Phosphorylation of the C-terminal tail of proteasome subunit α7 is required for binding of the proteasome quality control factor Ecm29

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Wani, Prashant S ^a   Suppahia, Anjana ^a   Capalla, Xavier ^a   Ondracek, Alex ^a   Roelofs, Jeroen ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ECM29 PROTEIN, S CEREVISIAE; PRE10 PROTEIN, S CEREVISIAE; PROTEASOME; RPT5 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

GENETICS; METABOLISM; PHOSPHORYLATION;

ADENOSINE TRIPHOSPHATASES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84975076561     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27873     Document Type: Article

References (70)

1. Finley, D., Ulrich, H. D., Sommer, T., Kaiser, P. The ubiquitin-proteasome system of Saccharomyces cerevisiae. Genetics 192, 319-360, doi: 10.1534/genetics.112.140467 (2012).
2. Shi, Y. et al. Rpn1 provides adjacent receptor sites for substrate binding and deubiquitination by the proteasome. Science 351, doi: 10.1126/science.aad9421 (2016).
3. Finley, D., Chen, X., Walters, K. J. Gates, Channels, Switches: Elements of the Proteasome Machine. Trends Biochem Sci 41, 77-93, doi: 10.1016/j.tibs.2015.10.009 (2016).
4. Bedford, L., Paine, S., Sheppard, P. W., Mayer, R. J., Roelofs, J. Assembly, structure, function of the 26S proteasome. Trends Cell Biol 20, 391-401, doi: 10.1016/j.tcb.2010.03.007 (2010).
5. Tomko, R. J., Jr., Hochstrasser, M. Molecular architecture and assembly of the eukaryotic proteasome. Annu Rev Biochem 82, 415-445, doi: 10.1146/annurev-biochem-060410-150257 (2013).
6. Wani, P. S., Rowland, M. A., Ondracek, A., Deeds, E. J., Roelofs, J. Maturation of the proteasome core particle induces an affinity switch that controls regulatory particle association. Nat Commun 6, 6384, doi: 10.1038/ncomms7384 (2015).
7. Kock, M. et al. Proteasome assembly from 15S precursors involves major conformational changes and recycling of the Pba1-Pba2 chaperone. Nat Commun 6, 6123, doi: 10.1038/ncomms7123 (2015).
8. Roelofs, J. et al. Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459, 861-865, doi: 10.1038/nature08063 (2009).
9. Barrault, M. B. et al. Dual functions of the Hsm3 protein in chaperoning and scaffolding regulatory particle subunits during the proteasome assembly. Proc Natl Acad Sci USA 109, E1001-1010, doi: 10.1073/pnas.1116538109 (2012).
10. Ehlinger, A. et al. Conformational dynamics of the rpt6 ATPase in proteasome assembly and rpn14 binding. Structure 21, 753-765, doi: 10.1016/j.str.2013.02.021 (2013).
11. Park, S. et al. Reconfiguration of the proteasome during chaperone-mediated assembly. Nature 497, 512-516, doi: 10.1038/nature12123 (2013).
12. Schmidt, M., Hanna, J., Elsasser, S., Finley, D. Proteasome-associated proteins: regulation of a proteolytic machine. Biol Chem 386, 725-737, doi: 10.1515/BC.2005.085 (2005).
13. Leggett, D. S. et al. Multiple associated proteins regulate proteasome structure and function. Mol Cell 10, 495-507, doi: 10.1016/S109727650200638X [pii] (2002).
14. De La Mota-Peynado, A. et al. The Proteasome-associated Protein Ecm29 Inhibits Proteasomal ATPase Activity and in Vivo Protein Degradation by the Proteasome. J Biol Chem 288, 29467-29481, doi: 10.1074/jbc.M113.491662 (2013).
15. Kleijnen, M. F. et al. Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites. Nat Struct Mol Biol 14, 1180-1188, doi: 10.1038/nsmb1335 (2007).
