Galectin-9 Ameliorates Clinical Severity of MRL/lpr Lupus-Prone Mice by Inducing Plasma Cell Apoptosis Independently of Tim-3

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Moritoki, Masahiro ^a   Kadowaki, Takeshi ^a   Niki, Toshiro ^a   Nakano, Daisuke ^a   Soma, Genichiro ^a   Mori, Hirohito ^a   Kobara, Hideki ^a   Masaki, Tsutomu ^a   Kohno, Masakazu ^a   Hirashima, Mitsuomi ^a  

^a KAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; CD19 ANTIGEN; CELL PROTEIN; DOUBLE STRANDED DNA ANTIBODY; ECALECTIN; PROTEIN TIM 3; SYNDECAN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; APOPTOSIS; ARTHRITIS; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG MECHANISM; HEMATOCRIT; HEMOLYTIC ANEMIA; LUPUS ERYTHEMATOSUS NEPHRITIS; MOUSE; NONHUMAN; PROTEINURIA; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL;

ANIMALS; ANTIBODIES, ANTINUCLEAR; APOPTOSIS; B-CELL ACTIVATING FACTOR; CD8-POSITIVE T-LYMPHOCYTES; GALECTINS; GENE EXPRESSION REGULATION; HEMATOCRIT; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED MRL LPR; PLASMA CELLS; PROTEINURIA; RECEPTORS, VIRUS; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; TH1 CELLS; TH17 CELLS;

MURINAE; MUS;

EID: 84876066355     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060807     Document Type: Article

References (44)

