Site-specific proteasome phosphorylation controls cell proliferation and tumorigenesis (original) (raw)

• Coux, O., Tanaka, K. & Goldberg, A. L. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65, 801–847 (1996).
  CAS PubMed Google Scholar
• Tai, H. C. & Schuman, E. M. Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat. Rev. Neurosci. 9, 826–838 (2008).
  CAS PubMed Google Scholar
• López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M. & Kroemer, G. The hallmarks of aging. Cell 153, 1194–1217 (2013).
  PubMed PubMed Central Google Scholar
• Hoeller, D. & Dikic, I. Targeting the ubiquitin system in cancer therapy. Nature 458, 438–444 (2009).
  CAS PubMed Google Scholar
• Orlowski, R. Z. & Kuhn, D. J. Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 14, 1649–1657 (2008).
  CAS PubMed Google Scholar
• Finley, D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477–513 (2009).
  CAS PubMed PubMed Central Google Scholar
• Bhattacharyya, S., Yu, H., Mim, C. & Matouschek, A. Regulated protein turnover: snapshots of the proteasome in action. Nat. Rev. Mol. Cell Biol. 15, 122–133 (2014).
  CAS PubMed PubMed Central Google Scholar
• Ehlinger, A. & Walters, K. J. Structural insights into proteasome activation by the 19S regulatory particle. Biochemistry 52, 3618–3628 (2013).
  CAS PubMed Google Scholar
• Murata, S., Yashiroda, H. & Tanaka, K. Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 10, 104–115 (2009).
  CAS PubMed Google Scholar
• Schmidt, M. & Finley, D. Regulation of proteasome activity in health and disease. Biochim. Biophys. Acta 1843, 13–25 (2014).
  CAS PubMed Google Scholar
• Radhakrishnan, S. K. et al. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38, 17–28 (2010).
  CAS PubMed PubMed Central Google Scholar
• Tomko, R. J. & Hochstrasser, M. Molecular architecture and assembly of the eukaryotic proteasome. Annu. Rev. Biochem. 82, 415–445 (2013).
  CAS PubMed Google Scholar
• Wang, X. et al. Mass spectrometric characterization of the affinity-purified human 26S proteasome complex. Biochemistry 46, 3553–3565 (2007).
  CAS PubMed Google Scholar
• Wang, X. & Huang, L. Identifying dynamic interactors of protein complexes by quantitative mass spectrometry. Mol. Cell Proteomics 7, 46–57 (2008).
  PubMed Google Scholar
• Hershko, A. Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr. Opin. Cell Biol. 9, 788–799 (1997).
  CAS PubMed Google Scholar
• Teixeira, L. K. & Reed, S. I. Ubiquitin ligases and cell cycle control. Annu. Rev. Biochem. 82, 387–414 (2013).
  CAS PubMed Google Scholar
• Bence, N. F., Sampat, R. M. & Kopito, R. R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552–1555 (2001).
  CAS PubMed Google Scholar
• Min, M. & Lindon, C. Substrate targeting by the ubiquitin–proteasome system in mitosis. Semin. Cell Dev. Biol. 23, 482–491 (2012).
  CAS PubMed Google Scholar
• Dephoure, N. et al. A quantitative atlas of mitotic phosphorylation. Proc. Natl Acad. Sci. USA 105, 10762–10767 (2008).
  CAS PubMed Google Scholar
• Olsen, J. V. et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3 (2010).
  PubMed Google Scholar
• Nagano, K. et al. Phosphoproteomic analysis of distinct tumor cell lines in response to nocodazole treatment. Proteomics 9, 2861–2874 (2009).
  CAS PubMed Google Scholar
• Kettenbach, A. N. et al. Quantitative phosphoproteomics identifies substrates and functional modules of aurora and polo-like kinase activities in mitotic cells. Sci. Signal. 4, rs5 (2011).
  CAS PubMed Google Scholar
• Bian, Y. et al. An enzyme assisted RP-RPLC approach for in-depth analysis of human liver phosphoproteome. J. Proteomics 96, 253–262 (2014).
  CAS PubMed Google Scholar
• Mayya, V. et al. Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein–protein interactions. Sci. Signal. 2, ra46 (2009).
  PubMed Google Scholar
• Kisselev, A. F. & Goldberg, A. L. Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol. 398, 364–378 (2005).
  CAS PubMed Google Scholar
• Besche, H. C. et al. Autoubiquitination of the 26S proteasome on Rpn13 regulates breakdown of ubiquitin conjugates. EMBO J. 33, 1159–1176 (2014).
