A combinatorial F box protein directed pathway controls TRAF adaptor stability to regulate inflammation

Nature Immunology

Volumn 14, Issue 5, 2013, Pages 470-479

  Chen, Bill B ^a   Coon, Tiffany A ^a   Glasser, Jennifer R ^a   McVerry, Bryan J ^a   Zhao, Jing ^a   Zhao, Yutong ^a   Zou, Chunbin ^a   Ellis, Bryon ^a   Sciurba, Frank C ^a   Zhang, Yingze ^a   Mallampalli, Rama K ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; BC 1215; F BOX PROTEIN; FBXL2; PROTEIN INHIBITOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE SEVERITY; DNA POLYMORPHISM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; MOLECULAR INTERACTION; MOLECULAR STABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; SEPSIS; UBIQUITINATION;

ANIMALS; CECUM; CELL LINE; CYTOKINES; DISEASE MODELS, ANIMAL; F-BOX MOTIFS; F-BOX PROTEINS; HUMANS; IMMUNOMODULATION; INFLAMMATION; MICE; MICE, INBRED C57BL; POLYMORPHISM, GENETIC; PROTEIN STABILITY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RNA, SMALL INTERFERING; SEPSIS; TRANSGENES; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS;

EID: 84876667044     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2565     Document Type: Article

References (43)

