Vitamin e γ-tocotrienol inhibits cytokine-stimulated NF-κB activation by induction of anti-inflammatory A20 via stress adaptive response due to modulation of sphingolipids

Journal of Immunology

Volumn 195, Issue 1, 2015, Pages 126-133

  Wang, Yun ^a   Park, Na Young ^a   Jang, Yumi ^a   Ma, Averil ^b   Jiang, Qing ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; DIHYDROCERAMIDE; GAMMA TOCOTRIENOL; I KAPPA B; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 2; INTERLEUKIN 1BETA; SPHINGOLIPID; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE; GAMMA TOCOPHEROL; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; NF-KAPPAB INHIBITOR ALPHA; OTUD7B PROTEIN, MOUSE; PROTEINASE; SIGNAL PEPTIDE; TNFAIP3 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE SILENCING; IMMUNOMODULATION; LIPOGENESIS; LIQUID CHROMATOGRAPHY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SPHINGOLIPID METABOLISM; TANDEM MASS SPECTROMETRY; UPREGULATION; ADAPTATION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE MARROW CELL; C57BL MOUSE; CELL LINE; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PHYSIOLOGICAL STRESS; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BONE MARROW CELLS; CELL LINE; CYSTEINE ENDOPEPTIDASES; ENDOPEPTIDASES; FIBROBLASTS; GAMMA-TOCOPHEROL; GENE EXPRESSION REGULATION; I-KAPPA B PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MAP KINASE KINASE 4; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; NF-KAPPA B; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; STRESS, PHYSIOLOGICAL;

EID: 84932125603     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1403149     Document Type: Article

References (44)

