Recent advances in the structural biology of the 26S proteasome

International Journal of Biochemistry and Cell Biology

Volumn 79, Issue , 2016, Pages 437-442

  Wehmer, Marc ^a   Sakata, Eri ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

26S proteasome; AAA+ ATPase; Cryoelectron microscopy; Single particle analysis; Structural biology

Indexed keywords

26S PROTEASOME; ADENOSINE TRIPHOSPHATASE; NUCLEOTIDASE; PROTEASOME; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE;

CHROMOSOME TRANSLOCATION; CRYOELECTRON MICROSCOPY; HYDROLYSIS; IMAGE PROCESSING; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN UNFOLDING; REVIEW; UBIQUITINATION; ANIMAL; CHEMISTRY; HUMAN; METABOLISM;

ANIMALS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 84991670386     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2016.08.008     Document Type: Review

References (54)

1. Asano, S., Fukuda, Y., Beck, F., Aufderheide, A., Förster, F., Danev, R., Baumeister, W., A molecular census of 26S proteasomes in intact neurons. Science 347:6220 (2015), 439–442.
2. Bai, X.C., Fernandez, I.S., McMullan, G., Scheres, S.H., Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife, 2, 2013, e00461.
3. Beck, F., Unverdorben, P., Bohn, S., Schweitzer, A., Pfeifer, G., Sakata, E., Nickell, S., Plitzko, J.M., Villa, E., Baumeister, W., Forster, F., Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. U. S. A. 109:37 (2012), 14870–14875.
4. Bohn, S., Beck, F., Sakata, E., Walzthoeni, T., Beck, M., Aebersold, R., Forster, F., Baumeister, W., Nickell, S., Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proc. Natl. Acad. Sci. U. S. A. 107:49 (2010), 20992–20997.
5. Dambacher, C.M., Worden, E.J., Herzik, M.A., Martin, A., Lander, G.C., Atomic structure of the 26S proteasome lid reveals the mechanism of deubiquitinase inhibition. eLife, 5, 2016, e13027.
6. Enemark, E.J., Joshua-Tor, L., Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442:7100 (2006), 270–275.
7. Erzberger, J.P., Berger, J.M., Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 35 (2006), 93–114.
8. Estrin, E., Lopez-Blanco, J.R., Chacon, P., Martin, A., Formation of an intricate helical bundle dictates the assembly of the 26S proteasome lid. Structure 21:9 (2013), 1624–1635.
9. Finley, D., Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem 78 (2009), 477–513.
10. Forster, F., Lasker, K., Beck, F., Nickell, S., Sali, A., Baumeister, W., An atomic model AAA-ATPase/20S core particle sub-complex of the 26S proteasome. Biochem. Biophys. Res. Commun. 388:2 (2009), 228–233.
11. Glickman, M.H., Rubin, D.M., Coux, O., Wefes, I., Pfeifer, G., Cjeka, Z., Baumeister, W., Fried, V.A., Finley, D., A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94:5 (1998), 615–623.
12. Groll, M., Ditzel, L., Lowe, J., Stock, D., Bochtler, M., Bartunik, H.D., Huber, R., Structure of 20S proteasome from yeast at 2.4A resolution. Nature 386:6624 (1997), 463–471.
13. Haglund, K., Dikic, I., Ubiquitylation and cell signaling. EMBO J. 24:19 (2005), 3353–3359.
14. He, J., Kulkarni, K., da Fonseca, P.C., Krutauz, D., Glickman, M.H., Barford, D., Morris, E.P., The structure of the 26S proteasome subunit Rpn2 reveals its PC repeat domain as a closed toroid of two concentric alpha-helical rings. Structure 20:3 (2012), 513–521.
15. Hershko, A., Ciechanover, A., The ubiquitin system. Annu. Rev. Biochem 67 (1998), 425–479.
16. Huang, X., Luan, B., Wu, J., Shi, Y., An atomic structure of the human 26S proteasome. Nat. Struct. Mol. Biol., 2016.
