Galectin-3 modulates Th17 responses by regulating dendritic cell cytokines

American Journal of Pathology

Volumn 183, Issue 4, 2013, Pages 1209-1222

  Fermin Lee, Agnes ^a   Chen, Huan Yuan ^a,b   Wan, Lei ^c   Wu, Sheng Yang ^d   Yu, Jhang Sian ^d   Huang, Annie C ^a   Miaw, Shi Chuen ^d   Hsu, Daniel K ^a,b   Wu Hsieh, Betty A ^d   Liu, Fu Tong ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CURDLAN; CYTOKINE; DECTIN 1; GALECTIN 3; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 23P19; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; RAF PROTEIN; TRANSCRIPTION FACTOR REL; TRANSFORMING GROWTH FACTOR BETA;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DENDRITIC CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH17 CELL;

ADOPTIVE TRANSFER; ANIMALS; BETA-GLUCANS; CANDIDA ALBICANS; CANDIDIASIS; CELL POLARITY; CHICKENS; CYTOKINES; DENDRITIC CELLS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GALECTIN 3; IMMUNITY; INTERLEUKIN-23; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS C-RAF; PROTO-ONCOGENE PROTEINS C-REL; SIGNAL TRANSDUCTION; TH17 CELLS;

EID: 84884543133     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.06.017     Document Type: Article

References (50)

