The 1.9 Å structure of a proteasome-11S activator complex and implications for proteasome-PAN/PA700 interactions

Molecular Cell

Volumn 18, Issue 5, 2005, Pages 589-599

  Förster, Andreas ^a   Masters, Eugene I ^a   Whitby, Frank G ^a   Robinson, Howard ^b   Hill, Christopher P ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARCHAEAL PROTEIN; LYSINE; PROTEASOME; PROTEIN PA 700; PROTEIN PAN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; MUSCLE PROTEIN; PA700 PROTEASOME ACTIVATOR; PROTEASOME, THERMOPLASMA; PROTEINASE; PSME1 PROTEIN, HUMAN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL ANALYSIS; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; WILD TYPE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

ARCHAEA;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ENDOPEPTIDASES; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT;

EID: 19444387760     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.04.016     Document Type: Article

References (52)

1. N. Benaroudj, and A.L. Goldberg PAN, the proteasome-activating nucleotidase from archaebacteria, is a protein-unfolding molecular chaperone Nat. Cell Biol. 1 2000 833 839
2. N. Benaroudj, P. Zwickl, E. Seemüller, W. Baumeister, and A.L. Goldberg ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation Mol. Cell 11 2003 69 78
3. T. Bergfors Seeds to crystals J. Struct. Biol. 142 2003 66 76
4. F. Beuron, M.R. Maurizi, D.M. Belnap, E. Kocsis, F.P. Booy, M. Kessel, and A.C. Steven At sixes and sevens: characterization of the symmetry mismatch of the ClpAP chaperone-assisted protease J. Struct. Biol. 123 1998 248 259
5. M. Bochtler, L. Ditzel, M. Groll, C. Hartmann, and R. Huber The proteasome Annu. Rev. Biophys. Biomol. Struct. 28 1999 295 317
6. M. Bochtler, L. Ditzel, M. Groll, and R. Huber Crystal structure of heat shock locus V (HslV) from Escherichia coli Proc. Natl. Acad. Sci. USA 94 1997 6070 6074
7. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
8. N. Collaborative Computational Project The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
9. W.L. DeLano 2002
10. W. Dubiel, G. Pratt, K. Ferrell, and M. Rechsteiner Purification of an 11 S regulator of the multicatalytic protease J. Biol. Chem. 267 1992 22369 22377
11. A.M. Eleuteri, R.A. Kohanski, C. Cardozo, and M. Orlowski Bovine spleen multicatalytic proteinase complex (proteasome). Replacement of X, Y, and Z subunits by LMP7, LMP2, and MECL1 and changes in properties and specificity J. Biol. Chem. 272 1997 11824 11831
12. A. Förster, F.G. Whitby, and C.P. Hill The pore of activated 20S proteasomes has an ordered 7-fold symmetric conformation EMBO J. 22 2003 4356 4364
13. S. Gottesman Proteolysis in bacterial regulatory circuits Annu. Rev. Cell Dev. Biol. 19 2003 565 587
14. M. Groll, M. Bajorek, A. Köhler, L. Moroder, D.M. Rubin, R. Huber, M.H. Glickman, and D. Finley A gated channel into the proteasome core particle Nat. Struct. Biol. 7 2000 1062 1067
15. M. Groll, H. Brandstetter, H. Bartunik, G. Bourenkow, and R. Huber Investigations on the maturation and regulation of archaebacterial proteasomes J. Mol. Biol. 327 2003 75 83
16. M. Groll, L. Ditzel, J. Löwe, D. Stock, M. Bochtler, H.D. Bartunik, and R. Huber Structure of 20S proteasome from yeast at 2.4Å resolution Nature 386 1997 463 471
17. F. Guo, M.R. Maurizi, L. Esser, and D. Xia Crystal structure of ClpA, an Hsp100 chaperone and regulator of ClpAP protease J. Biol. Chem. 277 2002 46743 46752
18. W. Heinemeyer, N. Trondle, G. Albrecht, and D.H. Wolf PRE5 and PRE6, the last missing genes encoding 20S proteasome subunits from yeast? Indication for a set of 14 different subunits in the eukaryotic proteasome core Biochemistry 33 1994 12229 12237
19. W. Hilt, W. Heinemeyer, and D.H. Wolf Studies on the yeast proteasome uncover its basic structural features and multiple in vivo functions Enzyme Protein 47 1993 189 201
20. T.A. Jones, J.Y. Zou, S.W. Cowan, and M. Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
21. A.V. Kajava, C. Gorbea, J. Ortega, M. Rechsteiner, and A.C. Steven New HEAT-like repeat motifs in proteins regulating proteasome structure and function J. Struct. Biol. 146 2004 425 430
22. D.Y. Kim, and K.K. Kim Crystal structure of ClpX molecular chaperone from Helicobacter pylori J. Biol. Chem. 278 2003 50664 50670
23. Y.I. Kim, I. Levchenko, K. Fraczkowska, R.V. Woodruff, R.T. Sauer, and T.A. Baker Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase Nat. Struct. Biol. 8 2001 230 233
24. J.R. Knowlton, S.C. Johnston, F.G. Whitby, C. Realini, Z. Zhang, M. Rechsteiner, and C.P. Hill Structure of the proteasome activator REGalpha (PA28alpha) Nature 390 1997 639 643
25. A. Köhler, P. Cascio, D.S. Leggett, K.M. Woo, A.L. Goldberg, and D. Finley The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release Mol. Cell 7 2001 1143 1152
