IL4I1 is a novel regulator of M2 macrophage polarization that can inhibit t cell activation via L-tryptophan and arginine depletion and IL-10 production

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Yue, Yinpu ^a   Huang, Wei ^a   Liang, Jingjing ^a   Guo, Jing ^a   Ji, Jian ^b   Yao, Yunliang ^a,c   Zheng, Mingzhu ^a   Cai, Zhijian ^a   Lu, Linrong ^a   Wang, Jianli ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c HUZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; INTERLEUKIN 10; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; STAT6 PROTEIN; TRYPTOPHAN; CD27 ANTIGEN; CYTOKINE; FLAVOPROTEIN; IL4I1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL POLARITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE; GENE EXPRESSION; GENE FUNCTION; IMMUNOREGULATION; IN VITRO STUDY; INTERLEUKIN 4 INDUCED GENE 1; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE ACTIVATION; ANIMAL; BIOSYNTHESIS; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD27; ARGININE; CELL POLARITY; CELL PROLIFERATION; CYTOKINES; FLAVOPROTEINS; GENE EXPRESSION REGULATION; INTERLEUKIN-10; MACROPHAGES; MICE; T-LYMPHOCYTES; TRYPTOPHAN;

EID: 84957563216     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142979     Document Type: Article

References (35)

1. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nature reviews Immunology. 2011; 11(11):723-37. doi: 10.1038/nri3073 PMID: 21997792
2. Gordon S. Alternative activation of macrophages. Nature reviews Immunology. 2003; 3(1):23-35. doi: 10.1038/nri978 PMID: 12511873
3. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. Journal of immunology. 2000; 164(12):6166-73.
4. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nature reviews Immunology. 2008; 8(12):958-69. doi: 10.1038/nri2448 PMID: 19029990
5. Benoit M, Desnues B, Mege JL. Macrophage polarization in bacterial infections. Journal of immunology. 2008; 181(6):3733-9.
6. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends in immunology. 2004; 25(12):677-86. doi: 10.1016/j.it.2004.09.015 PMID: 15530839
7. Ivashkiv LB. Epigenetic regulation of macrophage polarization and function. Trends in immunology. 2013; 34(5):216-23. doi: 10.1016/j.it.2012.11.001 PMID: 23218730
8. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Frontiers in bioscience: a journal and virtual library. 2008; 13:453-61.
9. Noel W, Raes G, Hassanzadeh Ghassabeh G, De Baetselier P, Beschin A. Alternatively activated macrophages during parasite infections. Trends in parasitology. 2004; 20(3):126-33. doi: 10.1016/j.pt. 2004.01.004 PMID: 15036034
10. Stein M, Keshav S, Harris N, Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. The Journal of experimental medicine. 1992; 176(1):287-92. PMID: 1613462
11. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends in immunology. 2002; 23(11):549-55. PMID: 12401408
12. Boulland ML, Marquet J, Molinier-Frenkel V, Moller P, Guiter C, Lasoudris F, et al. Human IL4I1 is a secreted L-phenylalanine oxidase expressed by mature dendritic cells that inhibits T-lymphocyte proliferation. Blood. 2007; 110(1):220-7. doi: 10.1182/blood-2006-07-036210 PMID: 17356132
13. Chu CC, Paul WE. Fig1, an interleukin 4-induced mouse B cell gene isolated by cDNA representational difference analysis. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94(6):2507-12. PMID: 9122225
14. Mason JM, Naidu MD, Barcia M, Porti D, Chavan SS, Chu CC. IL-4-induced gene-1 is a leukocyte Lamino acid oxidase with an unusual acidic pH preference and lysosomal localization. Journal of immunology. 2004; 173(7):4561-7.
15. Marquet J, Lasoudris F, Cousin C, Puiffe ML, Martin-Garcia N, Baud V, et al. Dichotomy between factors inducing the immunosuppressive enzyme IL-4-induced gene 1 (IL4I1) in B lymphocytes and mononuclear phagocytes. European journal of immunology. 2010; 40(9):2557-68. doi: 10.1002/eji. 201040428 PMID: 20683900
16. Carbonnelle-Puscian A, Copie-Bergman C, Baia M, Martin-Garcia N, Allory Y, Haioun C, et al. The novel immunosuppressive enzyme IL4I1 is expressed by neoplastic cells of several B-cell lymphomas and by tumor-associated macrophages. Leukemia. 2009; 23(5):952-60. doi: 10.1038/leu.2008.380 PMID: 19436310
17. Lasoudris F, Cousin C, Prevost-Blondel A, Martin-Garcia N, Abd-Alsamad I, Ortonne N, et al. IL4I1: an inhibitor of the CD8(+) antitumor T-cell response in vivo. European journal of immunology. 2011; 41 (6):1629-38. doi: 10.1002/eji.201041119 PMID: 21469114
18. Puiffe ML, Lachaise I, Molinier-Frenkel V, Castellano F. Antibacterial properties of the mammalian Lamino acid oxidase IL4I1. PloS one. 2013; 8(1):e54589. doi: 10.1371/journal.pone.0054589 PMID: 23355881
19. Morita S, Kojima T, Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene therapy. 2000; 7(12):1063-6. doi: 10.1038/sj.gt.3301206 PMID: 10871756
20. Kaplan MH, Schindler U, Smiley ST, Grusby MJ. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity. 1996; 4(3):313-9. PMID: 8624821
21. Takeda K, Clausen BE, Kaisho T, Tsujimura T, Terada N, Forster I, et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity. 1999; 10(1):39-49. PMID: 10023769
22. Gray MJ, Poljakovic M, Kepka-Lenhart D, Morris SM Jr. Induction of arginase I transcription by IL-4 requires a composite DNA response element for STAT6 and C/EBPbeta. Gene. 2005; 353(1):98-106. doi: 10.1016/j.gene.2005.04.004 PMID: 15922518
23. Stutz AM, Pickart LA, Trifilieff A, Baumruker T, Prieschl-Strassmayr E, Woisetschlager M. The Th2 cell cytokines IL-4 and IL-13 regulate found in inflammatory zone 1/resistin-like molecule alpha gene expression by a STAT6 and CCAAT/enhancer-binding protein-dependent mechanism. Journal of immunology. 2003; 170(4):1789-96.
24. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annual review of immunology. 2009; 27:451-83. doi: 10.1146/annurev.immunol.021908. 132532 PMID: 19105661
25. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. The Journal of clinical investigation. 2012; 122(3):787-95. doi: 10.1172/JCI59643 PMID: 22378047
26. Munn DH, Shafizadeh E, Attwood JT, Bondarev I, Pashine A, Mellor AL. Inhibition of T cell proliferation by macrophage tryptophan catabolism. The Journal of experimental medicine. 1999; 189(9):1363-72. PMID: 10224276
27. Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, Ferrara GB. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. The Journal of experimental medicine. 2002; 196(4):459-68. PMID: 12186838
28. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nature reviews Immunology. 2004; 4(10):762-74. doi: 10.1038/nri1457 PMID: 15459668
29. Hildeman DA, Mitchell T, Teague TK, Henson P, Day BJ, Kappler J, et al. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity. 1999; 10(6):735-44. PMID: 10403648
30. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. Journal of immunology. 2004; 172(2):989-99.
31. Curtsinger JM, Schmidt CS, Mondino A, Lins DC, Kedl RM, Jenkins MK, et al. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. Journal of immunology. 1999; 162 (6):3256-62.
32. Munn DH, Armstrong E. Cytokine regulation of human monocyte differentiation in vitro: the tumor-cytotoxic phenotype induced by macrophage colony-stimulating factor is developmentally regulated by gamma-interferon. Cancer research. 1993; 53(11):2603-13. PMID: 8495423
33. Munn DH, Pressey J, Beall AC, Hudes R, Alderson MR. Selective activation-induced apoptosis of peripheral T cells imposed by macrophages. A potential mechanism of antigen-specific peripheral lymphocyte deletion. Journal of immunology. 1996; 156(2):523-32.
34. Rodriguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunological reviews. 2008; 222:180-91. doi: 10.1111/j.1600-065X.2008.00608.x PMID: 18364002
35. Bingisser RM, Tilbrook PA, Holt PG, Kees UR. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. Journal of immunology. 1998; 160 (12):5729-34.