Galectin-9 inhibits TLR7-mediated autoimmunity in murine lupus models

Journal of Clinical Investigation

Volumn 128, Issue 5, 2018, Pages 1873-1887

  Panda, Santosh K ^a,b   Facchinetti, Valeria ^c   Voynova, Elisaveta ^a   Hanabuchi, Shino ^a,b   Karnell, Jodi L ^a   Hanna, Richard N ^a   Kolbeck, Roland ^a   Sanjuan, Miguel A ^a,e   Ettinger, Rachel ^a,d   Liu, Yong Jun ^a,b,c,d  

^a MEDIMMUNE   (United States)

^b BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d Viela Bio   (United States)

^e BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECALECTIN; TOLL LIKE RECEPTOR 7; AUTOANTIBODY; GALECTIN; GALECTIN 9, MOUSE; LGALS9 PROTEIN, HUMAN; MEMBRANE PROTEIN; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; S6 KINASE; TARGET OF RAPAMYCIN KINASE; TLR7 PROTEIN, HUMAN; TLR7 PROTEIN, MOUSE; TLR9 PROTEIN, HUMAN; TLR9 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY COMPLEX; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RESPONSE; DRUG MECHANISM; EXTRACELLULAR TRAP; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; MTOR SIGNALING; NONHUMAN; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; SPLENOMEGALY; SYSTEMIC LUPUS ERYTHEMATOSUS; THERAPY EFFECT; ANIMAL; DENDRITIC CELL; DISEASE MODEL; IMMUNOLOGY; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; GALECTINS; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MEMBRANE GLYCOPROTEINS; MICE; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9; TOR SERINE-THREONINE KINASES;

EID: 85046448306     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI97333     Document Type: Article

References (57)

1. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol. 2006;6(11):823-835.
2. Banchereau J, Pascual V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity. 2006;25(3):383-392.
3. Toong C, Adelstein S, Phan TG. Clearing the complexity: immune complexes and their treatment in lupus nephritis. Int J Nephrol Renovasc Dis. 2011;4:17-28.
4. Rönnblom L, Pascual V. The innate immune system in SLE: type I interferons and dendritic cells. Lupus. 2008;17(5):394-399.
5. Green NM, Marshak-Rothstein A. Toll-like receptor driven B cell activation in the induction of systemic autoimmunity. Semin Immunol. 2011;23(2):106-112.
6. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V. Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol. 2011;29:163-183.
7. Swiecki M, Colonna M. The multifaceted biology of plasmacytoid dendritic cells. Nat Rev Immunol. 2015;15(8):471-485.
8. Bao M, Liu YJ. Regulation of TLR7/9 signaling in plasmacytoid dendritic cells. Protein Cell. 2013;4(1):40-52.
9. Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol. 2008;8(8):594-606.
10. Garcia-Romo GS, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. SciTransl Med. 2011;3(73):73ra20.
11. Rowland SL, et al. Early, transient depletion of plasmacytoid dendritic cells ameliorates autoimmunity in a lupus model. J Exp Med. 2014;211(10):1977-1991.
12. Sisirak V, et al. Genetic evidence for the role of plasmacytoid dendritic cells in systemic lupus erythematosus. JExpMed. 2014;211(10):1969-1976.
13. Heer AK, et al. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. JImmunol. 2007;178(4):2182-2191.
14. Giltiay NV, et al. Overexpression of TLR7 promotes cell-intrinsic expansion and autoantibody production by transitional T1 B cells. J Exp Med. 2013;210(12):2773-2789.
15. Ehlers M, Fukuyama H, McGaha TL, Ader-em A, Ravetch JV. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J Exp Med. 2006;203(3):553-561.
16. Golden-Mason L, et al. Galectin-9 functionally impairs natural killer cells in humans and mice. JVirol. 2013;87(9):4835-4845.
17. Wu C, et al. Galectin-9-CD44 interaction enhances stability and function of adaptive regulatory T cells. Immunity. 2014;41(2):270-282.
18. Arikawa T, et al. Galectin-9 ameliorates immune complex-induced arthritis by regulating Fc gamma R expression on macrophages. Clin Immunol. 2009;133(3):382-392.
19. Seki M, et al. Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin Immunol. 2008;127(1):78-88.
20. Moritoki M, et al. Galectin-9 ameliorates clinical severity of MRL/lpr lupus-prone mice by inducing plasma cell apoptosis independently of Tim-3. PLoS One. 2013;8(4):e60807.
21. Barrat FJ, Meeker T, Chan JH, Guiducci C, Coffman RL. Treatment of lupus-prone mice with a dual inhibitor of TLR7 and TLR9 leads to reduction of autoantibody production and amelioration of disease symptoms. Eur J Immunol. 2007;37(12):3582-3586.
22. Baechler EC, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A. 2003;100(5):2610-2615.
23. Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat Rev Cancer. 2005;5(1):29-41.
24. Li Y, et al. The N- and C-terminal carbohydrate recognition domains of galectin-9 contribute differently to its multiple functions in innate immunity and adaptive immunity. MolImmunol. 2011;48(4):670-677.
25. Hirashima M, et al. Galectin-9 in physiological and pathological conditions. Glycoconj J. 2002;19(7-9):593-600.
26. Vachon E, et al. CD44-mediated phagocytosis induces inside-out activation of complement receptor-3 in murine macrophages. Blood. 2007;110(13):4492-4502.
27. Thorne RF, Legg JW, Isacke CM. The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events. JCellSci. 2004;117(pt 3):373-380.
28. Cao W, et al. Plasmacytoid dendritic cell-specific receptor ILT7-Fc epsilonRI gamma inhibits Toll-like receptor-induced interferon production. J Exp Med. 2006;203(6):1399-1405.
29. Cao W, et al. Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI(3)K-mTOR-p70S6K pathway. Nat Immunol. 2008;9(10):1157-1164.
30. Kobayashi T, et al. The histidine transporter SLC15A4 coordinates mTOR-dependent inflammatory responses and pathogenic antibody production. Immunity. 2014;41(3):375-388.
31. Zhu C, et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol. 2005;6(12):1245-1252.
32. Bi S, Hong PW, Lee B, Baum LG. Galectin-9 binding to cell surface protein disulfide isomerase regulates the redox environment to enhance T-cell migration and HIV entry. Proc Natl Acad Sci U S A. 2011;108(26):10650-10655.
33. Sharma S, et al. T cell immunoglobulin and mucin protein-3 (Tim-3)/Galectin-9 interaction regulates influenza A virus-specific humoral and CD8 T-cell responses. Proc Natl Acad Sci U S A. 2011;108(47):19001-19006.
34. Jayaraman P, et al. Tim3 binding to galectin-9 stimulates antimicrobial immunity. J Exp Med. 2010;207(11):2343-2354.
35. Leitner J, Rieger A, Pickl WF, Zlabinger G, Grab-meier-Pfistershammer K, Steinberger P. TIM-3 does not act as a receptor for galectin-9. PLoS Pathog. 2013;9(3):e1003253.
36. Golden-Mason L, et al. Galectin-9 functionally impairs natural killer cells in humans and mice. JVirol. 2013;87(9):4835-4845.
37. Oomizu S, et al. Galectin-9 suppresses Th17 cell development in an IL-2-dependent but Tim-3-independent manner. Clin Immunol. 2012;143(1):51-58.
38. Katoh S, et al. Galectin-9 inhibits CD44-hyaluro-nan interaction and suppresses a murine model of allergic asthma. Am J Respir Crit Care Med. 2007;176(1):27-35.
39. Tanikawa R, Tanikawa T, Hirashima M, Yamau-chi A, Tanaka Y. Galectin-9 induces osteoblast differentiation through the CD44/Smad signaling pathway. Biochem Biophys Res Commun. 2010;394(2):317-322.
40. Kawana H, et al. CD44 suppresses TLR-mediated inflammation. JImmunol. 2008;180(6):4235-4245.
41. Wu C, et al. Galectin-9-CD44 interaction enhances stability and function of adaptive regulatory T cells. Immunity. 2014;41(2):270-282.
42. Schmitz F, et al. Mammalian target of rapa-mycin (mTOR) orchestrates the defense program of innate immune cells. Eur J Immunol. 2008;38(11):2981-2992.
43. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4(7):528-539.
44. Bourguignon LY. Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskel-eton function promotes tumor progression. Semin Cancer Biol. 2008;18(4):251-259.
45. Ishikawa A, et al. Double-stranded RNA enhances the expression of galectin-9 in vascular endothelial cells. ImmunolCellBiol. 2004;82(4):410-414.
46. Daley D, et al. Dectin 1 activation on macrophages by galectin 9 promotes pancreatic carcinoma and peritumoral immune tolerance. Nat Med. 2017;23(5):556-567.
47. Santiago-Raber ML, et al. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J Exp Med. 2003;197(6):777-788.
48. Baccala R, Gonzalez-Quintial R, Schreiber RD, Lawson BR, Kono DH, Theofilopoulos AN. Anti-IFN-α/β receptor antibody treatment ameliorates disease in lupus-predisposed mice. JImmunol. 2012;189(12):5976-5984.
49. Hoffman RW. T cells in the pathogenesis of systemic lupus erythematosus. Clin Immunol. 2004;113(1):4-13.
50. Huber JP, Farrar JD. Regulation of effector and memory T-cell functions by type I interferon. Immunology. 2011;132(4):466-474.
51. Ito T, et al. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med. 2007;204(1):105-115.
52. + B-cell population is important for the development of autoimmunity. Blood. 2011;118(5):1305-1315.
53. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity. 2003;19(2):225-234.
54. Fairhurst AM, et al. Systemic IFN-α drives kidney nephritis in B6.Sle123 mice. Eur J Immunol. 2008;38(7):1948-1960.
55. Liu Z, Zou Y, Davidson A. Plasma cells in systemic lupus erythematosus: the long and short of it all. Eur J Immunol. 2011;41(3):588-591.
56. Henault J, et al. Self-reactive IgE exacerbates interferon responses associated with autoimmunity. Nat Immunol. 2016;17(2):196-203.
57. Niki T, et al. Galectin-9 is a high affinity IgE-bind-ing lectin with anti-allergic effect by blocking IgE-antigen complex formation. JBiolChem. 2009;284(47):32344-32352.