1. Ben-Neriah, Y., and M. Karin. 2011. Inflammation meets cancer, with NF-kB as the matchmaker. Nat. Immunol. 12: 715-723.
2. Oeckinghaus, A., M. S. Hayden, and S. Ghosh. 2011. Crosstalk in NF-kB signaling pathways. Nat. Immunol. 12: 695-708.
3. Wertz, I. E., and V.M. Dixit. 2010. Signaling to NF-kB: regulation by ubiquitination. Cold Spring Harb. Perspect. Biol. 2: a003350.
4. Hymowitz, S. G., and I. E. Wertz. 2010. A20: from ubiquitin editing to tumour suppression. Nat. Rev. Cancer 10: 332-341.
5. Ruland, J. 2011. Return to homeostasis: downregulation of NF-kB responses. Nat. Immunol. 12: 709-714.
6. Jäättelä, M., H. Mouritzen, F. Elling, and L. Bastholm. 1996. A20 zinc finger protein inhibits TNF and IL-1 signaling. J. Immunol. 156: 1166-1173.
7. Lee, E. G., D. L. Boone, S. Chai, S. L. Libby, M. Chien, J. P. Lodolce, and A. Ma. 2000. Failure to regulate TNF-induced NF-kB and cell death responses in A20-deficient mice. Science 289: 2350-2354.
8. Newton, K., M. L. Matsumoto, I. E. Wertz, D. S. Kirkpatrick, J. R. Lill, J. Tan, D. Dugger, N. Gordon, S. S. Sidhu, F. A. Fellouse, et al. 2008. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134: 668-678.
9. Wertz, I. E., K. M. O'Rourke, H. Zhou, M. Eby, L. Aravind, S. Seshagiri, P. Wu, C. Wiesmann, R. Baker, D. L. Boone, et al. 2004. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kB signalling. Nature 430: 694-699.
10. Vereecke, L., R. Beyaert, and G. van Loo. 2009. The ubiquitin-editing enzyme A20 (TNFAIP3) is a central regulator of immunopathology. Trends Immunol. 30: 383-391.
11. Lu, T. T., M. Onizawa, G. E. Hammer, E. E. Turer, Q. Yin, E. Damko, A. Agelidis, N. Shifrin, R. Advincula, J. Barrera, et al. 2013. Dimerization and ubiquitin mediated recruitment of A20, a complex deubiquitinating enzyme. Immunity 38: 896-905.
12. De, A., T. Dainichi, C. V. Rathinam, and S. Ghosh. 2014. The deubiquitinase activity of A20 is dispensable for NF-kB signaling. EMBO Rep. 15: 775-783.
13. Skaug, B., J. Chen, F. Du, J. He, A. Ma, and Z. J. Chen. 2011. Direct, noncatalytic mechanism of IKK inhibition by A20. Mol. Cell 44: 559-571.
14. Ahn, K. S., G. Sethi, K. Krishnan, and B. B. Aggarwal. 2007. Gammatocotrienol inhibits nuclear factor-kB signaling pathway through inhibition of receptor-interacting protein and TAK1 leading to suppression of antiapoptotic gene products and potentiation of apoptosis. J. Biol. Chem. 282: 809-820.
15. Jiang, Q. 2014. Natural forms of vitamin E: metabolism, antioxidant, and antiinflammatory activities and their role in disease prevention and therapy. Free Radic. Biol. Med. 72: 76-90.
16. Wang, Y., and Q. Jiang. 2013. g-Tocotrienol inhibits lipopolysaccharide-induced interlukin-6 and granulocyte colony-stimulating factor by suppressing C/EBPb and NF-kB in macrophages. J. Nutr. Biochem. 24: 1146-1152.
17. Qureshi, A. A., J. C. Reis, C. J. Papasian, D. C. Morrison, and N. Qureshi. 2010. Tocotrienols inhibit lipopolysaccharide-induced pro-inflammatory cytokines in macrophages of female mice. Lipids Health Dis. 9: 143.
18. Mahalingam, D., A. K. Radhakrishnan, Z. Amom, N. Ibrahim, and K. Nesaretnam. 2011. Effects of supplementation with tocotrienol-rich fraction on immune response to tetanus toxoid immunization in normal healthy volunteers. Eur. J. Clin. Nutr. 65: 63-69.
19. Zhang, X., R. Goncalves, and D. M. Mosser. 2008. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Chapter 14: Unit 14.1. doi:10.1002/0471142735.im1401s83
20. Merrill, A. H., Jr., M. C. Sullards, J. C. Allegood, S. Kelly, and E. Wang. 2005. Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry. Methods 36: 207-224.
21. Chen, Z. J. 2005. Ubiquitin signalling in the NF-kB pathway. Nat. Cell Biol. 7: 758-765.
22. Trompouki, E., E. Hatzivassiliou, T. Tsichritzis, H. Farmer, A. Ashworth, and G. Mosialos. 2003. CYLD is a deubiquitinating enzyme that negatively regulates NF-kB activation by TNFR family members. Nature 424: 793-796.
23. Shembade, N., A. Ma, and E. W. Harhaj. 2010. Inhibition of NF-kB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 327: 1135-1139.
24. Won, M., K. A. Park, H. S. Byun, K. C. Sohn, Y. R. Kim, J. Jeon, J. H. Hong, J. Park, J. H. Seok, J. M. Kim, et al. 2010. Novel anti-apoptotic mechanism of A20 through targeting ASK1 to suppress TNF-induced JNK activation. Cell Death Differ. 17: 1830-1841.
25. Krikos, A., C. D. Laherty, and V. M. Dixit. 1992. Transcriptional activation of the tumor necrosis factor a-inducible zinc finger protein, A20, is mediated by kB elements. J. Biol. Chem. 267: 17971-17976.
