NKG2D ligand overexpression in lupus nephritis correlates with increased NK cell activity and differentiation in kidneys but not in the periphery

Journal of Leukocyte Biology

Volumn 97, Issue 3, 2015, Pages 583-598

  Spada, Roberto ^a   Rojas, José M ^a   Pérez Yagüe, Sonia ^a   Mulens, Vladimir ^a   Cannata Ortiz, Pablo ^b   Bragado, Rafael ^b   Barber, Domingo F ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b HOSPITAL UNIVERSITARIO FUNDACIÓN JIMÉNEZ DÍAZ   (Spain)

Author keywords

Eomes; MICA; MRL lpr; MRL MpJ; Rae; T bet

Indexed keywords

ALPHA2 INTEGRIN; CD11B ANTIGEN; CD2 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR; INTERLEUKIN 2 RECEPTOR BETA; LEUKOSIALIN; LYMPHOCYTE RECEPTOR; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR NKG2D; NATURAL KILLER CELL RECEPTOR NKG2D LIGAND; STAT5 PROTEIN; SYNAPTOPODIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CARRIER PROTEIN; EOMES PROTEIN, MOUSE; HLA ANTIGEN CLASS 1; LIGAND; LY ANTIGEN; MHC CLASS I-RELATED CHAIN A; NCR1 PROTEIN, MOUSE; NUCLEAR MATRIX PROTEIN; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN; RAE1 PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21; UL16 BINDING PROTEIN 1, MOUSE;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE; GENE OVEREXPRESSION; GLOMERULUS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOGENESIS; IMMUNOREACTIVITY; KIDNEY; LUPUS ERYTHEMATOSUS NEPHRITIS; MICA GENE; MIDDLE AGED; MOUSE; MULT 1 GENE; NATURAL KILLER CELL; NONHUMAN; POPULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAE 1 GAMMA GENE; SYSTEMIC LUPUS ERYTHEMATOSUS; ULBP1 GENE; YOUNG ADULT; ANIMAL; BIOSYNTHESIS; IMMUNOLOGY; MALE; METABOLISM; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; PATHOLOGY; PHENOTYPE; PHOSPHORYLATION; SPLEEN;

MURINAE; MUS;

ADULT; AGED; ANIMALS; ANTIGENS, LY; BIOLOGICAL MARKERS; CARRIER PROTEINS; CELL DIFFERENTIATION; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERFERON-GAMMA; KIDNEY; KIDNEY GLOMERULUS; KILLER CELLS, NATURAL; LIGANDS; LUPUS NEPHRITIS; MALE; MICE, INBRED MRL LPR; MIDDLE AGED; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PHENOTYPE; PHOSPHORYLATION; SPLEEN; STAT5 TRANSCRIPTION FACTOR; T-BOX DOMAIN PROTEINS; YOUNG ADULT;

EID: 84928760905     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.4A0714-326R     Document Type: Article

References (70)

