Innate immune-directed NF-κB signaling requires site-specific NEMO ubiquitination

Cell Reports

Volumn 4, Issue 2, 2013, Pages 352-361

  Jun, Janice C ^a   Kertesy, Sylvia ^a   Jones, Mark B ^a   Marinis, Jill M ^a,b   Cobb, Brian A ^a   Tigno Aranjuez, Justine T ^a   Abbott, Derek W ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DERMATITIS; EMBRYO; EMBRYO DEATH; FATTY LIVER; FEMALE; HETEROZYGOTE; IN VIVO STUDY; INNATE IMMUNITY; MALE; MOUSE; NEMO GENE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPLENOMEGALY; UBIQUITINATION;

MUS;

ANIMALS; FEMALE; GENE KNOCK-IN TECHNIQUES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84880794284     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.06.036     Document Type: Article

References (35)

1. Abbott D.W., Wilkins A., Asara J.M., Cantley L.C. The Crohn's disease gene, NOD2, requires RIP2 in order to induce ubiquitinylation of a novel site on NEMO. Curr. Biol. 2004, 14:2217-2227.
2. Abbott D.W., Yang Y., Hutti J.E., Madhavarapu S., Kelliher M.A., Cantley L.C. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol. Cell. Biol. 2007, 27:6012-6025.
3. Belgnaoui S.M., Paz S., Samuel S., Goulet M.L., Sun Q., Kikkert M., Iwai K., Dikic I., Hiscott J., Lin R. Linear ubiquitination of NEMO negatively regulates the interferon antiviral response through disruption of the MAVS-TRAF3 complex. Cell Host Microbe 2012, 12:211-222.
4. Beraza N., Lüdde T., Assmus U., Roskams T., Vander Borght S., Trautwein C. Hepatocyte-specific IKK gamma/NEMO expression determines the degree of liver injury. Gastroenterology 2007, 132:2504-2517.
5. Beraza N., Malato Y., Sander L.E., Al-Masaoudi M., Freimuth J., Riethmacher D., Gores G.J., Roskams T., Liedtke C., Trautwein C. Hepatocyte-specific NEMO deletion promotes NK/NKT cell- and TRAIL-dependent liver damage. J.Exp. Med. 2009, 206:1727-1737.
6. Chen Z.J. Ubiquitination in signaling to and activation of IKK. Immunol. Rev. 2012, 246:95-106.
7. Chen G., Shaw M.H., Kim Y.G., Nuñez G. NOD-like receptors: role in innate immunity and inflammatory disease. Annu. Rev. Pathol. 2009, 4:365-398.
8. Cordier F., Grubisha O., Traincard F., Véron M., Delepierre M., Agou F. The zinc finger of NEMO is a functional ubiquitin-binding domain. J.Biol. Chem. 2009, 284:2902-2907.
9. Derudder E., Cadera E.J., Vahl J.C., Wang J., Fox C.J., Zha S., van Loo G., Pasparakis M., Schlissel M.S., Schmidt-Supprian M., Rajewsky K. Development of immunoglobulin lambda-chain-positive B cells, but not editing of immunoglobulin kappa-chain, depends on NF-kappaB signals. Nat. Immunol. 2009, 10:647-654.
10. Girardin S.E., Boneca I.G., Viala J., Chamaillard M., Labigne A., Thomas G., Philpott D.J., Sansonetti P.J. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J.Biol. Chem. 2003, 278:8869-8872.
11. Hadian K., Griesbach R.A., Dornauer S., Wanger T.M., Nagel D., Metlitzky M., Beisker W., Schmidt-Supprian M., Krappmann D. NF-κB essential modulator (NEMO) interaction with linear and lys-63 ubiquitin chains contributes to NF-κB activation. J.Biol. Chem. 2011, 286:26107-26117.
12. Hayden M.S., Ghosh S. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 2012, 26:203-234.
13. Hinz M., Stilmann M., Arslan S.C., Khanna K.K., Dittmar G., Scheidereit C. A cytoplasmic ATM-TRAF6-cIAP1 module links nuclear DNA damage signaling to ubiquitin-mediated NF-κB activation. Mol. Cell 2010, 40:63-74.
14. Ikeda F., Rahighi S., Wakatsuki S., Dikic I. Selective binding of linear ubiquitin chains to NEMO in NF-kappaB activation. Adv. Exp. Med. Biol. 2011, 691:107-114.
15. Inohara N., Ogura Y., Fontalba A., Gutierrez O., Pons F., Crespo J., Fukase K., Inamura S., Kusumoto S., Hashimoto M., et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J.Biol. Chem. 2003, 278:5509-5512.