1. W. Huang, L. Na, P.L. Fidel, and P. Schwarzenberger Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice J Infect Dis 190 2004 624 631
2. H.R. Conti, F. Shen, N. Nayyar, E. Stocum, J.N. Sun, M.J. Lindemann, A.W. Ho, J.H. Hai, J.J. Yu, J.W. Jung, S.G. Filler, P. Masso-Welch, M. Edgerton, and S.L. Gaffen Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis J Exp Med 206 2009 299 311
3. D.J. Cua, J. Sherlock, Y. Chen, C.A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, S. Zurawski, M. Wiekowski, S.A. Lira, D. Gorman, R.A. Kastelein, and J.D. Sedgwick Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain Nature 421 2003 744 748
4. C.L. Langrish, Y. Chen, W.M. Blumenschein, J. Mattson, B. Basham, J.D. Sedgwick, T. McClanahan, R.A. Kastelein, and D.J. Cua IL-23 drives a pathogenic T cell population that induces autoimmune inflammation J Exp Med 201 2005 233 240
5. E. Bettelli, Y. Carrier, W. Gao, T. Korn, T.B. Strom, M. Oukka, H.L. Weiner, and V.K. Kuchroo Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells Nature 441 2006 235 238
6. M. Veldhoen, R.J. Hocking, C.J. Atkins, R.M. Locksley, and B. Stockinger TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells Immunity 24 2006 179 189
7. G.J. Clark, N. Angel, M. Kato, J.A. Lopez, K. MacDonald, S. Vuckovic, and D.N.J. Hart The role of dendritic cells in the innate immune system Microbes Infect 2 2000 257 272
8. K. Ariizumi, G.-L. Shen, S. Shikano, S. Xu, R. Ritter, T. Kumamoto, D. Edelbaum, A. Morita, P.R. Bergstresser, and A. Takashima Identification of a novel dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning J Biol Chem 275 2000 20157 20167
9. G.D. Brown, and S. Gordon Immune recognition: a new receptor for β-glucans Nature 413 2001 36 37
10. S. LeibundGut-Landmann, O. Grosz, M.J. Robinson, F. Osorio, E.C. Slack, S.V. Tsoni, E. Schweighoffer, V. Tybulewicz, G.D. Brown, J. Ruland, and C. Reis e Sousa Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17 Nat Immunol 8 2007 630 638
11. S.I. Gringhuis, J. den Dunnen, M. Litjens, M. van der Vlist, B. Wevers, S.C.M. Bruijns, and T.B.H. Geijtenbeek Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-κB activation through Raf-1 and Syk Nat Immunol 10 2009 203 213
12. E.V. Acosta-Rodriguez, G. Napolitani, A. Lanzavecchia, and F. Sallusto Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells Nat Immunol 8 2007 942 949
13. F.-T. Liu, R.J. Patterson, and J.L. Wang Intracellular functions of galectins Biochim Biophys Acta 1572 2002 263 273
14. J. Ochieng, V. Furtak, and P. Lukyanov Extracellular functions of galectin-3 Glycoconj J 19 2004 527 535
15. J. Dumic, S. Dabelic, and M. Flogel Galectin-3: an open-ended story Biochim Biophys Acta 1760 2006 616 635
16. R.-Y. Yang, D.K. Hsu, and F.-T. Liu Expression of galectin-3 modulates T-cell growth and apoptosis Proc Natl Acad Sci U S A 93 1996 6737 6742
17. S.F. Dagher, J.L. Wang, and R.J. Patterson Identification of galectin-3 as a factor in pre-mRNA splicing Proc Natl Acad Sci U S A 92 1995 1213 1217
18. H. Sano, D.K. Hsu, J.R. Apgar, L. Yu, B.B. Sharma, I. Kuwabara, S. Izui, and F.-T. Liu Critical role of galectin-3 in phagocytosis by macrophages J Clin Invest 112 2003 389 397
19. D.K. Hsu, A.I. Chernyavsky, H.-Y. Chen, L. Yu, S.A. Grando, and F.-T. Liu Endogenous galectin-3 is localized in membrane lipid rafts and regulates migration of dendritic cells J Invest Dermatol 129 2008 573 583
20. R.I. Zuberi, D.K. Hsu, O. Kalayci, H.-Y. Chen, H.K. Sheldon, L. Yu, J.R. Apgar, T. Kawakami, C.M. Lilly, and F.-T. Liu Critical role for galectin-3 in airway inflammation and bronchial hyperresponsiveness in a murine model of asthma Am J Pathol 165 2004 2045 2053
21. E.S. Bernardes, N.M. Silva, L.P. Ruas, J.R. Mineo, A.M. Loyola, D.K. Hsu, F.-T. Liu, R. Chammas, and M.C. Roque-Barreira Toxoplasma gondii infection reveals a novel regulatory role for galectin-3 in the interface of innate and adaptive immunity Am J Pathol 168 2006 1910 1920
22. J. Saegusa, D.K. Hsu, H.-Y. Chen, L. Yu, A. Fermin, M.A. Fung, and F.-T. Liu Galectin-3 is critical for the development of the allergic inflammatory response in a mouse model of atopic dermatitis Am J Pathol 174 2009 922 931
23. G.A. Rabinovich, and A. Gruppi Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease Parasite Immunol 27 2005 103 114
24. T. Jouault, M. El Abed-El Behi, M. Martínez-Esparza, L. Breuilh, P.-A. Trinel, M. Chamaillard, F. Trottein, and D. Poulain Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling J Immunol 177 2006 4679 4687
25. A. Esteban, M.W. Popp, V.K. Vyas, K. Strijbis, H.L. Ploegh, and G.R. Fink Fungal recognition is mediated by the association of dectin-1 and galectin-3 in macrophages Proc Natl Acad Sci U S A 108 2011 14270 14275
