SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis (original) (raw)

References

  1. Grabbe, C. & Dikic, I. Functional roles of ubiquitin-like domain (ULD) and ubiquitin-binding domain (UBD) containing proteins. Chem. Rev. 109, 1481–1494 (2009)
    Article CAS Google Scholar
  2. Seymour, R. E. et al. Spontaneous mutations in the mouse Sharpin gene result in multiorgan inflammation, immune system dysregulation and dermatitis. Genes Immun. 8, 416–421 (2007)
    Article CAS Google Scholar
  3. Hayden, M. S. & Ghosh, S. Shared principles in NF-κB signaling. Cell 132, 344–362 (2008)
    Article CAS Google Scholar
  4. Wertz, I. E. & Dixit, V. M. Ubiquitin-mediated regulation of TNFR1 signaling. Cytokine Growth Factor Rev. 19, 313–324 (2008)
    Article CAS Google Scholar
  5. Ikeda, F. & Dikic, I. Atypical ubiquitin chains: new molecular signals. Review series ‘Protein modifications: beyond the usual suspects’. EMBO Rep. 9, 536–542 (2008)
    Article CAS Google Scholar
  6. Iwai, K. & Tokunaga, F. Linear polyubiquitination: a new regulator of NF-κΒ activation. EMBO Rep. 10, 706–713 (2009)
    Article CAS Google Scholar
  7. Pasparakis, M. Regulation of tissue homeostasis by NF-κB signalling: implications for inflammatory diseases. Nature Rev. Immunol. 9, 778–788 (2009)
    Article CAS Google Scholar
  8. Vallabhapurapu, S. & Karin, M. Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693–733 (2009)
    Article CAS Google Scholar
  9. Kirisako, T. et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25, 4877–4887 (2006)
    Article CAS Google Scholar
  10. Lim, S. et al. Sharpin, a novel postsynaptic density protein that directly interacts with the shank family of proteins. Mol. Cell. Neurosci. 17, 385–397 (2001)
    Article CAS Google Scholar
  11. Rahighi, S. et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation. Cell 136, 1098–1109 (2009)
    Article CAS Google Scholar
  12. Wagner, S. et al. Ubiquitin binding mediates the NF-κB inhibitory potential of ABIN proteins. Oncogene 27, 3739–3745 (2008)
    Article CAS Google Scholar
  13. Haas, T. L. et al. Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol. Cell 36, 831–844 (2009)
    Article CAS Google Scholar
  14. Tokunaga, F. et al. Involvement of linear polyubiquitylation of NEMO in NF-κB activation. Nature Cell Biol. 11, 123–132 (2009)
    Article CAS Google Scholar
  15. Gijbels, M. J. J., HogenEsch, H., Blauw, B., Roholl, P. & Zurcher, C. Ultrastructure of epidermis of mice with chronic proliferative dermatitis. Ultrastruct. Pathol. 19, 107–111 (1995)
    Article CAS Google Scholar
  16. Micheau, O. & Tschopp, J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181–190 (2003)
    Article CAS Google Scholar
  17. Wilson, N. S., Dixit, V. & Ashkenazi, A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nature Immunol. 10, 348–355 (2009)
    Article CAS Google Scholar
  18. Dynek, J. N. et al. c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J. 29, 4198–4209 (2010)
    Article CAS Google Scholar
  19. Ikeda, F., Crosetto, N. & Dikic, I. What determines the specificity and outcomes of ubiquitin signaling? Cell 143, 677–681 (2010)
    Article CAS Google Scholar
  20. Pickart, C. M. & Raasi, S. Controlled synthesis of polyubiquitin chains. Methods Enzymol. 399, 21–36 (2005)
    Article CAS Google Scholar
  21. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. & Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nature Protocols 1, 2856–2860 (2007)
    Article Google Scholar
  22. Nielsen, M. L. et al. Iodoacetamide-induced artifact mimics ubiquitination in mass spectrometry. Nature Methods 5, 459–460 (2008)
    Article CAS Google Scholar
  23. Ishihama, Y., Rappsilber, J. & Mann, M. Modular stop and go extraction tips with stacked disks for parallel and multidimensional peptide fractionation in proteomics. J. Proteome Res. 5, 988–994 (2006)
    Article CAS Google Scholar
  24. Borchert, N. et al. Proteogenomics of Pristionchus pacificus reveals distinct proteome structure of nematode models. Genome Res. 20, 837–846 (2010)
    Article CAS Google Scholar
  25. Olsen, J. V. et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010–2021 (2005)
    Article CAS Google Scholar
  26. Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnol. 26, 1367–1372 (2008)
    Article CAS Google Scholar
  27. Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nature Protocols 2, 1896–1906 (2007)
    Article CAS Google Scholar