16. Kajava, A. V., Gorbea, C., Ortega, J., Rechsteiner, M., Steven, A. C. New HEAT-like repeat motifs in proteins regulating proteasome structure and function. J Struct Biol 146, 425-430, doi: 10.1016/j.jsb.2004.01.013 (2004).
17. Park, S., Kim, W., Tian, G., Gygi, S. P., Finley, D. Structural defects in the regulatory particle-core particle interface of the proteasome induce a novel proteasome stress response. J Biol Chem 286, 36652-36666, doi: 10.1074/jbc.M111.285924 (2011).
18. Wang, X., Yen, J., Kaiser, P., Huang, L. Regulation of the 26S proteasome complex during oxidative stress. Sci Signal 3, ra88, doi: 10.1126/scisignal.2001232 (2010).
19. Gorbea, C., Goellner, G. M., Teter, K., Holmes, R. K., Rechsteiner, M. Characterization of mammalian Ecm29, a 26S proteasomeassociated protein that localizes to the nucleus and membrane vesicles. J Biol Chem 279, 54849-54861, doi: 10.1074/jbc.M410444200 (2004).
20. Gorbea, C. et al. A protein interaction network for Ecm29 links the 26S proteasome to molecular motors and endosomal components. J Biol Chem 285, 31616-31633, doi: 10.1074/jbc.M110.154120 (2010).
21. Gorbea, C., Rechsteiner, M., Vallejo, J. G., Bowles, N. E. Depletion of the 26S proteasome adaptor Ecm29 increases Toll-like receptor 3 signaling. Sci Signal 6, ra86, doi: 10.1126/scisignal.2004301 (2013).
22. Hsu, M. T. et al. Stage-Dependent Axon Transport of Proteasomes Contributes to Axon Development. Dev Cell 35, 418-431, doi: 10.1016/j.devcel.2015.10.018 (2015).
23. Lee, S. Y., De la Mota-Peynado, A., Roelofs, J. Loss of Rpt5 protein interactions with the core particle and Nas2 protein causes the formation of faulty proteasomes that are inhibited by Ecm29 protein. J Biol Chem 286, 36641-36651, doi: 10.1074/jbc.M111.280875 (2011).
24. Lehmann, A., Niewienda, A., Jechow, K., Janek, K., Enenkel, C. Ecm29 Fulfils Quality Control Functions in Proteasome Assembly. Molecular Cell 38, 879-888, doi: 10.1016/j.molcel.2010.06.016 (2010).
25. Panasenko, O. O., Collart, M. A. Not4 E3 ligase contributes to proteasome assembly and functional integrity in part through Ecm29. Molecular and Cellular Biology 31, 1610-1623, doi: 10.1128/mcb.01210-10 (2011).
26. Tian, G. et al. An asymmetric interface between the regulatory and core particles of the proteasome. Nat Struct Mol Biol 18, 1259-1267, doi: 10.1038/nsmb.2147 (2011).
27. Lander, G. C. et al. Complete subunit architecture of the proteasome regulatory particle. Nature 482, 186-191, doi: 10.1038/nature10774 (2012).
28. Lasker, K. et al. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci USA 109, 1380-1387, doi: 10.1073/pnas.1120559109 (2012).
29. Beck, F. et al. Near-atomic resolution structural model of the yeast 26S proteasome. Proc Natl Acad Sci USA 109, 14870-14875, doi: 10.1073/pnas.1213333109 (2012).
30. Groll, M. et al. Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386, 463-471, doi: 10.1038/386463a0 (1997).
31. Harshbarger, W., Miller, C., Diedrich, C., Sacchettini, J. Crystal structure of the human 20S proteasome in complex with carfilzomib. Structure 23, 418-424, doi: 10.1016/j.str.2014.11.017 (2015).
32. Schmidt, M. et al. The HEAT repeat protein Blm10 regulates the yeast proteasome by capping the core particle. Nat Struct Mol Biol 12, 294-303, doi: 10.1038/nsmb914 (2005).
33. Forster, A., Masters, E. I., Whitby, F. G., Robinson, H., Hill, C. P. The 1.9A structure of a proteasome-11S activator complex and implications for proteasome-PAN/PA700 interactions. Mol Cell 18, 589-599, doi: 10.1016/j.molcel.2005.04.016 (2005).