1. Flodström-Tullberg, M., Bryceson, Y. T., Shi, F. D., Höglund, P., Ljunggren, H. G. (2009) Natural killer cells in human autoimmunity. Curr. Opin. Immunol. 21, 634–640.
2. Gillgrass, A., Ashkar, A. (2011) Stimulating natural killer cells to protect against cancer: recent developments. Expert Rev. Clin. Immunol. 7, 367–382.
3. Lanier, L. L. (2005) NK cell recognition. Annu. Rev. Immunol. 23, 225–274.
4. Pisetsky, D. S., Rönnblom, L. (2009) Systemic lupus erythematosus: a matter of life and death. Arthritis Rheum. 60, 1567–1570.
5. Mills, J. A. (1994) Systemic lupus erythematosus. N. Engl. J. Med. 330, 1871–1879.
6. Sekine, H., Watanabe, H., Gilkeson, G. S. (2004) Enrichment of antiglomerular antigen antibody-producing cells in the kidneys of MRL/MpJFas(lpr) mice. J. Immunol. 172, 3913–3921.
7. Balow, J. E. (1991) Kidney disease in systemic lupus erythematosus. Rheumatol. Int. 11, 113–115.
8. Park, M. H., D’Agati, V., Appel, G. B., Pirani, C. L. (1986) Tubulointerstitial disease in lupus nephritis: relationship to immune deposits, interstitial inflammation, glomerular changes, renal function, and prognosis. Nephron 44, 309–319.
9. Park, Y. W., Kee, S. J., Cho, Y. N., Lee, E. H., Lee, H. Y., Kim, E. M., Shin, M. H., Park, J. J., Kim, T. J., Lee, S. S., Yoo, D. H., Kang, H. S. (2009) Impaired differentiation and cytotoxicity of natural killer cells in systemic lupus erythematosus. Arthritis Rheum. 60, 1753–1763.
10. Huang, Z., Fu, B., Zheng, S. G., Li, X., Sun, R., Tian, Z., Wei, H. (2011) Involvement of CD226+ NK cells in immunopathogenesis of systemic lupus erythematosus. J. Immunol. 186, 3421–3431.
11. Erkeller-Yuksel, F. M., Lydyard, P. M., Isenberg, D. A. (1997) Lack of NK cells in lupus patients with renal involvement. Lupus 6, 708–712.
12. Pan, L. Z., Dauphinée, M. J., Ansar Ahmed, S., Talal, N. (1986) Altered natural killer and natural cytotoxic cellular activities in lpr mice. Scand. J. Immunol. 23, 415–423.
13. Hervier, B., Beziat, V., Haroche, J., Mathian, A., Lebon, P., Ghillani- Dalbin, P., Musset, L., Debré, P., Amoura, Z., Vieillard, V. (2011) Phenotype and function of natural killer cells in systemic lupus erythematosus: excess interferon-g production in patients with active disease. Arthritis Rheum. 63, 1698–1706.
14. Bottino, C., Castriconi, R., Moretta, L., Moretta, A. (2005) Cellular ligands of activating NK receptors. Trends Immunol. 26, 221–226.
15. Lanier, L. L. (2008) Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9, 495–502.
16. Eagle, R. A., Trowsdale, J. (2007) Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 7, 737–744.
17. Dai, Z., Turtle, C. J., Booth, G. C., Riddell, S. R., Gooley, T. A., Stevens, A. M., Spies, T., Groh, V. (2009) Normally occurring NKG2D+CD4+ T cells are immunosuppressive and inversely correlated with disease activity in juvenile-onset lupus. J. Exp. Med. 206, 793–805.
18. Yang, D., Wang, H., Ni, B., He, Y., Li, J., Tang, Y., Fu, X., Wang, Q., Xu, G., Li, K., Yang, Z., Wu, Y. (2009) Mutual activation of CD4+ T cells and monocytes mediated by NKG2D-MIC interaction requires IFN-gamma production in systemic lupus erythematosus. Mol. Immunol. 46, 1432–1442.
19. Krmpotic, A., Hasan, M., Loewendorf, A., Saulig, T., Halenius, A., Lenac, T., Polic, B., Bubic, I., Kriegeskorte, A., Pernjak-Pugel, E., Messerle, M., Hengel, H., Busch, D. H., Koszinowski, U. H., Jonjic, S. (2005) NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145. J. Exp. Med. 201, 211–220.
20. Matkowskyj, K. A., Schonfeld, D., Benya, R. V. (2000) Quantitative immunohistochemistry by measuring cumulative signal strength using commercially available software Photoshop and Matlab. J. Histochem. Cytochem. 48, 303–312.