1. Anaya JM, Canas C, Mantilla RD, Pineda-Tamayo R, Tobon GJ, et al. (2011) Lupus nephritis in Colombians: contrasts and comparisons with other populations. Clin Rev Allergy Immunol 40: 199-207.
2. Davidson A, (2012) The Rationale for BAFF Inhibition in Systemic Lupus Erythematosus. Curr Rheumatol Rep 14: 295-302.
3. Liu Z, Davidson A, (2011) BAFF and selection of autoreactive B cells. Trends Immunol 32: 388-394.
4. Liu Z, Davidson A, (2011) BAFF inhibition: a new class of drugs for the treatment of autoimmunity. Exp Cell Res 317: 1270-1277.
5. Seki M, Oomizu S, Sakata KM, Sakata A, Arikawa T, et al. (2008) Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin Immunol 127: 78-88.
6. Oomizu S, Arikawa T, Niki T, Kadowaki T, Ueno M, et al. (2012) Galectin-9 suppresses Th17 cell development in an IL-2-dependent but Tim-3-independent manner. Clin Immunol 143: 51-58.
7. Kanzaki M, Wada J, Sugiyama K, Nakatsuka A, Teshigawara S, et al. (2012) Galectin-9 and T cell immunoglobulin mucin-3 pathway is a therapeutic target for type 1 diabetes. Endocrinology 153: 612-620.
8. Wiersma VR, de Bruyn M, Helfrich W, Bremer E (2011) Therapeutic potential of Galectin-9 in human disease. Med Res Rev July 26. doi:10 1002/med.20249.
9. Arikawa T, Watanabe K, Seki M, Matsukawa A, Oomizu S, et al. (2009) Galectin-9 ameliorates immune complex-induced arthritis by regulating Fc gamma R expression on macrophages. Clin Immunol 133 (2009) 382-392.
10. Nishi N, Itoh A, Fujiyama A, Yoshida N, Araya S, et al. (2005) Development of highly stable galectins: truncation of the linker peptide confers protease-resistance on tandem-repeat type galectins. FEBS Lett 579: 2058-2064.
11. Koopman WJ, Gay S (1988) The MRL-lpr/lpr mouse. A model for the study of rheumatoid arthritis, Scand J Rheumatol Suppl 75: 284-289.
12. Fagiolo E, Toriani-Terenzi C, (2003) Mechanisms of immunological tolerance loss versus erythrocyte self-antigens and autoimmune hemolytic anemia, Autoimmunity. 36: 199-204.
13. Lee J, Park EJ, Noh JW, Hwang JW, Bae EK, et al. (2012) Underexpression of TIM-3 and blunted galectin-9-induced apoptosis of CD4+ T cells in rheumatoid arthritis. Inflammation 35: 633-637.
14. Wang F, Xu J, Liao Y, Wang Y, Liu C, et al. (2011) Tim-3 ligand galectin-9 reduces IL-17 level and accelerates Klebsiella pneumoniae infection. Cell Immunol 269: 22-28.
15. Sakai K, Kawata E, Ashihara E, Nakagawa Y, Yamauchi A, et al. (2011) Galectin-9 ameliorates acute GVH disease through the induction of T-cell apoptosis. Eur J Immunol 41: 67-75.
16. Tsuchiyama Y, Wada J, Zhang H, Morita Y, Hiragushi K, et al. (2000) Efficacy of galectins in the amelioration of nephrotoxic serum nephritis in Wistar Kyoto rats. Kidney Int 58: 1941-1952.
17. Wang F, He W, Zhou H, Yuan J, Wu K, et al. (2007) The Tim-3 ligand galectin-9 negatively regulates CD8+ alloreactive T cell and prolongs survival of skin graft. Cell Immunol 250: 68-74.
18. Dillon SR, Harder B, Lewis KB, Moore MD, Liu H, et al. (2010) B-lymphocyte stimulator/a proliferation-inducing ligand heterotrimers are elevated in the sera of patients with autoimmune disease and are neutralized by atacicept and B-cell maturation antigen-immunoglobulin. Arthritis Res Ther 12: R48.
19. Koyama T, Tsukamoto H, Miyagi Y, Himeji D, Otsuka J, et al. (2005) Raised serum APRIL levels in patients with systemic lupus erythematosus. Ann Rheum Dis 64: 1065-1067.
20. Gross JA, Johnston J, Mudri S, Enselman R, Dillon SR, et al. (2000) TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404: 995-999.
21. Mackay F, Sierro F, Grey ST, Gordon TP, (2005) The BAFF/APRIL system: an important player in systemic rheumatic diseases. Curr Dir Autoimmun 8: 243-265.
22. Shah K, Lee WW, Lee SH, Kim SH, Kang SW, et al. (2010) Dysregulated balance of Th17 and Th1 cells in systemic lupus erythematosus. Arthritis Res Ther 12: R53.
23. Kleczynska W, Jakiela B, Plutecka H, Milewski M, Sanak M, et al. (2011) Imbalance between Th17 and regulatory T-cells in systemic lupus erythematosus. Folia Histochem Cytobiol 49: 646-653.