26. F. Kopp, K.B. Hendil, B. Dahlmann, P. Kristensen, A. Sobek, and W. Uerkvitz Subunit arrangement in the human 20S proteasome Proc. Natl. Acad. Sci. USA 94 1997 2939 2944
27. S.Y. Lee, A. De La Torre, D. Yan, S. Kustu, B.T. Nixon, and D.E. Wemmer Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains Genes Dev. 17 2003 2552 2563
28. J. Li, X. Gao, L. Joss, and M. Rechsteiner The proteasome activator 11 S REG or PA28: chimeras implicate carboxyl-terminal sequences in oligomerization and proteasome binding but not in the activation of specific proteasome catalytic subunits J. Mol. Biol. 299 2000 641 654
29. J. Löwe, D. Stock, B. Jap, P. Zwickl, W. Baumeister, and R. Huber Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution Science 268 1995 533 539
30. C.P. Ma, C.A. Slaughter, and G.N. DeMartino Identification, purification, and characterization of a protein activator (PA28) of the 20 S proteasome (macropain) J. Biol. Chem. 267 1992 10515 10523
31. C.P. Ma, P.J. Willy, C.A. Slaughter, and G.N. DeMartino PA28, an activator of the 20 S proteasome, is inactivated by proteolytic modification at its carboxyl terminus J. Biol. Chem. 268 1993 22514 22519
32. S. Majeed, G. Ofek, A. Belachew, C.C. Huang, T. Zhou, and P.D. Kwong Enhancing protein crystallization through precipitant synergy Structure 11 2003 1061 1070
33. D. Missiakas, F. Schwager, J.M. Betton, C. Georgopoulos, and S. Raina Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli EMBO J. 15 1996 6899 6909
34. R.J. Morris, A. Perrakis, and V.S. Lamzin ARP/wARP and automatic interpretation of protein electron density maps Methods Enzymol. 374 2003 229 244
35. G.N. Murshudov Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
36. D.L. Mykles Differential effects of bovine PA28 on six peptidase activities of the lobster muscle proteasome (multicatalytic proteinase) Arch. Biochem. Biophys. 325 1996 77 81
37. J. Navaza Implementation of molecular replacement in AMoRe Acta Crystallogr. D Biol. Crystallogr. 57 2001 1367 1372
38. A.F. Neuwald, L. Aravind, J.L. Spouge, and E.V. Koonin AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes Genome Res. 9 1999 27 43
39. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
40. J.S. Philo A method for directly fitting the time derivative of sedimentation velocity data and an alternative algorithm for calculating sedimentation coefficient distribution functions Anal. Biochem. 279 2000 151 163
41. M. Rechsteiner, and C.P. Hill Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors Trends Cell Biol. 15 2005 27 33
42. S.K. Singh, J. Rozycki, J. Ortega, T. Ishikawa, J. Lo, A.C. Steven, and M.R. Maurizi Functional domains of the ClpA and ClpX molecular chaperones identified by limited proteolysis and deletion analysis J. Biol. Chem. 276 2001 29420 29429
43. X. Song, J. von Kampen, C.A. Slaughter, and G.N. DeMartino Relative functions of the α and β subunits of the proteasome activator, PA28 J. Biol. Chem. 272 1997 27994 28000
44. M.C. Sousa, C.B. Trame, H. Tsuruta, S.M. Wilbanks, V.S. Reddy, and D.B. McKay Crystal and solution structures of an HslUV protease-chaperone complex Cell 103 2000 633 643
45. M. Unno, T. Mizushima, Y. Morimoto, Y. Tomisugi, K. Tanaka, N. Yasuoka, and T. Tsukihara The structure of the mammalian 20S proteasome at 2.75 Å resolution Structure 10 2002 609 618
46. V. Ustrell, L. Hoffman, G. Pratt, and M. Rechsteiner PA200, a nuclear proteasome activator involved in DNA repair EMBO J. 21 2002 3516 3525
47. I. Velichutina, P.L. Connerly, C.S. Arendt, X. Li, and M. Hochstrasser Plasticity in eucaryotic 20S proteasome ring assembly revealed by a subunit deletion in yeast EMBO J. 23 2004 500 510
48. J. Wang, J.J. Song, M.C. Franklin, S. Kamtekar, Y.J. Im, S.H. Rho, I.S. Seong, C.S. Lee, C.H. Chung, and S.H. Eom Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism Structure 9 2001 177 184
49. F.G. Whitby, E.I. Masters, L. Kramer, J.R. Knowlton, Y. Yao, C.C. Wang, and C.P. Hill Structural basis for the activation of 20S proteasomes by 11S regulators Nature 408 2000 115 120
50. Y. Yao, L. Huang, A. Krutchinsky, M.L. Wong, K.G. Standing, A.L. Burlingame, and C.C. Wang Structural and functional characterization of the proteasome-activating protein PA26 from Trypanosoma brucei J. Biol. Chem. 274 1999 33921 33930
51. Z. Zhang, A. Clawson, C. Realini, C.C. Jensen, J.R. Knowlton, C.P. Hill, and M. Rechsteiner Identification of an activation region in the proteasome activator REGalpha Proc. Natl. Acad. Sci. USA 95 1998 2807 2811
52. P. Zwickl, D. Ng, K.M. Woo, H.P. Klenk, and A.L. Goldberg An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26 S proteasome, activates protein breakdown by 20 S proteasomes J. Biol. Chem. 274 1999 26008 26014