Regulation of inflammatory response by 3-methyladenine involves the coordinative actions on akt and glycogen synthase kinase 3β rather than autophagy

Journal of Immunology

Volumn 189, Issue 8, 2012, Pages 4154-4164

  Lin, Yi Chieh ^a   Kuo, Hsuan Cheng ^a   Wang, Jang Shiun ^a   Lin, Wan Wan ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; AUTOPHAGY PROTEIN 5; BETA INTERFERON; CYCLOOXYGENASE 2; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 12; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; STAT1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; CYTOKINE PRODUCTION; INFLAMMATION; INNATE IMMUNITY; INTERFERON PRODUCTION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ADENINE; ANIMALS; AUTOPHAGY; CELL LINE; GLYCOGEN SYNTHASE KINASE 3; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84867294606     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102739     Document Type: Article

References (59)

1. Kawai, T., and S. Akira. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650.
2. Häcker, H., P. H. Tseng, and M. Karin. 2011. Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat. Rev. Immunol. 11: 457-468.
3. Kawai, T., and S. Akira. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
4. Hazeki, K., K. Nigorikawa, and O. Hazeki. 2007. Role of phosphoinositide 3-kinase in innate immunity. Biol. Pharm. Bull. 30: 1617-1623.
5. Guha, M., and N. Mackman. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277: 32124-32132.
6. Luyendyk, J. P., G. A. Schabbauer, M. Tencati, T. Holscher, R. Pawlinski, and N. Mackman. 2008. Genetic analysis of the role of the PI3K-Akt pathway in lipopolysaccharide-induced cytokine and tissue factor gene expression in monocytes/macrophages. J. Immunol. 180: 4218-4226.
7. Androulidaki, A., D. Iliopoulos, A. Arranz, C. Doxaki, S. Schworer, V. Zacharioudaki, A. N. Margioris, P. N. Tsichlis, and C. Tsatsanis. 2009. The kinase Akt1 controls macrophage response to lipopolysaccharide by regulating microRNAs. Immunity 31: 220-231.
8. Steinbrecher, K. A., W. Wilson, III, P. C. Cogswell, and A. S. Baldwin. 2005. Glycogen synthase kinase 3beta functions to specify gene-specific, NF-kappaB-dependent transcription. Mol. Cell. Biol. 25: 8444-8455.
9. Woodgett, J. R., and P. S. Ohashi. 2005. GSK3: an in-Toll-erant protein kinase? Nat. Immunol. 6: 751-752.
10. Zhao, L., J. Y. Lee, and D. H. Hwang. 2008. The phosphatidylinositol 3-kinase/Akt pathway negatively regulates Nod2-mediated NF-kappaB pathway. Biochem. Pharmacol. 75: 1515-1525.
11. Arbibe, L., J. P. Mira, N. Teusch, L. Kline, M. Guha, N. Mackman, P. J. Godowski, R. J. Ulevitch, and U. G. Knaus. 2000. Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. Nat. Immunol. 1: 533-540.
12. Madrid, L. V., M. W. Mayo, J. Y. Reuther, and A. S. Baldwin, Jr. 2001. Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38. J. Biol. Chem. 276: 18934-18940.
13. Thomas, K. W., M. M. Monick, J. M. Staber, T. Yarovinsky, A. B. Carter, and G. W. Hunninghake. 2002. Respiratory syncytial virus inhibits apoptosis and induces NF-kappa B activity through a phosphatidylinositol 3-kinase-dependent pathway. J. Biol. Chem. 277: 492-501.
14. Pengal, R.A., L. P. Ganesan, G. Wei, H. Fang, M. C. Ostrowski, and S. Tridandapani. 2006. Lipopolysaccharide-induced production of interleukin-10 is promoted by the serine/threonine kinase Akt. Mol. Immunol. 43: 1557-1564.