1. Inoue, J. et al. Tumor necrosis factor receptor-associated factor (TRAF) family: adaptor proteins that mediate cytokine signaling. Exp. Cell Res. 254, 14-24 (2000).
2. Xu, L.G., Li, L.Y. & Shu, H.B. TRAF7 potentiates MEKK3-induced AP1 and CHOP activation and induces apoptosis. J. Biol. Chem. 279, 17278-17282 (2004).
3. Alvarez, S.E. et al. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465, 1084-1088 (2010).
4. London, N.R. et al. Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and infuenza. Sci. Transl. Med. 2, 23ra19 (2010).
5. Harrison, C. Sepsis: calming the cytokine storm. Nat. Rev. Drug Discov. 9, 360-361 (2010).
6. Lutgens, E. et al. Defcient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinfammatory profle. J. Exp. Med. 207, 391-404 (2010).
7. Zhu, L.J. et al. Suppression of tumor necrosis factor receptor associated factor (TRAF)-2 attenuates the proinfammatory and proliferative effect of aggregated IgG on rat renal mesangial cells. Cytokine 49, 201-208 (2010).
8. Yamashita, M. et al. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol. Cell 31, 918-924 (2008).
9. Lamothe, B. et al. The RING domain and frst zinc fnger of TRAF6 coordinate signaling by interleukin-1, lipopolysaccharide, and RANKL. J. Biol. Chem. 283, 24871-24880 (2008).
10. Ha, H., Han, D. & Choi, Y. TRAF-mediated TNFR-family signaling. Curr. Protoc. Immunol. 11, Unit 11 9D (2009).
11. Tanaka, Y. et al. c-Cbl-dependent monoubiquitination and lysosomal degradation of gp130. Mol. Cell Biol. 28, 4805-4818 (2008).
12. Hochstrasser, M. Biochemistry. All in the ubiquitin family. Science 289, 563-564 (2000).
13. Tyers, M. & Willems, A.R. One ring to rule a superfamily of E3 ubiquitin ligases. Science 284, 603-604 (1999).
14. Zheng, N. et al. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416, 703-709 (2002).
15. Cardozo, T. & Pagano, M. The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751 (2004).
16. Jin, J. et al. Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev. 18, 2573-2580 (2004).
17. Cenciarelli, C. et al. Identifcation of a family of human F-box proteins. Curr. Biol. 9, 1177-1179 (1999).
18. Chen, B.B., Coon, T.A., Glasser, J.R. & Mallampalli, R.K. Calmodulin antagonizes a calcium-activated SCF ubiquitin E3 ligase subunit, FBXL2, to regulate surfactant homeostasis. Mol. Cell Biol. 31, 1905-1920 (2011).
19. Chen, B.B. et al. F box protein FBXL2 targets cyclin D2 for ubiquitination and degradation to inhibit leukemic cell proliferation. Blood 119, 3132-3141 (2012).
20. Chen, B.B., Glasser, J.R., Coon, T.A. & Mallampalli, R.K. F-box protein FBXL2 exerts human lung tumor suppressor-like activity by ubiquitin-mediated degradation of cyclin D3 resulting in cell cycle arrest. Oncogene 31, 2566-2579 (2012).
21. Chen, B.B., Glasser, J.R., Coon, T.A. & Mallampalli, R.K. FBXL2 is a ubiquitin E3 ligase subunit that triggers mitotic arrest. Cell Cycle 10, 3487-3494 (2011).
22. Shima, Y. et al. PML activates transcription by protecting HIPK2 and p300 from SCFFbx3-mediated degradation. Mol. Cell Biol. 28, 7126-7138 (2008).
23. Levy, M.M. et al. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Defnitions Conference. Crit. Care Med. 31, 1250-1256 (2003).
24. Hildebrand, J.M. et al. Roles of tumor necrosis factor receptor associated factor 3 (TRAF3) and TRAF5 in immune cell functions. Immunol. Rev. 244, 55-74 (2011).
25. Ishida, T.K. et al. TRAF5, a novel tumor necrosis factor receptor-associated factor family protein, mediates CD40 signaling. Proc. Natl. Acad. Sci. USA 93, 9437-9442 (1996).
26. Vallabhapurapu, S. et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat. Immunol. 9, 1364-1370 (2008).
27. Tseng, P.H. et al. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinfammatory cytokines. Nat. Immunol. 11, 70-75 (2010).
28. Xie, P., Stunz, L.L., Larison, K.D., Yang, B. & Bishop, G.A. Tumor necrosis factor receptor-associated factor 3 is a critical regulator of B cell homeostasis in secondary lymphoid organs. Immunity 27, 253-267 (2007).
29. van Eyndhoven, W.G., Gamper, C.J., Cho, E., Mackus, W.J. & Lederman, S. TRAF-3 mRNA splice-deletion variants encode isoforms that induce NF-kappaB activation. Mol. Immunol. 36, 647-658 (1999).
30. Habelhah, H. Emerging complexity of protein ubiquitination in the NF-kappaB pathway. Genes Cancer 1, 735-747 (2010).
31. Li, S. et al. Ubiquitin ligase Smurf1 targets TRAF family proteins for ubiquitination and degradation. Mol. Cell Biochem. 338, 11-17 (2010).
32. Nakhaei, P. et al. The E3 ubiquitin ligase Triad3A negatively regulates the RIG-I/MAVS signaling pathway by targeting TRAF3 for degradation. PLoS Pathog. 5, e1000650 (2009).
33. Skaar, J.R., D'Angiolella, V., Pagan, J.K. & Pagano, M. SnapShot: F Box Proteins II. Cell 137, 1358 (2009).
34. Bashir, T., Dorrello, N.V., Amador, V., Guardavaccaro, D. & Pagano, M. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428, 190-193 (2004).
35. Galan, J.M. & Peter, M. Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism. Proc. Natl. Acad. Sci. USA 96, 9124-9129 (1999).
36. Chin, K.H. et al. Preparation, crystallization and preliminary X-ray analysis of XC2382, an ApaG protein of unknown structure from Xanthomonas campestris. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 700-702 (2005).
37. Ilyin, G.P., Rialland, M., Pigeon, C. & Guguen-Guillouzo, C. cDNA cloning and expression analysis of new members of the mammalian F-box protein family. Genomics 67, 40-47 (2000).
38. Liu, L., Rodriguez-Belmonte, E.M., Mazloum, N., Xie, B. & Lee, M.Y. Identifcation of a novel protein, PDIP38, that interacts with the p50 subunit of DNA polymerase delta and proliferating cell nuclear antigen. J. Biol. Chem. 278, 10041-10047 (2003).
39. Zhang, J. et al. Novel mutations in ubiquitin-specifc protease 26 gene might cause spermatogenesis impairment and male infertility. Asian J. Androl. 9, 809-814 (2007).
40. Month, S.R. et al. Analysis of 5′ fanking regions of the gamma globin genes from major African haplotype backgrounds associated with sickle cell disease. J. Clin. Invest. 85, 364-370 (1990).
41. Geva, A. et al. Hemoglobin Jamaica plain-a sickling hemoglobin with reduced oxygen affnity. N. Engl. J. Med. 351, 1532-1538 (2004).
42. Dodge, J.A. & Burton, L. Letter: Heterozygote advantage in cystic fbrosis. Lancet 1, 572-573 (1975).
43. Ebong, S.J. et al. Immunopathologic responses to non-lethal sepsis. Shock 12, 118-126 (1999).