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Acknowledgements

We thank E. Kim, K. Rajalingham and H.-J. Kreienkampfor reagents used in this study, I. Matic for initial MS analysis of HOIP/HOIL-1L samples, S. Wahl for sample preparation, and V. Dötsch and members of the Dikic lab for discussions and comments. This work was supported by grants from the Deutsche Forschungsgemeinschaft (DI 931/3-1), the Cluster of Excellence “Macromolecular Complexes” of the Goethe University Frankfurt (EXC115) to I.D., Landesstiftung Baden-Württemberg to B.M., the Medical Research Council UK to K.R. and B.S., JSPS Postdoctoral Fellowships for Research Abroad to F.I., EMBO long-term fellowship to S.S.S. and The National Institutes of Health (AR049288 to J.P.S.). V.N. was supported by the Unity Through Knowledge Fund, 3B Grant. C.G. acknowledges support from The International Human Frontier Science Program Organization.

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Author notes

  1. Yonathan Lissanu Deribe and Sigrid S. Skånland: These authors contributed equally to this work.

Authors and Affiliations

  1. Frankfurt Institute for Molecular Life Sciences and Institute of Biochemistry II, Goethe University School of Medicine, Theodor-Stern-Kai 7, D-60590 Frankfurt (Main), Germany,
    Fumiyo Ikeda, Yonathan Lissanu Deribe, Sigrid S. Skånland, Caroline Grabbe, Sjoerd J. L. van Wijk, Panchali Goswami & Ivan Dikic
  2. MRC-National Institute for Medical Research, The Ridgeway, London NW7 1AA, UK,
    Benjamin Stieglitz & Katrin Rittinger
  3. Department of Molecular Biology, Umeå University, Building 6L, 901 87 Umeå, Sweden,
    Caroline Grabbe
  4. Proteome Center Tübingen, Interfaculty Institute for Cell Biology, University of Tübingen, Auf der Morgenstelle 15, 72076 Tübingen, Germany,
    Mirita Franz-Wachtel & Boris Macek
  5. IMBA-Institute of Molecular Biotechnology of the Austrian Academy of Sciences, Dr. Bohrgasse 3, 1030 Vienna, Austria,
    Vanja Nagy
  6. School of Medicine, University of Split, Soltanska 2, Split, HR-21000, Croatia,
    Janos Terzic & Ivan Dikic
  7. Department of Biophysics and Biochemistry, Graduate School of Medicine, Osaka University, Suita, Osaka 565-0871, Japan,
    Fuminori Tokunaga, Tomoko Nakagawa & Kazuhiro Iwai
  8. Institute for Genetics, Centre for Molecular Medicine (CMMC), and Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Zülpicher Str. 47a, 50674 Cologne, Germany,
    Ariadne Androulidaki & Manolis Pasparakis
  9. Cell Biology and Metabolism Group, Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka 565-0871, Japan,
    Kazuhiro Iwai
  10. The Jackson Laboratory, Bar Harbor, 04609, Maine, USA
    John P. Sundberg
  11. Division Nephropharmakologie, Allgemeine Pharmakologie und Toxikologie, Klinikum der Goethe Universität, Theodor-Stern Kai 7, 60590 Frankfurt, Germany,
    Liliana Schaefer

Authors

  1. Fumiyo Ikeda
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  2. Yonathan Lissanu Deribe
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  3. Sigrid S. Skånland
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  4. Benjamin Stieglitz
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  5. Caroline Grabbe
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  6. Mirita Franz-Wachtel
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  7. Sjoerd J. L. van Wijk
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  8. Panchali Goswami
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  9. Vanja Nagy
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  10. Janos Terzic
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  11. Fuminori Tokunaga
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  12. Ariadne Androulidaki
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  13. Tomoko Nakagawa
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  14. Manolis Pasparakis
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  15. Kazuhiro Iwai
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  16. John P. Sundberg
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  17. Liliana Schaefer
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  18. Katrin Rittinger
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  19. Boris Macek
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  20. Ivan Dikic
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Contributions

F.I., Y.L.D., S.S.S., B.S., C.G., S.J.L.v.W., B.M., V.N., M.F.-W. and P.G. performed the experiments. F.T., A.A. and T.N. contributed with reagents used throughout the study. F.I., Y.L.D., S.S.S., C.G., M.P., J.T., K.I., J.P.S., L.F., B.M. and K.R. contributed to the project by co-ordination of experimental work and writing the manuscript. I.D. provided ideas, co-ordinated the entire project and wrote the manuscript.

Corresponding author

Correspondence toIvan Dikic.

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The authors declare no competing financial interests.

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Ikeda, F., Deribe, Y., Skånland, S. et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis.Nature 471, 637–641 (2011). https://doi.org/10.1038/nature09814

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