15. Joung, S. M., Z. Y. Park, S. Rani, O. Takeuchi, S. Akira, and J. Y. Lee. 2011. Akt contributes to activation of the TRIF-dependent signaling pathways of TLRs by interacting with TANK-binding kinase 1. J. Immunol. 186: 499-507.
16. Kim, A. H., G. Khursigara, X. Sun, T. F. Franke, and M. V. Chao. 2001. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol. Cell. Biol. 21: 893-901.
17. Levine, B., and G. Kroemer. 2008. Autophagy in the pathogenesis of disease. Cell 132: 27-42.
18. Münz, C. 2009. Enhancing immunity through autophagy. Annu. Rev. Immunol. 27: 423-449.
19. Levine, B., and V. Deretic. 2007. Unveiling the roles of autophagy in innate and adaptive immunity. Nat. Rev. Immunol. 7: 767-777.
20. Schmid, D., and C. Münz. 2007. Innate and adaptive immunity through autophagy. Immunity 27: 11-21.
21. Orvedahl, A., and B. Levine. 2009. Eating the enemy within: autophagy in infectious diseases. Cell Death Differ. 16: 57-69.
22. Shi, C. S., and J. H. Kehrl. 2008. MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J. Biol. Chem. 283: 33175-33182.
23. Delgado, M. A., R. A. Elmaoued, A. S. Davis, G. Kyei, and V. Deretic. 2008. Toll-like receptors control autophagy. EMBO J. 27: 1110-1121.
24. Lee, H. K., J. M. Lund, B. Ramanathan, N. Mizushima, and A. Iwasaki. 2007. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315: 1398-1401.
25. Cadwell, K., J. Y. Liu, S. L. Brown, H. Miyoshi, J. Loh, J. K. Lennerz, C. Kishi, W. Kc, J. A. Carrero, S. Hunt, et al. 2008. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456: 259-263.
26. Jounai, N., F. Takeshita, K. Kobiyama, A. Sawano, A. Miyawaki, K. Q. Xin, K. J. Ishii, T. Kawai, S. Akira, K. Suzuki, and K. Okuda. 2007. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. USA 104: 14050-14055.
27. Saitoh, T., N. Fujita, M. H. Jang, S. Uematsu, B. G. Yang, T. Satoh, H. Omori, T. Noda, N. Yamamoto, M. Komatsu, et al. 2008. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456: 264-268.
28. Seglen, P. O., and P. B. Gordon. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA 79: 1889-1892.
29. Blommaart, E. F., U. Krause, J. P. Schellens, H. Vreeling- Sindelárová, and A. J. Meijer. 1997. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243: 240-246.
30. Mizushima, N., A. Yamamoto, M. Hatano, Y. Kobayashi, Y. Kabeya, K. Suzuki, T. Tokuhisa, Y. Ohsumi, and T. Yoshimori. 2001. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152: 657-668.
31. Ito, S., N. Koshikawa, S. Mochizuki, and K. Takenaga. 2007. 3-Methyladenine suppresses cell migration and invasion of HT1080 fibrosarcoma cells through inhibiting phosphoinositide 3-kinases independently of autophagy inhibition. Int. J. Oncol. 31: 261-268.
32. Wu, Y. T., H. L. Tan, G. Shui, C. Bauvy, Q. Huang, M. R. Wenk, C. N. Ong, P. Codogno, and H. M. Shen. 2010. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J. Biol. Chem. 285: 10850-10861.
33. Kim, S., H. Takahashi, W. W. Lin, P. Descargues, S. Grivennikov, Y. Kim, J. L. Luo, and M. Karin. 2009. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457: 102-106.
34. Chen, J. C., M. L. Wu, K. C. Huang, and W. W. Lin. 2008. HMG-CoA reductase inhibitors activate the unfolded protein response and induce cytoprotective GRP78 expression. Cardiovasc. Res. 80: 138-150.
35. Kimura, S., T. Noda, and T. Yoshimori. 2007. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3: 452-460.
36. Li, G., C. D'Souza-Schorey,M. A. Barbieri, R. L. Roberts, A. Klippel, L. T.Williams, and P. D. Stahl. 1995. Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc. Natl. Acad. Sci. USA 92: 10207-10211.