34. Rabl, J. et al. Mechanism of Gate Opening in the 20S Proteasome by the Proteasomal ATPases. Molecular Cell 30, 360-368, doi: 10.1016/j.molcel.2008.03.004 (2008).
35. Gillette, T. G., Kumar, B., Thompson, D., Slaughter, C. A., DeMartino, G. N. Differential roles of the COOH termini of AAA subunits of PA700 (19S regulator) in asymmetric assembly and activation of the 26S proteasome. J Biol Chem 283, 31813-31822, doi: 10.1074/jbc.M805935200 (2008).
36. Smith, D. M. et al. Docking of the Proteasomal ATPases' Carboxyl Termini in the 20S Proteasome's ? Ring Opens the Gate for Substrate Entry. Molecular Cell 27, 731-744, doi: 10.1016/j.molcel.2007.06.033 (2007).
37. Iwafune, Y., Kawasaki, H., Hirano, H. Identification of three phosphorylation sites in the alpha7 subunit of the yeast 20S proteasome in vivo using mass spectrometry. Arch Biochem Biophys 431, 9-15, doi: 10.1016/j.abb.2004.07.020 (2004).
38. Helbig, A. O. et al. Perturbation of the yeast N-acetyltransferase NatB induces elevation of protein phosphorylation levels. BMC Genomics 11, 685, doi: 10.1186/1471-2164-11-685 (2010).
39. Soufi, B. et al. Global analysis of the yeast osmotic stress response by quantitative proteomics. Mol Biosyst 5, 1337-1346, doi: 10.1039/b902256b (2009).
40. Gnad, F. et al. High-accuracy identification and bioinformatic analysis of in vivo protein phosphorylation sites in yeast. Proteomics 9, 4642-4652, doi: 10.1002/pmic.200900144 (2009).
41. Albuquerque, C. P. et al. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 7, 1389-1396, doi: 10.1074/mcp.M700468-MCP200 (2008).
42. Swaney, D. L. et al. Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat Methods 10, 676-682, doi: 10.1038/nmeth.2519 (2013).
43. Gersch, M. et al. A mass spectrometry platform for a streamlined investigation of proteasome integrity, posttranslational modifications, inhibitor binding. Chem Biol 22, 404-411, doi: 10.1016/j.chembiol.2015.01.004 (2015).
44. Wang, X. et al. Mass spectrometric characterization of the affinity-purified human 26S proteasome complex. Biochemistry 46, 3553-3565, doi: 10.1021/bi061994u (2007).
45. Claverol, S., Burlet-Schiltz, O., Girbal-Neuhauser, E., Gairin, J. E., Monsarrat, B. Mapping and structural dissection of human 20S proteasome using proteomic approaches. Mol Cell Proteomics 1, 567-578 doi: 10.1074/mcp.M200030-MCP200 (2002).
46. 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, doi: 10.1042/BJ20031122 (2004).
47. Castano, J. G., Mahillo, E., Arizti, P., Arribas, J. Phosphorylation of C8 and C9 subunits of the multicatalytic proteinase by casein kinase II and identification of the C8 phosphorylation sites by direct mutagenesis. Biochemistry 35, 3782-3789, doi: 10.1021/bi952540s (1996).
48. Meggio, F., Pinna, L. A. One-thousand-and-one substrates of protein kinase CK2? FASEB J 17, 349-368, doi: 10.1096/fj.02-0473rev (2003).
49. Sha, Z., Peth, A., Goldberg, A. L. Keeping proteasomes under control-a role for phosphorylation in the nucleus. Proc Natl Acad Sci USA 108, 18573-18574, doi: 10.1073/pnas.1115315108 (2011).
50. 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, doi: 10.1074/jbc.M109.021956 (2009).
51. Zhang, F. et al. Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. J Biol Chem 282, 22460-22471, doi: 10.1074/jbc.M702439200 (2007).