17. Kim, Y.C., Snoberger, A., Schupp, J., Smith, D.M., ATP binding to neighbouring subunits and intersubunit allosteric coupling underlie proteasomal ATPase function. Nat. Commun., 6, 2015, 8520.
18. Koga, N., Kameda, T., Okazaki, K., Takada, S., Paddling mechanism for the substrate translocation by AAA+ motor revealed by multiscale molecular simulations. Proc. Natl. Acad. Sci. U. S. A. 106:43 (2009), 18237–18242.
19. Kuhlbrandt, W., Cryo-EM enters a new era. eLife, 3, 2014, e03678.
20. Labbadia, J., Morimoto, R.I., The biology of proteostasis in aging and disease. Annu. Rev. Biochem 84 (2015), 435–464.
21. Lander, G.C., Estrin, E., Matyskiela, M.E., Bashore, C., Nogales, E., Martin, A., Complete subunit architecture of the proteasome regulatory particle. Nature 482:7384 (2012), 186–191.
22. Lasker, K., Forster, F., Bohn, S., Walzthoeni, T., Villa, E., Unverdorben, P., Beck, F., Aebersold, R., Sali, A., Baumeister, W., Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl. Acad. Sci. U. S. A. 109:5 (2012), 1380–1387.
23. Li, X., Mooney, P., Zheng, S., Booth, C.R., Braunfeld, M.B., Gubbens, S., Agard, D.A., Cheng, Y., Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10:6 (2013), 584–590.
24. Lingaraju, G.M., Bunker, R.D., Cavadini, S., Hess, D., Hassiepen, U., Renatus, M., Fischer, E.S., Thoma, N.H., Crystal structure of the human COP9 signalosome. Nature, 2014.
25. Luan, B., Huang, X., Wu, J., Mei, Z., Wang, Y., Xue, X., Yan, C., Wang, J., Finley, D.J., Shi, Y., Wang, F., Structure of an endogenous yeast 26S proteasome reveals two major conformational states. Proc. Natl. Acad. Sci. U. S. A. 113:10 (2016), 2642–2647.
26. Martin, A., Baker, T.A., Sauer, R.T., Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat. Struct. Mol. Biol. 15:11 (2008), 1147–1151.
27. Matyskiela, M.E., Lander, G.C., Martin, A., Conformational switching of the 26S proteasome enables substrate degradation. Nat. Struct. Mol. Biol. 20:7 (2013), 781–788.
28. Nickell, S., Beck, F., Scheres, S.H., Korinek, A., Forster, F., Lasker, K., Mihalache, O., Sun, N., Nagy, I., Sali, A., Plitzko, J.M., Carazo, J.M., Mann, M., Baumeister, W., Insights into the molecular architecture of the 26S proteasome. Proc. Natl. Acad. Sci. U. S. A. 106:29 (2009), 11943–11947.
29. Nogales, E., Scheres, S.H., Cryo-EM: a unique tool for the visualization of macromolecular complexity. Mol. Cell 58:4 (2015), 677–689.
30. Nyquist, K., Martin, A., Marching to the beat of the ring: polypeptide translocation by AAA+ proteases. Trends Biochem. Sci., 2013.
31. Paraskevopoulos, K., Kriegenburg, F., Tatham Michael, H., Rösner Heike, I., Medina, B., Larsen Ida, B., Brandstrup, R., Hardwick Kevin, G., Hay Ronald, T., Kragelund Birthe, B., Hartmann-Petersen, R., Gordon, C., Dss1 is a 26S proteasome ubiquitin receptor. Mol. Cell 56:3 (2014), 453–461.
32. Pathare, G.R., Nagy, I., Bohn, S., Unverdorben, P., Hubert, A., Korner, R., Nickell, S., Lasker, K., Sali, A., Tamura, T., Nishioka, T., Forster, F., Baumeister, W., Bracher, A., The proteasomal subunit Rpn6 is a molecular clamp holding the core and regulatory subcomplexes together. Proc. Natl. Acad. Sci. U. S. A. 109:1 (2012), 149–154.
33. Peters, J.M., Cejka, Z., Harris, J.R., Kleinschmidt, J.A., Baumeister, W., Structural features of the 26S proteasome complex. J. Mol. Biol. 234:4 (1993), 932–937.
34. Petroski, M.D., The ubiquitin system, disease, and drug discovery. BMC Biochem., 9(Suppl. 1), 2008, S7.
35. Querol-Audi, J., Sun, C., Vogan, J.M., Smith, M.D., Gu, Y., Cate, J.H., Nogales, E., Architecture of human translation initiation factor 3. Structure 21:6 (2013), 920–928.