21. Xu, W. D., Zhang, Y. J., Li, R., Pan, H. F., Ye, D. Q. (2012) New evidence for a role of MICA in the pathogenesis of systemic lupus erythematosus: comment on the article by Yoshida et al. Arthritis Rheum. 64, 1294–1295.
22. Yoshida, K., Komai, K., Shiozawa, K., Mashida, A., Horiuchi, T., Tanaka, Y., Nose, M., Hashiramoto, A., Shiozawa, S. (2011) Role of the MICA polymorphism in systemic lupus erythematosus. Arthritis Rheum. 63, 3058–3066.
23. Ueda, H., Miyazaki, Y., Matsusaka, T., Utsunomiya, Y., Kawamura, T., Hosoya, T., Ichikawa, I. (2008) Bmp in podocytes is essential for normal glomerular capillary formation. J. Am. Soc. Nephrol. 19, 685–694.
24. Barutta, F., Corbelli, A., Mastrocola, R., Gambino, R., Di Marzo, V., Pinach, S., Rastaldi, M. P., Perin, P. C., Gruden, G. (2010) Cannabinoid receptor 1 blockade ameliorates albuminuria in experimental diabetic nephropathy. Diabetes 59, 1046–1054.
25. Vosshenrich, C. A., Samson-Villéger, S. I., Di Santo, J. P. (2005) Distinguishing features of developing natural killer cells. Curr. Opin. Immunol. 17, 151–158.
26. Di Santo, J. P. (2006) Natural killer cell developmental pathways: a question of balance. Annu. Rev. Immunol. 24, 257–286.
27. Huntington, N. D., Vosshenrich, C. A., Di Santo, J. P. (2007) Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat. Rev. Immunol. 7, 703–714.
28. Chiossone, L., Chaix, J., Fuseri, N., Roth, C., Vivier, E., Walzer, T. (2009) Maturation of mouse NK cells is a 4-stage developmental program. Blood 113, 5488–5496.
29. Narni-Mancinelli, E., Chaix, J., Fenis, A., Kerdiles, Y. M., Yessaad, N., Reynders, A., Gregoire, C., Luche, H., Ugolini, S., Tomasello, E., Walzer, T., Vivier, E. (2011) Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 108, 18324–18329.
30. Gordon, S. M., Chaix, J., Rupp, L. J., Wu, J., Madera, S., Sun, J. C., Lindsten, T., Reiner, S. L. (2012) The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36, 55–67.
31. Daussy, C., Faure, F., Mayol, K., Viel, S., Gasteiger, G., Charrier, E., Bienvenu, J., Henry, T., Debien, E., Hasan, U. A., Marvel, J., Yoh, K., Takahashi, S., Prinz, I., de Bernard, S., Buffat, L., Walzer, T. (2014) T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J. Exp. Med. 211, 563–577.
32. Bernardini, G., Benigni, G., Antonangeli, F., Ponzetta, A., Santoni, A. (2014) Multiple levels of chemokine receptor regulation in the control of mouse natural killer cell development. Front. Immunol. 5, 44.
33. Huang, X., Guo, Y., Bao, C., Shen, N. (2011) Multidimensional single cell based STAT phosphorylation profiling identifies a novel biosignature for evaluation of systemic lupus erythematosus activity. PLoS ONE 6, e21671.
34. Lieberman, L. A., Tsokos, G. C. (2010) The IL-2 defect in systemic lupus erythematosus disease has an expansive effect on host immunity. J. Biomed. Biotechnol. 2010, 740619.
35. Holmén, C., Elsheikh, E., Stenvinkel, P., Qureshi, A. R., Pettersson, E., Jalkanen, S., Sumitran-Holgersson, S. (2005) Circulating inflammatory endothelial cells contribute to endothelial progenitor cell dysfunction in patients with vasculitis and kidney involvement. J. Am. Soc. Nephrol. 16, 3110–3120.
36. Schrambach, S., Ardizzone, M., Leymarie, V., Sibilia, J., Bahram, S. (2007) In vivo expression pattern of MICA and MICB and its relevance to auto-immunity and cancer. PLoS ONE 2, e518.
37. Groh, V., Wu, J., Yee, C., Spies, T. (2002) Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419, 734–738.
38. Diefenbach, A., Jensen, E. R., Jamieson, A. M., Raulet, D. H. (2001) Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413, 165–171.