  CAS PubMed PubMed Central Google Scholar
• Taipale, M. et al. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150, 987–1001 (2012).
  CAS PubMed PubMed Central Google Scholar
• Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912–1934 (2002).
  CAS PubMed Google Scholar
• Djuranovic, S. et al. Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol. Cell 34, 580–590 (2009).
  CAS PubMed Google Scholar
• Beckwith, R., Estrin, E., Worden, E. J. & Martin, A. Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA + unfoldase. Nat. Struct. Mol. Biol. 20, 1164–1172 (2013).
  CAS PubMed PubMed Central Google Scholar
• Liu, C. W. et al. ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome. Mol. Cell 24, 39–50 (2006).
  CAS PubMed PubMed Central Google Scholar
• Smith, D. M. et al. ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol. Cell 20, 687–698 (2005).
  CAS PubMed Google Scholar
• Peth, A., Kukushkin, N., Bosse, M. & Goldberg, A. L. Ubiquitinated proteins activate the proteasomal ATPases by binding to Usp14 or Uch37 homologs. J. Biol. Chem. 288, 7781–7790 (2013).
  CAS PubMed PubMed Central Google Scholar
• Śledź, P. et al. Structure of the 26S proteasome with ATP-γ S bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc. Natl Acad. Sci. USA 110, 7264–7269 (2013).
  PubMed Google Scholar
• Santarius, T., Shipley, J., Brewer, D., Stratton, M. R. & Cooper, C. S. A census of amplified and overexpressed human cancer genes. Nat. Rev. Cancer 10, 59–64 (2010).
  CAS PubMed Google Scholar
• Györffy, B. et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res. Treat. 123, 725–731 (2010).
  PubMed Google Scholar
• Petrocca, F. et al. A genome-wide siRNA screen identifies proteasome addiction as a vulnerability of basal-like triple-negative breast cancer cells. Cancer Cell 24, 182–196 (2013).
  CAS PubMed PubMed Central Google Scholar
• Vilchez, D. et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 489, 304–308 (2012).
  CAS PubMed PubMed Central Google Scholar
• Shabaneh, T. B. et al. Molecular basis of differential sensitivity of myeloma cells to clinically relevant bolus treatment with bortezomib. PLoS ONE 8, e56132 (2013).
  CAS PubMed PubMed Central Google Scholar
• Mason, G. G., Murray, R. Z., Pappin, D. & Rivett, A. J. Phosphorylation of ATPase subunits of the 26S proteasome. FEBS Lett. 430, 269–274 (1998).
  CAS PubMed Google Scholar
• Bose, S., Stratford, F. L., Broadfoot, K. I., Mason, G. G. & Rivett, A. J. Phosphorylation of 20S proteasome alpha subunit C8 (alpha7) stabilizes the 26S proteasome and plays a role in the regulation of proteasome complexes by gamma-interferon. Biochem. J. 378, 177–184 (2004).
  CAS PubMed PubMed Central Google Scholar
• Satoh, K., Sasajima, H., Nyoumura, K.-i., Yokosawa, H. & Sawada, H. Assembly of the 26S proteasome is regulated by phosphorylation of the p45/Rpt6 ATPase subunit. Biochemistry 40, 314–319 (2000).
  Google Scholar
• Feng, Y., Longo, D. L. & Ferris, D. K. Polo-like kinase interacts with proteasomes and regulates their activity. Cell Growth Differ. 12, 29–37 (2001).
  CAS PubMed Google Scholar
• Zhang, F. et al. Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. J. Biol. Chem. 282, 22460–22471 (2007).
  CAS PubMed Google Scholar
• Djakovic, S. N., Schwarz, L. A., Barylko, B., DeMartino, G. N. & Patrick, G. N. Regulation of the proteasome by neuronal activity and calcium/calmodulin-dependent protein kinase II. J. Biol. Chem. 284, 26655–26665 (2009).
  CAS PubMed PubMed Central Google Scholar
• Bingol, B. et al. Autophosphorylated CaMKIIα acts as a scaffold to recruit proteasomes to dendritic spines. Cell 140, 567–578 (2010).
  CAS PubMed Google Scholar
• Djakovic, S. N. et al. Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons. J. Neurosci. 32, 5126–5131 (2012).
  CAS PubMed PubMed Central Google Scholar
• Hamilton, A. M. et al. Activity-dependent growth of new dendritic spines is regulated by the proteasome. Neuron 74, 1023–1030 (2012).