36. Sakata, E., Bohn, S., Mihalache, O., Kiss, P., Beck, F., Nagy, I., Nickell, S., Tanaka, K., Saeki, Y., Forster, F., Baumeister, W., Localization of the proteasomal ubiquitin receptors Rpn10 and Rpn13 by electron cryomicroscopy. Proc. Natl. Acad. Sci. U. S. A. 109:5 (2012), 1479–1484.
37. Sato, Y., Yoshikawa, A., Yamagata, A., Mimura, H., Yamashita, M., Ookata, K., Nureki, O., Iwai, K., Komada, M., Fukai, S., Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains. Nature 455:7211 (2008), 358–362.
38. Schwartz, A.L., Ciechanover, A., Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu. Rev. Pharmacool. Toxicol. 49 (2009), 73–96.
39. Schweitzer, A., Aufderheide, A., Rudack, T., Beck, F., Pfeifer, G., Plitzko, J.M., Sakata, E., Schulten, K., Forster, F., Baumeister, W., Structure of the human 26S proteasome at a resolution of 3.9 A. Proc. Natl. Acad. Sci. U. S. A., 2016.
40. Shi, Y., Chen, X., Elsasser, S., Stocks, B.B., Tian, G., Lee, B.-H., Shi, Y., Zhang, N., de Poot, S.A.H., Tuebing, F., Sun, S., Vannoy, J., Tarasov, S.G., Engen, J.R., Finley, D., Walters, K.J., Rpn1 provides adjacent receptor sites for substrate binding and deubiquitination by the proteasome. Science, 351(6275), 2016.
41. Sledz, P., Unverdorben, P., Beck, F., Pfeifer, G., Schweitzer, A., Forster, F., Baumeister, W., Structure of the 26S proteasome with ATP-gammaS bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc. Natl. Acad. Sci. U. S. A. 110:18 (2013), 7264–7269.
42. 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 144:4 (2011), 526–538.
43. Thomsen, N.D., Berger, J.M., Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 139:3 (2009), 523–534.
44. Thrower, J.S., Hoffman, L., Rechsteiner, M., Pickart, C.M., Recognition of the polyubiquitin proteolytic signal. EMBO J. 19:1 (2000), 94–102.
45. Tomko, R.J. Jr., Hochstrasser, M., Incorporation of the Rpn12 subunit couples completion of proteasome regulatory particle lid assembly to lid-base joining. Mol. Cell 44:6 (2011), 907–917.
46. Tomko, R.J. Jr., Funakoshi, M., Schneider, K., Wang, J., Hochstrasser, M., Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: implications for proteasome structure and assembly. Mol. Cell 38:3 (2010), 393–403.
47. Tomko, R.J. Jr., Taylor, D.W., Chen, Z.A., Wang, H.W., Rappsilber, J., Hochstrasser, M., A single alpha helix drives extensive remodeling of the proteasome lid and completion of regulatory particle assembly. Cell 163:2 (2015), 432–444.
48. Unverdorben, P., Beck, F., Sledz, P., Schweitzer, A., Pfeifer, G., Plitzko, J.M., Baumeister, W., Forster, F., Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome. Proc. Natl. Acad. Sci. U. S. A. 111:15 (2014), 5544–5549.
49. Verma, R., Aravind, L., Oania, R., McDonald, W.H., Yates, J.R. 3rd, Koonin, E.V., Deshaies, R.J., Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:5593 (2002), 611–615.
50. Voges, D., Zwickl, P., Baumeister, W., The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68 (1999), 1015–1068.
51. Wendler, P., Ciniawsky, S., Kock, M., Kube, S., Structure and function of the AAA+ nucleotide binding pocket. Biochim. Biophys. Acta 1823:1 (2012), 2–14.
52. Worden, E.J., Padovani, C., Martin, A., Structure of the Rpn11-Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation. Nat. Struct. Mol. Biol., 2014 advance online publication.
53. Yao, T., Cohen, R.E., A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419:6905 (2002), 403–407.
54. da Fonseca, P.C., He, J., Morris, E.P., Molecular model of the human 26S proteasome. Mol. Cell 46:1 (2012), 54–66.