39. Markiewicz, M. A., Wise, E. L., Buchwald, Z. S., Pinto, A. K., Zafirova, B., Polic, B., Shaw, A. S. (2012) RAE1e ligand expressed on pancreatic islets recruits NKG2D receptor-expressing cytotoxic T cells independent of T cell receptor recognition. Immunity 36, 132–141.
40. Jabs, D. A., Prendergast, R. A. (1988) Murine models of Sjögren’s syndrome. Immunohistologic analysis of different strains. Invest. Ophthalmol. Vis. Sci. 29, 1437–1443.
41. Teachey, D. T., Seif, A. E., Grupp, S. A. (2010) Advances in the management and understanding of autoimmune lymphoproliferative syndrome (ALPS). Br. J. Haematol. 148, 205–216.
42. Vidal, S., Kono, D. H., Theofilopoulos, A. N. (1998) Loci predisposing to autoimmunity in MRL-Fas lpr and C57BL/6-Faslpr mice. J. Clin. Invest. 101, 696–702.
43. Lucas, M., Schachterle, W., Oberle, K., Aichele, P., Diefenbach, A. (2007) Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26, 503–517.
44. Roth, C., Rothlin, C., Riou, S., Raulet, D. H., Lemke, G. (2007) Stromalcell regulation of natural killer cell differentiation. J. Mol. Med. (Berl) 85, 1047–1056.
45. Magilavy, D. B., Steinberg, A. D., Latta, S. L. (1987) High hepatic natural killer cell activity in murine lupus. J. Exp. Med. 166, 271–276.
46. Nilsson, N., Carlsten, H. (1996) Enhanced natural but diminished antibody-mediated cytotoxicity in the lungs of MRLlpr/lpr mice. Clin. Exp. Immunol. 105, 480–485.
47. Tayade, C., Fang, Y., Black, G. P., Paffaro, V. A., Jr., Erlebacher, A., Croy, B. A. (2005) Differential transcription of Eomes and T-bet during maturation of mouse uterine natural killer cells. J. Leukoc. Biol. 78, 1347–1355.
48. Zhu, J., Jankovic, D., Oler, A. J., Wei, G., Sharma, S., Hu, G., Guo, L., Yagi, R., Yamane, H., Punkosdy, G., Feigenbaum, L., Zhao, K., Paul, W. E. (2012) The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses. Immunity 37, 660–673.
49. Martin, M. P., Nelson, G., Lee, J. H., Pellett, F., Gao, X., Wade, J., Wilson, M. J., Trowsdale, J., Gladman, D., Carrington, M. (2002) Cutting edge: susceptibility to psoriatic arthritis: influence of activating killer Ig-like receptor genes in the absence of specific HLA-C alleles. J. Immunol. 169, 2818–2822.
50. Van der Slik, A. R., Koeleman, B. P., Verduijn, W., Bruining, G. J., Roep, B. O., Giphart, M. J. (2003) KIR in type 1 diabetes: disparate distribution of activating and inhibitory natural killer cell receptors in patients versus HLA-matched control subjects. Diabetes 52, 2639–2642.
51. French, A. R., Yokoyama, W. M. (2004) Natural killer cells and autoimmunity. Arthritis Res. Ther. 6, 8–14.
52. Bilbao, J. R., Martín-Pagola, A., Pérez De Nanclares, G., Calvo, B., Vitoria, J. C., Vázquez, F., Castaño, L. (2003) HLA-DRB1 and MICA in autoimmunity: common associated alleles in autoimmune disorders. Ann. N. Y. Acad. Sci. 1005, 314–318.
53. Seery, J. P., Carroll, J. M., Cattell, V., Watt, F. M. (1997) Antinuclear autoantibodies and lupus nephritis in transgenic mice expressing interferon gamma in the epidermis. J. Exp. Med. 186, 1451–1459.
54. Lee, S. K., Silva, D. G., Martin, J. L., Pratama, A., Hu, X., Chang, P. P., Walters, G., Vinuesa, C. G. (2012) Interferon-g excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity 37, 880–892.
55. Pollard, K. M., Cauvi, D. M., Toomey, C. B., Morris, K. V., Kono, D. H. (2013) Interferon-g and systemic autoimmunity. Discov. Med. 16, 123–131.
56. Eckelhart, E., Warsch, W., Zebedin, E., Simma, O., Stoiber, D., Kolbe, T., Rülicke, T., Mueller, M., Casanova, E., Sexl, V. (2011) A novel Ncr1-Cre mouse reveals the essential role of STAT5 for NK-cell survival and development. Blood 117, 1565–1573.