  CAS PubMed PubMed Central Google Scholar
• Ranek, M. J., Terpstra, E. J., Li, J., Kass, D. A. & Wang, X. Protein kinase g positively regulates proteasome-mediated degradation of misfolded proteins. Circulation 128, 365–376 (2013).
  CAS PubMed PubMed Central Google Scholar
• Aranda, S., Laguna, A. & de la Luna, S. DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. FASEB J. 25, 449–462 (2011).
  CAS PubMed Google Scholar
• Becker, W. Emerging role of DYRK family protein kinases as regulators of protein stability in cell cycle control. Cell Cycle 11, 3389–3394 (2012).
  CAS PubMed PubMed Central Google Scholar
• Lander, G. C. et al. Complete subunit architecture of the proteasome regulatory particle. Nature 482, 186–191 (2012).
  CAS PubMed PubMed Central Google Scholar
• da Fonseca, P. C. A., He, J. & Morris, E. P. Molecular model of the human 26S proteasome. Mol. Cell 46, 54–66 (2012).
  PubMed Google Scholar
• Matyskiela, M. E., Lander, G. C. & Martin, A. Conformational switching of the 26S proteasome enables substrate degradation. Nat. Struct. Mol. Biol. 20, 781–788 (2013).
  CAS PubMed PubMed Central Google Scholar
• Miller, C. T. et al. Amplification and overexpression of the dual-specificity tyrosine-(Y)-phosphorylation regulated kinase 2 (DYRK2) gene in esophageal and lung adenocarcinomas. Cancer Res. 63, 4136–4143 (2003).
  CAS PubMed Google Scholar
• Bonifaci, N. et al. Exploring the link between germline and somatic genetic alterations in breast carcinogenesis. PLoS ONE 5, e14078 (2010).
  PubMed PubMed Central Google Scholar
• Gorringe, K. L., Boussioutas, A., Bowtell, D. D. & Melbourne Gastric Cancer Group, P. M. M. A. F. Novel regions of chromosomal amplification at 6p21, 5p13, and 12q14 in gastric cancer identified by array comparative genomic hybridization. Genes Chromosomes Cancer 42, 247–259 (2005).
  CAS PubMed Google Scholar
• Taira, N. et al. DYRK2 priming phosphorylation of c-Jun and c-Myc modulates cell cycle progression in human cancer cells. J. Clin. Invest. 122, 859–872 (2012).
  CAS PubMed PubMed Central Google Scholar
• Guo, X. et al. Axin and GSK3-β control Smad3 protein stability and modulate TGF-β signaling. Genes Dev. 22, 106–120 (2008).
  CAS PubMed PubMed Central Google Scholar
• Inobe, T., Fishbain, S., Prakash, S. & Matouschek, A. Defining the geometry of the two-component proteasome degron. Nat. Chem. Biol. 7, 161167 (2011).
  Google Scholar
• Fishbain, S. et al. Sequence composition of disordered regions fine-tunes protein half-life. Nat. Struct. Mol. Biol. 22, 214221 (2015).
  Google Scholar
• Soundararajan, M. et al. Structures of Down syndrome kinases, DYRKs, reveal mechanisms of kinase activation and substrate recognition. Structure 21, 986–996 (2013).
  CAS PubMed PubMed Central Google Scholar
• Kaake, R. M., Milenković, T., Pržulj, N., Kaiser, P. & Huang, L. Characterization of cell cycle specific protein interaction networks of the yeast 26S proteasome complex by the QTAX strategy. J. Proteome Res. 9, 2016–2029 (2010).
  CAS PubMed PubMed Central Google Scholar
• Ong, S. E. & Mann, M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1, 2650–2660 (2006).
  CAS PubMed Google Scholar
• Guo, X. et al. UBLCP1 is a 26S proteasome phosphatase that regulates nuclear proteasome activity. Proc. Natl Acad. Sci. USA 108, 18649–18654 (2011).
  CAS PubMed Google Scholar
• Smith, D. M., Fraga, H., Reis, C., Kafri, G. & Goldberg, A. L. ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144, 526–538 (2011).
  CAS PubMed PubMed Central Google Scholar
• Jacobson, A. D., MacFadden, A., Wu, Z., Peng, J. & Liu, C.-W. Autoregulation of the 26S proteasome by in situ ubiquitination. Mol. Biol. Cell 25, 1824–1835 (2014).
  PubMed PubMed Central Google Scholar
• Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281–2308 (2013).
  CAS PubMed PubMed Central Google Scholar
• Rape, M. & Kirschner, M. W. Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 432, 588–595 (2004).
  CAS PubMed Google Scholar