α-galactosylceramide but not phenyl-glycolipids induced NKT cell anergy and IL-33-mediated myeloid-derived suppressor cell accumulation via upregulation of egr2/3

Journal of Immunology

Volumn 192, Issue 4, 2014, Pages 1972-1981

  Huang, Jing Rong ^a,b   Tsai, Yi Chien ^b,c   Chang, Ya Jen ^b   Wu, Jen Chien ^b,d   Hung, Jung Tung ^b,d   Lin, Kun Hsien ^b,e   Wong, Chi Huey ^b   Yu, Alice L ^b,d,f  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b GENOMICS RESEARCH CENTER   (Taiwan)

^c NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^d CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CBL PROTEIN; EARLY GROWTH RESPONSE FACTOR 2; EARLY GROWTH RESPONSE FACTOR 3; FAS LIGAND; GLYCOLIPID; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 33; PHENYLGLYCOLIPID; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARG 1 GENE; ARTICLE; BONE MARROW CELL; CLONAL ANERGY; CONTROLLED STUDY; EGR2 GENE; EGR3 GENE; FEMALE; GENE; KUPFFER CELL; LIVER INJURY; MACROPHAGE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SUPPRESSOR CELL; TUMOR ASSOCIATED LEUKOCYTE; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD274; ANTINEOPLASTIC AGENTS; ARGINASE; CELL LINE, TUMOR; CLONAL ANERGY; EARLY GROWTH RESPONSE PROTEIN 2; EARLY GROWTH RESPONSE PROTEIN 3; FAS LIGAND PROTEIN; FEMALE; GALACTOSYLCERAMIDES; GRANULOCYTE COLONY-STIMULATING FACTOR; IMMUNOSUPPRESSION; IMMUNOTHERAPY; INTERLEUKINS; KUPFFER CELLS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MYELOID CELLS; NATURAL KILLER T-CELLS; PROGRAMMED CELL DEATH 1 RECEPTOR; PROTO-ONCOGENE PROTEINS C-CBL; RNA, MESSENGER; SPLEEN; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UP-REGULATION;

EID: 84896726330     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302623     Document Type: Article

References (51)