26. L. Kohatsu, D.K. Hsu, A.G. Jegalian, F.-T. Liu, and L.G. Baum Galectin-3 induces death of Candida species expressing specific beta-1,2-linked mannans J Immunol 177 2006 4718 4726
27. D.K. Hsu, R.-Y. Yang, Z. Pan, L. Yu, D.R. Salomon, W.-P. Fung-Leung, and F.-T. Liu Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses Am J Pathol 156 2000 1073 1083
28. K. Inaba, M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R.M. Steinman Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor J Exp Med 176 1992 1693 1702
29. C.F. d'Ostiani, G. Del Sero, A. Bacci, C. Montagnoli, A. Spreca, A. Mencacci, P. Ricciardi-Castagnoli, and L. Romani Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans J Exp Med 191 2000 1661 1674
30. M. Peters, K. Dudziak, M. Stiehm, and A. Bufe T-cell polarization depends on concentration of the danger signal used to activate dendritic cells Immunol Cell Biol 88 2010 537 544
31. R.J. Carmody, Q. Ruan, H.-C. Liou, and Y.H. Chen Essential roles of c-Rel in TLR-induced IL-23 p19 gene expression in dendritic cells J Immunol 178 2007 186 191
32. S.I. Gringhuis, J. den Dunnen, M. Litjens, B. van het Hof, Y. van Kooyk, and T.B.H. Geijtenbeek C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kB Immunity 26 2007 605 616
33. C. Wellbrock, M. Karasarides, and R. Marais The RAF proteins take centre stage Nat Rev Mol Cell Biol 5 2004 875 885
34. M.G. Netea, G.D. Brown, B.J. Kullberg, and N.A.R. Gow An integrated model of the recognition of Candida albicans by the innate immune system Nat Rev Micro 6 2008 67 78
35. N.A.R. Gow, M.G. Netea, C.A. Munro, G. Ferwerda, S. Bates, H.M. Mora-Montes, L. Walker, T. Jansen, L. Jacobs, V. Tsoni, G.D. Brown, F.C. Odds, J.W.M. Van der Meer, A.J.P. Brown, and B.J. Kullberg Immune recognition of Candida albicans beta-glucan by dectin-1 J Infect Dis 196 2007 1565 1571
36. L. Romani Immunity to fungal infections Nat Rev Immunol 4 2004 11 24
37. M. Laan, Z.-H. Cui, H. Hoshino, J. Lötvall, M. Sjöstrand, D.C. Gruenert, B.-E. Skoogh, and A. Lindén Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways J Immunol 162 1999 2347 2352
38. F. Annunziato, L. Cosmi, V. Santarlasci, L. Maggi, F. Liotta, B. Mazzinghi, E. Parente, L. Filì, S. Ferri, F. Frosali, F. Giudici, P. Romagnani, P. Parronchi, F. Tonelli, E. Maggi, and S. Romagnani Phenotypic and functional features of human Th17 cells J Exp Med 204 2007 1849 1861
39. M.J. McGeachy, Y. Chen, C.M. Tato, A. Laurence, B. Joyce-Shaikh, W.M. Blumenschein, T.K. McClanahan, J.J. O'Shea, and D.J. Cua The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo Nat Immunol 10 2009 314 324
40. G. Radosavljevic, I. Jovanovic, I. Majstorovic, M. Mitrovic, V. Lisnic, N. Arsenijevic, S. Jonjic, and M. Lukic Deletion of galectin-3 in the host attenuates metastasis of murine melanoma by modulating tumor adhesion and NK cell activity Clin Exp Metastasis 28 2011 451 462
41. H.-R. Jiang, Z. Al Rasebi, E. Mensah-Brown, A. Shahin, D. Xu, C.S. Goodyear, S.Y. Fukada, F.-T. Liu, F.Y. Liew, and M.L. Lukic Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis J Immunol 182 2009 1167 1173
42. S. Xu, J. Huo, M. Gunawan, I.H. Su, and K.-P. Lam Activated dectin-1 localizes to lipid raft microdomains for signaling and activation of phagocytosis and cytokine production in dendritic cells J Biol Chem 284 2009 22005 22011
43. K. Nakahira, H.P. Kim, X.H. Geng, A. Nakao, X. Wang, N. Murase, P.F. Drain, X. Wang, M. Sasidhar, E.G. Nabel, T. Takahashi, N.W. Lukacs, S.W. Ryter, K. Morita, and A.M.K. Choi Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts J Exp Med 203 2006 2377 2389
44. J. Cuschieri Implications of lipid raft disintegration: enhanced anti-inflammatory macrophage phenotype Surgery 136 2004 169 175
45. G. Elad-Sfadia, R. Haklai, E. Balan, and Y. Kloog Galectin-3 Augments K-Ras activation and triggers a Ras signal that attenuates ERK but not phosphoinositide 3-kinase activity J Biol Chem 279 2004 34922 34930
46. S.A. Moodie, B.M. Willumsen, M.J. Weber, and A. Wolfman Complexes of Ras. GTP with Raf-1 and mitogen-activated protein kinase kinase Science 260 1993 1658 1661
47. R. Shalom-Feuerstein, S.J. Plowman, B. Rotblat, N. Ariotti, T. Tian, J.F. Hancock, and Y. Kloog K-Ras nanoclustering is subverted by overexpression of the scaffold protein galectin-3 Cancer Res 68 2008 6608 6616
48. S.J. Plowman, C. Muncke, R.G. Parton, and J.F. Hancock H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton Proc Natl Acad Sci U S A 102 2005 15500 15505
49. R. Marais, Y. Light, H.F. Paterson, and C.J. Marshall Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation EMBO J 14 1995 3136 3145
50. M.S. Hayden, and S. Ghosh Signaling to NF-kappaB Genes Dev 18 2004 2195 2224