FBXW7α attenuates inflammatory signalling by downregulating C/EBPδ and its target gene Tlr4

Nature Communications

Volumn 4, Issue , 2013, Pages

  Balamurugan, Kuppusamy ^a   Sharan, Shikha ^a   Klarmann, Kimberly D ^b   Zhang, Youhong ^a   Coppola, Vincenzo ^c   Summers, Glenn H ^b   Roger, Thierry ^d   Morrison, Deborah K ^a   Keller, Jonathan R ^b   Sterneck, Esta ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^d LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN DELTA; LIGAND; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR 4;

GENE EXPRESSION; IMMUNE RESPONSE; LIGAND; MAMMAL; POLYSACCHARIDE; PROTEIN; SIGNALING; TUMOR;

ANIMAL CELL; ARTICLE; BREAST TUMOR; CANCER CELL; DOWN REGULATION; GENE DELETION; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; METASTASIS; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN PHOSPHORYLATION; TUMOR SUPPRESSOR GENE;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL LINE, TUMOR; DOWN-REGULATION; F-BOX PROTEINS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION; MICE; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; UBIQUITIN-PROTEIN LIGASES;

EID: 84877724618     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2677     Document Type: Article

References (53)

1. Kawai, T. & Akira, S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650 (2011).
2. Roger, T. et al. Protection from lethal gram-negative bacterial sepsis by targeting Toll-like receptor 4. Proc. Natl Acad. Sci. USA 106, 2348-2352 (2009).
3. Lin, Q., Li, M., Fang, D., Fang, J. & Su, S. B. The essential roles of Toll-like receptor signaling pathways in sterile inflammatory diseases. Int. Immunopharmacol. 11, 1422-1432 (2011).
4. Huang, B. et al. Toll-like receptors on tumor cells facilitate evasion of immune surveillance. Cancer Res. 65, 5009-5014 (2005). (Pubitemid 40827306)
5. Szczepanski, M. J. et al. Triggering of Toll-like receptor 4 expressed on human head and neck squamous cell carcinoma promotes tumor development and protects the tumor from immune attack. Cancer Res. 69, 3105-3113 (2009).
6. Liao, S. J. et al. Triggering of Toll-like receptor 4 on metastatic breast cancer cells promotes alphavbeta3-mediated adhesion and invasive migration. Breast Cancer Res Treat. 133, 853-863 (2012).
7. Yang, H. et al. Reduced expression of Toll-like receptor 4 inhibits human breast cancer cells proliferation and inflammatory cytokines secretion. J. Exp. Clin. Cancer Res. 29, 92 (2010).
8. Zhao, Y. et al. Metadherin mediates lipopolysaccharide-induced migration and invasion of breast cancer cells. PLoS One 6, e29363 (2011).
9. Ramji, D. P. & Foka, P. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365, 561-575 (2002). (Pubitemid 34864439)
10. Litvak, V. et al. Function of C/EBPdelta in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat. Immunol. 10, 437-443 (2009).
11. Slofstra, S. H. et al. Gene expression profiling identifies C/EBPdelta as a candidate regulator of endotoxin-induced disseminated intravascular coagulation. Am. J. Respir. Crit. Care Med. 176, 602-609 (2007). (Pubitemid 47403278)
12. Tsai, V. W. W. et al. Ccaat/enhancer binding protein-delta expression by dendritic cells regulates CNS autoinflammatory disease. J. Neurosci. 31, 17612-17621 (2011).
13. Balamurugan, K. et al. The tumour suppressor C/EBPdelta inhibits FBXW7 expression and promotes mammary tumour metastasis. EMBO J. 29, 4106-4117 (2010).
14. Welcker, M. & Clurman, B. E. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 8, 83-93 (2008). (Pubitemid 351161321)
15. Cheng, Y. & Li, G. Role of the ubiquitin ligase Fbw7 in cancer progression. Cancer Metastasis Rev. 31, 75-87 (2012).
16. Semenza, G. L. HIF-1: upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev. 20, 51-56 (2010).
17. Wong, C. C. et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc. Natl Acad. Sci. USA 108, 16369-16374 (2011).
18. Lu, X. & Kang, Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin. Cancer Res. 16, 5928-5935 (2010).
19. Guy, C. T. et al. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl Acad. Sci. USA 89, 10578-10582 (1992).
20. Pawar, S. A. et al. C/EBPdelta targets cyclin D1 for proteasome-mediated degradation via induction of CDC27/APC3 expression. Proc. Natl Acad. Sci. USA 107, 9210-9215 (2010).
21. Sarkar, T. R. et al. Identification of a Src tyrosine kinase/SIAH2 E3 ubiquitin ligase pathway that regulates C/EBPdelta expression and contributes to transformation of breast tumor cells. Mol. Cell Biol. 32, 320-332 (2012).
22. Cramer, T. et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112, 645-657 (2003). (Pubitemid 36331777)
23. Outtz, H. H., Wu, J. K., Wang, X. & Kitajewski, J. Notch1 deficiency results in decreased inflammation during wound healing and regulates vascular endothelial growth factor receptor-1 and inflammatory cytokine expression in macrophages. J. Immunol. 185, 4363-4373 (2010).
24. Frede, S., Stockmann, C., Freitag, P. & Fandrey, J. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-kappaB. Biochem J. 396, 517-527 (2006). (Pubitemid 44228166)