1. Kronenberg, M. 2005. Toward an understanding of NKT cell biology: progress and paradoxes. Annu. Rev. Immunol. 23: 877-900.
2. Okajo, J., Y. Kaneko, Y. Murata, T. Tomizawa, C. Okuzawa, Y. Saito, Y. Kaneko, T. Ishikawa-Sekigami, H. Okazawa, H. Ohnishi, et al. 2007. Regulation by Src homology 2 domain-containing protein tyrosine phosphatase substrate-1 of α-galactosylceramide-induced antimetastatic activity and Th1 and Th2 responses of NKT cells. J. Immunol. 178: 6164-6172.
3. Onoé, K., Y. Yanagawa, K. Minami, N. Iijima, and K. Iwabuchi. 2007. Th1 or Th2 balance regulated by interaction between dendritic cells and NKT cells. Immunol. Res. 38: 319-332.
4. Shin, T., T. Nakayama, Y. Akutsu, S. Motohashi, Y. Shibata, M. Harada, N. Kamada, C. Shimizu, E. Shimizu, T. Saito, T. Ochiai, and M. Taniguchi. 2001. Inhibition of tumor metastasis by adoptive transfer of IL-12-activated Vα14 NKT cells. Int. J. Cancer 91: 523-528.
5. Furlan, R., A. Bergami, D. Cantarella, E. Brambilla, M. Taniguchi, P. Dellabona, G. Casorati, and G. Martino. 2003. Activation of invariant NKT cells by αGalCer administration protects mice from MOG35-55-induced EAE: critical roles for administration route and IFN-γ. Eur. J. Immunol. 33: 1830-1838.
6. Parekh, V. V., M. T. Wilson, D. Olivares-Villagómez, A. K. Singh, L. Wu, C. R. Wang, S. Joyce, and L. Van Kaer. 2005. Glycolipid antigen induces longterm natural killer T cell anergy in mice. J. Clin. Invest. 115: 2572-2583.
7. Chang, Y. J., J. R. Huang, Y. C. Tsai, J. T. Hung, D. Wu, M. Fujio, C. H. Wong, and A. L. Yu. 2007. Potent immune-modulating and anticancer effects of NKT cell stimulatory glycolipids. Proc. Natl. Acad. Sci. USA 104: 10299-10304.
8. Wu, T. N., K. H. Lin, Y. J. Chang, J. R. Huang, J. Y. Cheng, A. L. Yu, and C. H. Wong. 2011. Avidity of CD1d-ligand-receptor ternary complex contributes to T-helper 1 (Th1) polarization and anticancer efficacy. Proc. Natl. Acad. Sci. USA 108: 17275-17280.
9. Parekh, V. V., S. Lalani, S. Kim, R. Halder, M. Azuma, H. Yagita, V. Kumar, L. Wu, and L. V. Kaer. 2009. PD-1/PD-L blockade prevents anergy induction and enhances the anti-tumor activities of glycolipid-activated invariant NKT cells. J. Immunol. 182: 2816-2826.
10. Tsushima, F., S. Yao, T. Shin, A. Flies, S. Flies, H. Xu, K. Tamada, D. M. Pardoll, and L. Chen. 2007. Interaction between B7-H1 and PD-1 determines initiation and reversal of T-cell anergy. Blood 110: 180-185.
11. Jeon, M. S., A. Atfield, K. Venuprasad, C. Krawczyk, R. Sarao, C. Elly, C. Yang, S. Arya, K. Bachmaier, L. Su, et al. 2004. Essential role of the E3 ubiquitin ligase Cbl-b in T cell anergy induction. Immunity 21: 167-177.
12. Kojo, S., C. Elly, Y. Harada, W. Y. Langdon, M. Kronenberg, and Y. C. Liu. 2009. Mechanisms of NKT cell anergy induction involve Cbl-b-promoted monoubiquitination of CARMA1. Proc. Natl. Acad. Sci. USA 106: 17847-17851.
13. Ascierto, P. A., E. Simeone, M. Sznol, Y. X. Fu, and I. Melero. 2010. Clinical experiences with anti-CD137 and anti-PD1 therapeutic antibodies. Semin. Oncol. 37: 508-516.
14. Simpson, K. D., and J. V. Cross. 2013. MIF: metastasis/MDSC-inducing factor? OncoImmunology 2: e23337.
15. Bunt, S. K., P. Sinha, V. K. Clements, J. Leips, and S. Ostrand-Rosenberg. 2006. Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 176: 284-290.
16. Sinha, P., V. K. Clements, and S. Ostrand-Rosenberg. 2005. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J. Immunol. 174: 636-645.