24. Yang J, Chu Y, Yang X, Gao D, Zhu L, et al. (2009) Th17 and natural Treg cell population dynamics in systemic lupus erythematosus. Arthritis Rheum 60: 1472-1483.
25. Hou LF, He SJ, Li X, Yang Y, He PL, et al. (2011) Oral administration of artemisinin analogue SM 934 ameliorates lupus syndromes in MRL/lpr mice by inhibiting Th1 and Th17 cell responses. Arthritis Rheum 63: 2445-2455.
26. Wang F, He W, Zhou H, Yuan J, Wu K, et al. (2007) The Tim-3 ligand galectin-9 negatively regulates CD8+ alloreactive T cell and prolongs survival of skin graft. Cell Immunol 250: 68-74.
27. Reddy PB, Sehrawat S, Suryawanshi A, Rajasagi NK, Mulik S, et al. (2011) Influence of galectin-9/Tim-3 interaction on herpes simplex virus-1 latency. J Immunol 187: 5745-5755.
28. Sehrawat S, Reddy PB, Rajasagi N, Suryanshi A, Hirashima M, et al. (2010) Galectin-9/TIM-3 interaction regulates virus-specific primary and memory CD8 T cell response. PLoS Pathog 6: e1000882.
29. Winchester R, Wiesendanger M, Zhang HZ, Steshenko V, Peterson K, et al. (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.
30. Manzi S, Sanchez-Guerrero J, Merrill JT, Furie R, Gladman D, et al. (2012) Effects of belimumab, a B lymphocyte stimulator-specific inhibitor, on disease activity across multiple organ domains in patients with systemic lupus erythematosus: combined results from two phase III trials. Ann Rheum Dis May 11.
31. Fiorina P, Sayegh MH, (2009) B cell-targeted therapies in autoimmunity: rationale and progress. F1000 Biol Rep May 28 1: 39 doi:10.3410/B1-39.
32. Dall'Era M, Chakravarty E, Wallace D, Genovese M, Weisman M, et al. (2007) Reduced B lymphocyte and immunoglobulin levels after atacicept treatment in patients with systemic lupus erythematosus: results of a multicenter, phase Ib, double-blind, placebo-controlled, dose-escalating trial. Arthritis Rheum 56: 4142-4150.
33. Chu VT, Enghard P, Riemekasten G, Berek C, (2007) In vitro and in vivo activation induces BAFF and APRIL expression in B cells. J Immunol 179: 5947-5957.
34. Belnoue E, Pihlgren M, McGaha TL, Tougne C, Rochat AF, (2008) APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells. Blood 111: 2755-2764.
35. WilsonLE, Widman D, Dikman SH, Gorevic PD, (2002) Autoimmune disease complicating antiviral therapy for hepatitis C virus infection. Semin Arthritis Rheum 32: 163-173.
36. Mathian A, Weinberg A, Gallegos M, Banchereau J, Koutouzov S, (2005) IFN-alpha induces early lethal lupus in preautoimmune (New Zealand Black x New Zealand White) F1 but not in BALB/c mice. J Immunol 174: 2499-2506.
37. Mohan AK, Edwards ET, Cote TR, Siegel JN, Braun MM, (2002) Drug-induced systemic lupus erythematosus and TNF-alpha blockers. Lancet 360: 646.
38. Nagel A, Podstawa E, Eickmann M, Muller HH, Hertl M, et al. (2009) Rituximab mediates a strong elevation of B-cell-activating factor associated with increased pathogen-specific IgG but not autoantibodies in pemphigus vulgaris. J Invest Dermatol 129: 2202-2210.
39. Jones RB, Ndhlovu LC, Barbour JD, Sheth PM, Jha AR, et al. (2008) Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 205: 2763-79.
40. Reddy PB, Sehrawat S, Suryawanshi A, Rajasagi NK, Mulik S, et al. (2011) Influence of galectin-9/Tim-3 interaction on herpes simplex virus-1 latency. J. Immunol 187: 5745-55.
41. Pan HF, Zhang N, Li WX, Tao JH, Ye DQ, (2010) TIM-3 as a new therapeutic target in systemic lupus erythematosus. Mol Biol Rep 37: 395-398.
42. Wang Y, Meng J, Wang X, Liu S, Shu Q, et al. (2008) Expression of human TIM-1 and TIM-3 on lymphocytes from systemic lupus erythematosus patients. Scand J Immunol 67: 63-70.
43. Kadowaki T, Arikawa T, Shinonaga R, Oomizu S, Inagawa H, et al. (2012) Galectin-9 signaling prolongs survival in murine lung-cancer by inducing macrophages to differentiate into plasmacytoid dendritic cell-like macrophages. Clin Immunol 142: 296-307.
44. Arikawa T, Saita N, Oomizu S, Ueno M, Matsukawa A, et al. (2010) Galectin-9 expands immunosuppressive macrophages to ameliorate T-cell-mediated lung inflammation. Eur J Immunol 40: 548-558.