25. Mao, J. H. et al. FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression. Science 321, 1499-1502 (2008).
26. Martin, M., Rehani, K., Jope, R. S. & Michalek, S. M. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6, 777-784 (2005). (Pubitemid 43090463)
27. Wang, H. et al. IFN-beta production by TLR4-stimulated innate immune cells is negatively regulated by GSK3-beta. J. Immunol. 181, 6797-6802 (2008).
28. Marques, J. T. & Williams, B. R. Activation of the mammalian immune system by siRNAs. Nat. Biotechnol. 23, 1399-1405 (2005). (Pubitemid 41679392)
29. Roger, T., David, J., Glauser, M. P. & Calandra, T. MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 414, 920-924 (2001). (Pubitemid 34024744)
30. Won, J. S., Im, Y. B., Key, L., Singh, I. & Singh, A. K. The involvement of glucose metabolism in the regulation of inducible nitric oxide synthase gene expression in glial cells: possible role of glucose-6-phosphate dehydrogenase and CCAAT/enhancing binding protein. J. Neurosci. 23, 7470-7478 (2003). (Pubitemid 37034063)
31. Zhang, Z. & Schluesener, H. J. Mammalian toll-like receptors: from endogenous ligands to tissue regeneration. Cell. Mol. Life Sci. 63, 2901-2907 (2006). (Pubitemid 46072297)
32. Hiratsuka, S. et al. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat. Cell Biol. 10, 1349-1355 (2008).
33. Grivennikov, S. I., Greten, F. R. & Karin, M. Immunity, inflammation, and cancer. Cell 140, 883-899 (2010).
34. Karnoub, A. E. & Weinberg, R. A. Chemokine networks and breast cancer metastasis. Breast Dis. 26, 75-85 (2006). (Pubitemid 46647416)
35. Gonzalez-Martin, A., Gomez, L., Lustgarten, J., Mira, E. & Manes, S. Maximal T cell-mediated antitumor responses rely upon CCR5 expression in both CD4(+) and CD8(+) T cells. Cancer Res. 71, 5455-5466 (2011).
36. Goswami, S. et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res. 65, 5278-5283 (2005). (Pubitemid 40827339)
37. Yan, C., Zhu, M., Staiger, J., Johnson, P. F. & Gao, H. C5a-regulated CCAAT/enhancer binding protein beta and-delta are essential in Fcgamma receptor-mediated inflammatory cytokine and chemokine production in macrophages. J. Biol. Chem. 287, 3217-3230 (2012).
38. Zannetti, C. et al. C/EBP{delta} and STAT-1 are required for TLR8 transcriptional activity. J. Biol. Chem. 285, 34773-34780 (2010).
39. Kravchenko, V. V., Mathison, J. C., Schwamborn, K., Mercurio, F. & Ulevitch, R. J. IKKi/IKKepsilon plays a key role in integrating signals induced by pro-inflammatory stimuli. J. Biol. Chem. 278, 26612-26619 (2003). (Pubitemid 36876806)
40. Lu, Y. C. et al. Differential role for c-Rel and C/EBPbeta/delta in TLR-mediated induction of proinflammatory cytokines. J. Immunol. 182, 7212-7221 (2009).
41. Maitra, U., Gan, L., Chang, S. & Li, L. Low-Dose Endotoxin Induces Inflammation by Selectively Removing Nuclear Receptors and Activating CCAAT/Enhancer-Binding Protein {delta}. J. Immunol. 186, 4467-4473 (2011).
42. Min, Y. et al. C/EBP-delta regulates VEGF-C autocrine signaling in lymphangiogenesis and metastasis of lung cancer through HIF-1alpha. Oncogene 30, 4901-4909 (2011).
43. Corzo, C. A. et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207, 2439-2453 (2010).
44. Imtiyaz, H. Z. & Simon, M. C. Hypoxia-inducible factors as essential regulators of inflammation. Curr. Top Microbiol. Immunol. 345, 105-120 (2010).
45. Gonzalez-Reyes, S. et al. Study of TLR3, TLR4 and TLR9 in breast carcinomas and their association with metastasis. BMC Cancer 10, 665 (2010).
46. Ahmed, A., Wang, J. H. & Redmond, H. P. Silencing of TLR4 Increases Tumor Progression and Lung Metastasis in a Murine Model of Breast Cancer. Ann. Surg. Oncol. e-pub ahead of print (2012).
47. Etokebe, G. E. et al. Single-nucleotide polymorphisms in genes encoding tolllike receptor-2,-3,-4, and-9 in case-control study with breast cancer. Genet. Test Mol. Biomarkers 13, 729-734 (2009).
48. Apetoh, L., Tesniere, A., Ghiringhelli, F., Kroemer, G. & Zitvogel, L. Molecular interactions between dying tumor cells and the innate immune system determine the efficacy of conventional anticancer therapies. Cancer Res. 68, 4026-4030 (2008).
49. Sterneck, E. et al. Selectively enhanced contextual fear conditioning in mice lacking the transcriptional regulator CCAAT/enhancer binding protein delta. Proc. Natl Acad. Sci. USA 95, 10908-10913 (1998). (Pubitemid 28413167)
50. Hoover, D. L. & Nacy, C. A. Macrophage activation to kill Leishmania tropica: defective intracellular killing of amastigotes by macrophages elicited with sterile inflammatory agents. J. Immunol. 132, 1487-1493 (1984). (Pubitemid 14156070)
51. van Drogen, F. et al. Ubiquitylation of cyclin E requires the sequential function of SCF complexes containing distinct hCdc4 isoforms. Mol. Cell 23, 37-48 (2006).
52. Morrison, D. K., Heidecker, G., Rapp, U. R. & Copeland, T. D. Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268, 17309-17316 (1993). (Pubitemid 23236968)
53. Roger, T. et al. Critical role for Ets, AP-1 and GATA-like transcription factors in regulating mouse Toll-like receptor 4 (Tlr4) gene expression. Biochem. J. 387, 355-365 (2005). (Pubitemid 40571221)