16. Kensche T., Tokunaga F., Ikeda F., Goto E., Iwai K., Dikic I. Analysis of nuclear factor-κB (NF-κB) essential modulator (NEMO) binding to linear and lysine-linked ubiquitin chains and its role in the activation of NF-κB. J.Biol. Chem. 2012, 287:23626-23634.
17. Kim S., La Motte-Mohs R.N., Rudolph D., Zuniga-Pflucker J.C., Mak T.W. The role of NF-kB essential modulator (NEMO) in B cell development and survival. Proc. Natl. Acad. Sci. USA 2003, 100:1203-1208.
18. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
19. Laplantine E., Fontan E., Chiaravalli J., Lopez T., Lakisic G., Véron M., Agou F., Israël A. NEMO specifically recognizes K63-linked poly-ubiquitin chains through a new bipartite ubiquitin-binding domain. EMBO J. 2009, 28:2885-2895.
20. Lo Y.C., Lin S.C., Rospigliosi C.C., Conze D.B., Wu C.J., Ashwell J.D., Eliezer D., Wu H. Structural basis for recognition of diubiquitins by NEMO. Mol. Cell 2009, 33:602-615.
21. Luedde T., Beraza N., Kotsikoris V., van Loo G., Nenci A., De Vos R., Roskams T., Trautwein C., Pasparakis M. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 2007, 11:119-132.
22. Makris C., Godfrey V.L., Krähn-Senftleben G., Takahashi T., Roberts J.L., Schwarz T., Feng L., Johnson R.S., Karin M. Female mice heterozygous for IKK gamma/NEMO deficiencies develop a dermatopathy similar to the human X-linked disorder incontinentia pigmenti. Mol. Cell 2000, 5:969-979.
23. Nenci A., Huth M., Funteh A., Schmidt-Supprian M., Bloch W., Metzger D., Chambon P., Rajewsky K., Krieg T., Haase I., Pasparakis M. Skin lesion development in a mouse model of incontinentia pigmenti is triggered by NEMO deficiency in epidermal keratinocytes and requires TNF signaling. Hum. Mol. Genet. 2006, 15:531-542.
24. Ni C.Y., Wu Z.H., Florence W.C., Parekh V.V., Arrate M.P., Pierce S., Schweitzer B., Van Kaer L., Joyce S., Miyamoto S., et al. Cutting edge: K63-linked polyubiquitination of NEMO modulates TLR signaling and inflammation invivo. J.Immunol. 2008, 180:7107-7111.
25. Niu J., Shi Y., Iwai K., Wu Z.H. LUBAC regulates NF-κB activation upon genotoxic stress by promoting linear ubiquitination of NEMO. EMBO J. 2011, 30:3741-3753.
26. Rahighi S., Ikeda F., Kawasaki M., Akutsu M., Suzuki N., Kato R., Kensche T., Uejima T., Bloor S., Komander D., et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 2009, 136:1098-1109.
27. Rudolph D., Yeh W.C., Wakeham A., Rudolph B., Nallainathan D., Potter J., Elia A.J., Mak T.W. Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev. 2000, 14:854-862.
28. Schmidt-Supprian M., Bloch W., Courtois G., Addicks K., Israël A., Rajewsky K., Pasparakis M. NEMO/IKK gamma-deficient mice model incontinentia pigmenti. Mol. Cell 2000, 5:981-992.
29. Stark G.R., Darnell J.E. The JAK-STAT pathway at twenty. Immunity 2012, 36:503-514.
30. Tigno-Aranjuez J.T., Asara J.M., Abbott D.W. Inhibition of RIP2's tyrosine kinase activity limits NOD2-driven cytokine responses. Genes Dev. 2010, 24:2666-2677.
31. Tokunaga F., Sakata S., Saeki Y., Satomi Y., Kirisako T., Kamei K., Nakagawa T., Kato M., Murata S., Yamaoka S., et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 2009, 11:123-132.
32. Wu C.J., Conze D.B., Li T., Srinivasula S.M., Ashwell J.D. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat. Cell Biol. 2006, 8:398-406.
33. Yang H.T., Papoutsopoulou S., Belich M., Brender C., Janzen J., Gantke T., Handley M., Ley S.C. Coordinate regulation of TPL-2 and NF-κB signaling in macrophages by NF-κB1 p105. Mol. Cell. Biol. 2012, 32:3438-3451.
34. Zhao T., Yang L., Sun Q., Arguello M., Ballard D.W., Hiscott J., Lin R. The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways. Nat. Immunol. 2007, 8:592-600.
35. Zhou H., Wertz I., O'Rourke K., Ultsch M., Seshagiri S., Eby M., Xiao W., Dixit V.M. Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 2004, 427:167-171.