52. Lokireddy, S., Kukushkin, N. V., Goldberg, A. L. cAMP-induced phosphorylation of 26S proteasomes on Rpn6/PSMD11 enhances their activity and the degradation of misfolded proteins. Proc Natl Acad Sci USA 112, E7176-7185, doi: 10.1073/pnas.1522332112 (2015).
53. Guo, X. et al. Site-specific proteasome phosphorylation controls cell proliferation and tumorigenesis. Nat Cell Biol 18, 202-212, doi: 10.1038/ncb3289 (2016).
54. Guo, X. et al. UBLCP1 is a 26S proteasome phosphatase that regulates nuclear proteasome activity. Proc Natl Acad Sci USA 108, 18649-18654, doi: 10.1073/pnas.1113170108 (2011).
55. 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, doi: 10.1021/bi001815n (2001).
56. Semplici, F., Meggio, F., Pinna, L. A., Oliviero, S. CK2-dependent phosphorylation of the E2 ubiquitin conjugating enzyme UBC3B induces its interaction with beta-TrCP and enhances beta-catenin degradation. Oncogene 21, 3978-3987, doi: 10.1038/sj. onc.1205574 (2002).
57. Sanchez-Lanzas, R., Castano, J. G. Proteins directly interacting with mammalian 20S proteasomal subunits and ubiquitinindependent proteasomal degradation. Biomolecules 4, 1140-1154, doi: 10.3390/biom4041140 (2014).
58. Geng, S., White, S. N., Paine, M. L., Snead, M. L. Protein Interaction between Ameloblastin and Proteasome Subunit alpha Type 3 Can Facilitate Redistribution of Ameloblastin Domains within Forming Enamel. J Biol Chem 290, 20661-20673, doi: 10.1074/jbc. M115.640185 (2015).
59. Xie, Y., Varshavsky, A. RPN4 is a ligand, substrate, transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc Natl Acad Sci USA 98, 3056-3061, doi: 10.1073/pnas.071022298 (2001).
60. Mannhaupt, G., Schnall, R., Karpov, V., Vetter, I., Feldmann, H. Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett 450, 27-34, doi: 10.1016/S0014-5793(99)00467-6 (1999).
61. Unverdorben, P. et al. Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome. Proc Natl Acad Sci USA 111, 5544-5549, doi: 10.1073/pnas.1403409111 (2014).
62. Matyskiela, M. E., Lander, G. C., Martin, A. Conformational switching of the 26S proteasome enables substrate degradation. Nat Struct Mol Biol 20, 781-788, doi: 10.1038/nsmb.2616 (2013).
63. Asano, S. et al. Proteasomes. A molecular census of 26S proteasomes in intact neurons. Science 347, 439-442, doi: 10.1126/science.1261197 (2015).
64. Fishbain, S. et al. Sequence composition of disordered regions fine-tunes protein half-life. Nat Struct Mol Biol 22, 214-221, doi: 10.1038/nsmb.2958 (2015).
65. Goldstein, A. L., McCusker, J. H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553, doi: 10.1002/(SICI)1097-0061(199910)15:14 3.0.CO;2-K (1999).
66. Longtine, M. S. et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961, doi: 10.1002/(SICI)1097-0061(199807)14:10 3.0.CO;2-U (1998).
67. Elsasser, S., Schmidt, M., Finley, D. Characterization of the Proteasome Using Native Gel Electrophoresis. Methods in Enzymology 398, 353-363, doi: 10.1016/s0076-6879(05)98029-4 (2005).
68. Finley, D., Ozkaynak, E., Varshavsky, A. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, other stresses. Cell 48, 1035-1046, doi: 10.1016/0092-8674(87)90711-2 (1987).
69. Leggett, D. S., Glickman, M. H., Finley, D. Purification of proteasomes, proteasome subcomplexes, proteasome-associated proteins from budding yeast. Methods Mol Biol 301, 57-70, doi: 10.1385/1-59259-895-1:057 (2005).
70. Brachmann, C. B. et al. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132, doi: 10.1002/(SICI)1097-0061(19980130)14:2 3.0.CO;2-2 (1998).