57. Aramaki, T., Ida, H., Izumi, Y., Fujikawa, K., Huang, M., Arima, K., Tamai, M., Kamachi, M., Nakamura, H., Kawakami, A., Origuchi, T., Matsuoka, N., Eguchi, K. (2009) A significantly impaired natural killer cell activity due to a low activity on a per-cell basis in rheumatoid arthritis. Mod. Rheumatol. 19, 245–252.
58. De Matos, C. T., Berg, L., Michaëlsson, J., Felländer-Tsai, L., Kärre, K., Söderström, K. (2007) Activating and inhibitory receptors on synovial fluid natural killer cells of arthritis patients: role of CD94/NKG2A in control of cytokine secretion. Immunology 122, 291–301.
59. Inoue, A., Hasegawa, H., Kohno, M., Ito, M. R., Terada, M., Imai, T., Yoshie, O., Nose, M., Fujita, S. (2005) Antagonist of fractalkine (CX3CL1) delays the initiation and ameliorates the progression of lupus nephritis in MRL/lpr mice. Arthritis Rheum. 52, 1522–1533.
60. Schwarting, A., Tesch, G., Kinoshita, K., Maron, R., Weiner, H. L., Kelley, V. R. (1999) IL-12 drives IFN-gamma-dependent autoimmune kidney disease in MRL-Fas(lpr) mice. J. Immunol. 163, 6884–6891.
61. Kikawada, E., Lenda, D. M., Kelley, V. R. (2003) IL-12 deficiency in MRLFas(lpr) mice delays nephritis and intrarenal IFN-gamma expression, and diminishes systemic pathology. J. Immunol. 170, 3915–3925.
62. Yoneda, O., Imai, T., Nishimura, M., Miyaji, M., Mimori, T., Okazaki, T., Domae, N., Fujimoto, H., Minami, Y., Kono, T., Bloom, E. T., Umehara, H. (2003) Membrane-bound form of fractalkine induces IFN-gamma production by NK cells. Eur. J. Immunol. 33, 53–58.
63. Boswell, J. M., Yui, M. A., Burt, D. W., Kelley, V. E. (1988) Increased tumor necrosis factor and IL-1 beta gene expression in the kidneys of mice with lupus nephritis. J. Immunol. 141, 3050–3054.
64. Brennan, D. C., Yui, M. A., Wuthrich, R. P., Kelley, V. E. (1989) Tumor necrosis factor and IL-1 in New Zealand Black/White mice. Enhanced gene expression and acceleration of renal injury. J. Immunol. 143, 3470–3475.
65. Williams, V. L., Cohen, P. R. (2011) TNF alpha antagonist-induced lupuslike syndrome: report and review of the literature with implications for treatment with alternative TNF alpha antagonists. Int. J. Dermatol. 50, 619–625.
66. Yung, S., Cheung, K. F., Zhang, Q., Chan, T. M. (2013) Mediators of inflammation and their effect on resident renal cells: implications in lupus nephritis. Clin. Dev. Immunol. 2013, 317682.
67. Iwata, Y., Wada, T., Furuichi, K., Sakai, N., Matsushima, K., Yokoyama, H., Kobayashi, K. (2003) P38 Mitogen-activated protein kinase contributes to autoimmune renal injury in MRL-Fas lpr mice. J. Am. Soc. Nephrol. 14, 57–67.
68. Baranda, L., de la Fuente, H., Layseca-Espinosa, E., Portales-Pérez, D., Niño-Moreno, P., Valencia-Pacheco, G., Abud-Mendoza, C., Alcocer- Varela, J., González-Amaro, R. (2005) IL-15 and IL-15R in leucocytes from patients with systemic lupus erythematosus. Rheumatology (Oxford) 44, 1507–1513.
69. Bo, H., Wei, X. Q., Dong, H., Zhang, Y., Lv, P., Liu, W., Koutoulaki, A., Gao, X. M. (2009) Elevated expression of transmembrane IL-15 in immune cells correlates with the development of murine lupus: a potential target for immunotherapy against SLE. Scand. J. Immunol. 69, 119–129.
70. Postól, E., Meyer, A., Cardillo, F., de Alencar, R., Pessina, D., Nihei, J., Mariano, M., Mengel, J. (2008) Long-term administration of IgG2a anti- NK1.1 monoclonal antibody ameliorates lupus-like disease in NZB/W mice in spite of an early worsening induced by an IgG2a-dependent BAFF/BLyS production. Immunology 125, 184–196.