37. Wang, Q. M., C. J. Fiol, A. A. DePaoli-Roach, and P. J. Roach. 1994. Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 269: 14566-14574.
38. Morton, S., R. J. Davis, A. McLaren, and P. Cohen. 2003. A reinvestigation of the multisite phosphorylation of the transcription factor c-Jun. EMBO J. 22: 3876-3886.
39. Zhang, F., C. J. Phiel, L. Spece, N. Gurvich, and P. S. Klein. 2003. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J. Biol. Chem. 278: 33067-33077.
40. Cohen, P., and S. Frame. 2001. The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2: 769-776.
41. Tolkovsky, A. M., L. Xue, G. C. Fletcher, and V. Borutaite. 2002. Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease? Biochimie 84: 233-240.
42. Mizushima, N., T. Yoshimori, and B. Levine. 2010. Methods in mammalian autophagy research. Cell 140: 313-326.
43. Petiot, A., E. Ogier-Denis, E. F. Blommaart, A. J. Meijer, and P. Codogno. 2000. Distinct classes of phosphatidylinositol 39-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275: 992-998.
44. Aksoy, E., W. Vanden Berghe, S. Detienne, Z. Amraoui, K. A. Fitzgerald, G. Haegeman, M. Goldman, and F. Willems. 2005. Inhibition of phosphoinositide 3-kinase enhances TRIF-dependent NF-kappa B activation and IFN-beta synthesis downstream of Toll-like receptor 3 and 4. Eur. J. Immunol. 35: 2200-2209.
45. Park, S. J., S. C. Lee, S. H. Hong, and H. M. Kim. 2002. Degradation of IkappaBalpha in activated RAW264.7 cells is blocked by the phosphatidylinositol 3-kinase inhibitor LY294002. Cell Biol. Toxicol. 18: 121-130.
46. Sato, S., H. Sanjo, K. Takeda, J. Ninomiya-Tsuji, M. Yamamoto, T. Kawai, K. Matsumoto, O. Takeuchi, and S. Akira. 2005. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6: 1087-1095.
47. Tseng, P. H., A. Matsuzawa, W. Zhang, T. Mino, D. A. Vignali, and M. Karin. 2010. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat. Immunol. 11: 70-75.
48. Fukao, T., and S. Koyasu. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24: 358-363.
49. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6: 777-784.
50. Wang, H., J. Brown, and M. Martin. 2011. Glycogen synthase kinase 3: a point of convergence for the host inflammatory response. Cytokine 53: 130-140.
51. Trinchieri, G. 2010. Type I interferon: friend or foe? J. Exp. Med. 207: 2053-2063.
52. Wang, H., C. A. Garcia, K. Rehani, C. Cekic, P. Alard, D. F. Kinane, T. Mitchell, and M. Martin. 2008. IFN-beta production by TLR4-stimulated innate immune cells is negatively regulated by GSK3-beta. J. Immunol. 181: 6797-6802.
53. Weichhart, T., G. Costantino, M. Poglitsch, M. Rosner, M. Zeyda, K. M. Stuhlmeier, T. Kolbe, T. M. Stulnig, W. H. Hörl, M. Hengstschläger, et al. 2008. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29: 565-577.
54. Yu, H., D. Pardoll, and R. Jove. 2009. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 9: 798-809.
55. Blander, J. M., and R. Medzhitov. 2004. Regulation of phagosome maturation by signals from toll-like receptors. Science 304: 1014-1018.
56. Xu, Y., C. Jagannath, X. D. Liu, A. Sharafkhaneh, K. E. Kolodziejska, and N. T. Eissa. 2007. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 27: 135-144.
57. Fésüs, L., M. A. Demény, and G. Petrovski. 2011. Autophagy shapes inflammation. Antioxid. Redox Signal. 14: 2233-2243.
58. Levine, B., N. Mizushima, and H. W. Virgin. 2011. Autophagy in immunity and inflammation. Nature 469: 323-335.
59. Saitoh, T., and S. Akira. 2010. Regulation of innate immune responses by autophagy-related proteins. J. Cell Biol. 189: 925-935.