzen-Logmans, T. M. Vroom, J. H. Berden, and T. J. Swaak. 1990. Contribution of renal biopsy data in predicting outcome in lupus nephritis. Analysis of 116 patients. Arthritis. Rheum. 33:970–977.
53. Whiting-O’Keefe, Q., J. E. Henke, M. A. Shearn, J. Hopper, Jr. C. G. Biava, and W. V. Epstein. 1982. The information content from renal biopsy in systemic lupus erythematosus. Ann. Intern. Med. 96:718–723.
54. Schwartz, M. M. 1985. The role of renal biopsy in the management of lupus nephritis. Semin. Nephrol. 5:255–263.
55. Lewis, E. J., K. Kawala, and M. M. Schwartz. 1987. Histologic features that correlate with the prognosis of patients with lupus nephritis. Am. J. Kidney Dis. 10:192–197.