17. Youn, J. I., S. Nagaraj, M. Collazo, and D. I. Gabrilovich. 2008. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181: 5791-5802.
18. Dugast, A. S., T. Haudebourg, F. Coulon, M. Heslan, F. Haspot, N. Poirier, R. Vuillefroy de Silly, C. Usal, H. Smit, B. Martinet, et al. 2008. Myeloid-derived suppressor cells accumulate in kidney allograft tolerance and specifically suppress effector T cell expansion. J. Immunol. 180: 7898-7906.
19. + T cells. J. Immunol. 183: 937-944.
20. Moliné-Velázquez, V., H. Cuervo, V. Vila-Del Sol, M. C. Ortega, D. Clemente, and F. de Castro. 2011. Myeloid-derived suppressor cells limit the inflammation by promoting T lymphocyte apoptosis in the spinal cord of a murine model of multiple sclerosis. Brain Pathol. 21: 678-691.
21. Li, H., Y. Han, Q. Guo, M. Zhang, and X. Cao. 2009. Cancer-expanded myeloidderived suppressor cells induce anergy of NK cells through membrane-bound TGF-β1. J. Immunol. 182: 240-249.
22. Rodríguez, P. C., and A. C. Ochoa. 2008. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol. Rev. 222: 180-191.
23. Raber, P., A. C. Ochoa, and P. C. Rodríguez. 2012. Metabolism of L-arginine by myeloid-derived suppressor cells in cancer: mechanisms of T cell suppression and therapeutic perspectives. Immunol. Invest. 41: 614-634.
24. - bone marrow progenitor cells into myeloid-derived suppressor cells. Breast Cancer Res. Treat. 123: 39-49.
25. Domínguez-Soto, A., E. Sierra-Filardi, A. Puig-Kröger, B. Pérez-Maceda, F. Gómez-Aguado, M. T. Corcuera, P. Sánchez-Mateos, and A. L. Corbí. 2011. Dendritic cell-specific ICAM-3-grabbing nonintegrin expression on M2-polarized and tumor-associated macrophages is macrophage-CSF dependent and enhanced by tumor-derived IL-6 and IL-10. J. Immunol. 186: 2192-2200.
26. Sinha, P., V. K. Clements, and S. Ostrand-Rosenberg. 2005. Interleukin-13-regulated M2 macrophages in combination with myeloid suppressor cells block immune surveillance against metastasis. Cancer Res. 65: 11743-11751.
27. Bansal, V., and J. B. Ochoa. 2003. Arginine availability, arginase, and the immune response. Curr. Opin. Clin. Nutr. Metab. Care 6: 223-228.
28. Fujii, H., S. Seki, S. Kobayashi, T. Kitada, N. Kawakita, K. Adachi, H. Tsutsui, K. Nakanishi, H. Fujiwara, Y. Ikarashi, et al. 2005. A murine model of NKT cellmediated liver injury induced by α-galactosylceramide/D- galactosamine. Virch. Arch. 446: 663-673.
29. Zheng, Y., Y. Zha, and T. F. Gajewski. 2008. Molecular regulation of T-cell anergy. EMBO Rep. 9: 50-55.
30. Fujio, M., D. Wu, R. Garcia-Navarro, D. D. Ho, M. Tsuji, and C. H. Wong. 2006. Structure-based discovery of glycolipids for CD1d-mediated NKT cell activation: tuning the adjuvant versus immunosuppression activity. J. Am. Chem. Soc. 128: 9022-9023.
31. Sidobre, S., O. V. Naidenko, B. C. Sim, N. R. Gascoigne, K. C. Garcia, and M. Kronenberg. 2002. The Vα14 NKT cell TCR exhibits high-affinity binding to a glycolipid/CD1d complex. J. Immunol. 169: 1340-1348.
32. Liu, Y., Y. Yu, S. Yang, B. Zeng, Z. Zhang, G. Jiao, Y. Zhang, L. Cai, and R. Yang. 2009. Regulation of arginase I activity and expression by both PD-1 and CTLA-4 on the myeloid-derived suppressor cells. Cancer Immunol. Immunother. 58: 687-697.
33. Arshad, M. I., M. Rauch, A. L'helgoualc'h, V. Julia, M. C. Leite-de-Moraes, C. Lucas-Clerc, C. Piquet-Pellorce, and M. Samson. 2011. NKT cells are required to induce high IL-33 expression in hepatocytes during Con A-induced acute hepatitis. Eur. J. Immunol. 41: 2341-2348.