26. Park, S. K., B. G. Sanders, and K. Kline. 2010. Tocotrienols induce apoptosis in breast cancer cell lines via an endoplasmic reticulum stress-dependent increase in extrinsic death receptor signaling. Breast Cancer Res. Treat. 124: 361-375.
27. Gopalan, A., W. Yu, Q. Jiang, Y. Jang, B. G. Sanders, and K. Kline. 2012. Involvement of de novo ceramide synthesis in g-tocopherol and gamma-tocotrienolinduced apoptosis in human breast cancer cells. Mol. Nutr. Food Res. 56: 1803-1811.
28. Deng, J., P. D. Lu, Y. Zhang, D. Scheuner, R. J. Kaufman, N. Sonenberg, H. P. Harding, and D. Ron. 2004. Translational repression mediates activation of nuclear factor kB by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 24: 10161-10168.
29. Jiang, Q., X. Rao, C. Y. Kim, H. Freiser, Q. Zhang, Z. Jiang, and G. Li. 2012. Gamma-tocotrienol induces apoptosis and autophagy in prostate cancer cells by increasing intracellular dihydrosphingosine and dihydroceramide. Int. J. Cancer 130: 685-693.
30. Jiang, Q., J. Wong, H. Fyrst, J. D. Saba, and B. N. Ames. 2004. g-Tocopherol or combinations of vitamin E forms induce cell death in human prostate cancer cells by interrupting sphingolipid synthesis. Proc. Natl. Acad. Sci. USA 101: 17825-17830.
31. Sims, K., C. A. Haynes, S. Kelly, J. C. Allegood, E. Wang, A. Momin, M. Leipelt, D. Reichart, C. K. Glass, M. C. Sullards, and A. H. Merrill, Jr. 2010. Kdo2-lipid A, a TLR4-specific agonist, induces de novo sphingolipid biosynthesis in RAW264.7 macrophages, which is essential for induction of autophagy. J. Biol. Chem. 285: 38568-38579.
32. Gagliostro, V., J. Casas, A. Caretti, J. L. Abad, L. Tagliavacca, R. Ghidoni, G. Fabrias, and P. Signorelli. 2012. Dihydroceramide delays cell cycle G1/S transition via activation of ER stress and induction of autophagy. Int. J. Biochem. Cell Biol. 44: 2135-2143.
33. Fabrias, G., J. Munõz-Olaya, F. Cingolani, P. Signorelli, J. Casas, V. Gagliostro, and R. Ghidoni. 2012. Dihydroceramide desaturase and dihydrosphingolipids: debutant players in the sphingolipid arena. Prog. Lipid Res. 51: 82-94.
34. Traenckner, E. B., S. Wilk, and P. A. Baeuerle. 1994. A proteasome inhibitor prevents activation of NF-kB and stabilizes a newly phosphorylated form of IkBa that is still bound to NF-kB. EMBO J. 13: 5433-5441.
35. Boone, D. L., E. E. Turer, E. G. Lee, R. C. Ahmad, M. T. Wheeler, C. Tsui, P. Hurley, M. Chien, S. Chai, O. Hitotsumatsu, et al. 2004. The ubiquitinmodifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5: 1052-1060.
36. Hammer, G. E., E. E. Turer, K. E. Taylor, C. J. Fang, R. Advincula, S. Oshima, J. Barrera, E. J. Huang, B. Hou, B. A. Malynn, et al. 2011. Expression of A20 by dendritic cells preserves immune homeostasis and prevents colitis and spondyloarthritis. Nat. Immunol. 12: 1184-1193.
37. Lademann, U., T. Kallunki, and M. Jäättelä. 2001. A20 zinc finger protein inhibits TNF-induced apoptosis and stress response early in the signaling cascades and independently of binding to TRAF2 or 14-3-3 proteins. Cell Death Differ. 8: 265-272.
38. Papa, S., F. Zazzeroni, C. G. Pham, C. Bubici, and G. Franzoso. 2004. Linking JNK signaling to NF-kB: a key to survival. J. Cell Sci. 117: 5197-5208.
39. Hannun, Y. A., and L. M. Obeid. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9: 139-150.
40. Rodriguez-Cuenca, S., N. Barbarroja, and A. Vidal-Puig. 2015. Dihydroceramide desaturase 1, the gatekeeper of ceramide induced lipotoxicity. Biochim. Biophys. Acta 1851: 40-50.
41. Kraveka, J. M., L. Li, Z. M. Szulc, J. Bielawski, B. Ogretmen, Y. A. Hannun, L. M. Obeid, and A. Bielawska. 2007. Involvement of dihydroceramide desaturase in cell cycle progression in human neuroblastoma cells. J. Biol. Chem. 282: 16718-16728.
42. Hayakawa, K., N. Hiramatsu, M. Okamura, H. Yamazaki, S. Nakajima, J. Yao, A. W. Paton, J. C. Paton, and M. Kitamura. 2009. Acquisition of anergy to proinflammatory cytokines in nonimmune cells through endoplasmic reticulum stress response: a mechanism for subsidence of inflammation. J. Immunol. 182: 1182-1191.
43. Wang, Y., M. Moreland, J. G. Wagner, B. N. Ames, B. Illek, D. B. Peden, and Q. Jiang. 2012. Vitamin E forms inhibit IL-13/STAT6-induced eotaxin-3 secretion by up-regulation of PAR4, an endogenous inhibitor of atypical PKC in human lung epithelial cells. J. Nutr. Biochem. 23: 602-608.
44. Burikhanov, R., Y. Zhao, A. Goswami, S. Qiu, S. R. Schwarze, and V. M. Rangnekar. 2009. The tumor suppressor Par-4 activates an extrinsic pathway for apoptosis. Cell 138: 377-388.