34. Nakagawa, R., I. Nagafune, Y. Tazunoki, H. Ehara, H. Tomura, R. Iijima, K. Motoki, M. Kamishohara, and S. Seki. 2001. Mechanisms of the antimetastatic effect in the liver and of the hepatocyte injury induced by α- galactosylceramide in mice. J. Immunol. 166: 6578-6584.
35. Arshad, M. I., C. Piquet-Pellorce, A. L'Helgoualc'h, M. Rauch, S. Patrat-Delon, F. Ezan, C. Lucas-Clerc, S. Nabti, A. Lehuen, F. J. Cubero, et al. 2012. TRAIL but not FasL and TNFα, regulates IL-33 expression in murine hepatocytes during acute hepatitis. Hepatology 56: 2353-2362.
36. Mittelstadt, P. R., and J. D. Ashwell. 1999. Role of Egr-2 in up-regulation of Fas ligand in normal T cells and aberrant double-negative lpr and gld T cells. J. Biol. Chem. 274: 3222-3227.
37. Bonello, M. R., and L. M. Khachigian. 2004. Fibroblast growth factor-2 represses platelet-derived growth factor receptor-α (PDGFR-α) transcription via ERK1/2-dependent Sp1 phosphorylation and an atypical cis-acting element in the proximal PDGFR-α promoter. J. Biol. Chem. 279: 2377-2382.
38. Ostrand-Rosenberg, S. 2010. Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol. Immunother. 59: 1593-1600.
39. Lechler, R., J. G. Chai, F. Marelli-Berg, and G. Lombardi. 2001. The contributions of T-cell anergy to peripheral T-cell tolerance. Immunology 103: 262-269.
40. + T cells induced by low avidity engagement of T cell receptor. J. Exp. Med. 194: 719-731.
41. Li, S., T. Miao, M. Sebastian, P. Bhullar, E. Ghaffari, M. Liu, A. L. Symonds, and P. Wang. 2012. The transcription factors Egr2 and Egr3 are essential for the control of inflammation and antigen-induced proliferation of B and T cells. Immunity 37: 685-696.
42. Song, L., S. Asgharzadeh, J. Salo, K. Engell, H. W. Wu, R. Sposto, T. Ara, A. M. Silverman, Y. A. DeClerck, R. C. Seeger, and L. S. Metelitsa. 2009. Vα24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J. Clin. Invest. 119: 1524-1536.
43. + cells, and mediates regulatory T cell-dependent promotion of cardiac allograft survival. J. Immunol. 187: 4598-4610.
44. Peranzoni, E., S. Zilio, I. Marigo, L. Dolcetti, P. Zanovello, S. Mandruzzato, and V. Bronte. 2010. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr. Opin. Immunol. 22: 238-244.
45. Osman, Y., T. Kawamura, T. Naito, K. Takeda, L. Van Kaer, K. Okumura, and T. Abo. 2000. Activation of hepatic NKT cells and subsequent liver injury following administration of alpha-galactosylceramide. Eur. J. Immunol. 30: 1919-1928.
46. Rengarajan, J., P. R. Mittelstadt, H. W. Mages, A. J. Gerth, R. A. Kroczek, J. D. Ashwell, and L. H. Glimcher. 2000. Sequential involvement of NFAT and Egr transcription factors in FasL regulation. Immunity 12: 293-300.
47. Liew, F. Y., N. I. Pitman, and I. B. McInnes. 2010. Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat. Rev. Immunol. 10: 103-110.
48. Arshad, M. I., C. Piquet-Pellorce, and M. Samson. 2012. IL-33 and HMGB1 alarmins: sensors of cellular death and their involvement in liver pathology. Liver Int. 32: 1200-1210.
49. Barbalat, R., S. E. Ewald, M. L. Mouchess, and G. M. Barton. 2011. Nucleic acid recognition by the innate immune system. Annu. Rev. Immunol. 29: 185-214.
50. Ugel, S., F. Delpozzo, G. Desantis, F. Papalini, F. Simonato, N. Sonda, S. Zilio, and V. Bronte. 2009. Therapeutic targeting of myeloid-derived suppressor cells. Curr. Opin. Pharmacol. 9: 470-481.
51. Kline, J., and T. F. Gajewski. 2010. Clinical development of mAbs to block the PD1 pathway as an immunotherapy for cancer. Curr. Opin. Investig. Drugs 11: 1354-1359.