Distinct conformations of the protein complex p97- Ufd1-Npl4 revealed by electron cryomicroscopy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 4, 2012, Pages 1098-1103

  Bebeacua, Cecilia ^a   For̈ster, Andreas ^a   McKeown, Ciarań ^a   Meyer, Hemmo H ^b   Zhang, Xiaodong ^a   Freemont, Paul S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Asymmetric complex; ATPase; Electron microscopy; Mechanism; Structure

Indexed keywords

HYBRID PROTEIN; NUCLEOTIDE; P97 UFD1 NPL4 FUSION PROTEIN; PROTEIN P97; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; RING OPENING; THREE DIMENSIONAL IMAGING;

ADENOSINE TRIPHOSPHATASES; CARRIER PROTEINS; CELL CYCLE PROTEINS; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN CONFORMATION; PROTEINS;

EID: 84863020783     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1114341109     Document Type: Article

References (51)

1. Peters JM, Walsh MJ, Franke WW (1990) An abundant and ubiquitous homooligomeric ring-shaped ATPase particle related to the putative vesicle fusion proteins Sec18p and NSF. EMBO J 9:1757-1767.
2. Dreveny I, et al. (2004) p97 and close encounters of every kind: a brief review. Biochem Soc Trans 32:715-720. (Pubitemid 39524361)
3. Meyer HH, Shorter JG, Seemann J, Pappin D, Warren G (2000) A complex of mammalian ufd1 and npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways. EMBO J 19:2181-2192. (Pubitemid 30258999)
4. Bruderer RM, Brasseur C, Meyer HH (2004) The AAA ATPase p97/VCP interacts with its alternative co-factors, Ufd1-Npl4 and p47, through a common bipartite binding mechanism. J Biol Chem 279:49609-49616. (Pubitemid 39577763)
5. Pye VE, et al. (2007) Structural insights into the p97-Ufd1-Npl4 complex. Proc Natl Acad Sci USA 104:467-472. (Pubitemid 46123049)
6. Isaacson RL, et al. (2007) Detailed structural insights into the p97-Npl4-Ufd1 interface. J Biol Chem 282:21361-21369. (Pubitemid 47099912)
7. Bays NW, Wilhovsky SK, Goradia A, Hodgkiss-Harlow K, Hampton RY (2001) HRD4/ NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol Biol Cell 12:4114-4128. (Pubitemid 34001096)
8. Braun S, Matuschewski K, Rape M, Thoms S, Jentsch S (2002) Role of the ubiquitinselective CDC48(UFD1/NPL4) chaperone (segregase) in ERAD of OLE1 and other substrates. EMBO J 21:615-621. (Pubitemid 34174042)
9. Jarosch E, Geiss-Friedlander R, Meusser B, Walter J, Sommer T (2002) Protein dislocation from the endoplasmic reticulum 'pulling out the suspect'. Traffic 3:530-536. (Pubitemid 35452890)
10. Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414:652-656. (Pubitemid 33151262)
11. Hetzer M, et al. (2001) Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat Cell Biol 3:1086-1091. (Pubitemid 33130459)
12. Ramadan K, et al. (2007) Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 450:1258-1262.
13. Mouysset J, et al. (2008) Cell cycle progression requires the CDC-48UFD-1/NPL-4 complex for efficient DNA replication. Proc Natl Acad Sci USA 105:12879-12884.
14. Hoppe T, et al. (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577-586.
15. Rape M, et al. (2001) Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone. Cell 107:667-677. (Pubitemid 34014867)
16. Ye Y, Meyer HH, Rapoport TA (2003) Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J Cell Biol 162:71-84. (Pubitemid 36859536)
17. Dobrynin G, et al. (2011) Cdc48/p97-Ufd1-Npl4 antagonizes Aurora B during chromosome segregation in HeLa cells. J Cell Sci 124:1571-1580.
18. Jentsch S, Rumpf S (2007) Cdc48 (p97): a 'molecular gearbox' in the ubiquitin pathway? Trends Biochem Sci 32:6-11.
19. Rumpf S, Jentsch S (2006) Functional division of substrate processing cofactors of the ubiquitin-selective Cdc48 chaperone. Mol Cell 21:261-269. (Pubitemid 43099941)
20. Zhang X, et al. (2000) Structure of the AAA ATPase p97. Mol Cell 6:1473-1484. (Pubitemid 32045938)
21. Huyton T, et al. (2003) The crystal structure of murine p97/VCP at 3.6 A. J Struct Biol 144:337-348. (Pubitemid 37468391)
22. DeLaBarre B, Brunger AT (2003) Complete structure of p97/valosin- containing protein reveals communication between nucleotide domains. Nat Struct Biol 10:856-863. (Pubitemid 37187659)
23. Yeung HO, et al. (2008) Insights into adaptor binding to the AAA protein p97. Biochem Soc Trans 36:62-67. (Pubitemid 351269623)
24. Song C, Wang Q, Li C-CH (2003) ATPase activity of p97-valosin-containing protein (VCP). D2 mediates the major enzyme activity, and D1 contributes to the heat-induced activity. J Biol Chem 278:3648-3655. (Pubitemid 36801088)
25. Wang B, et al. (2003) Structure and ubiquitin interactions of the conserved zinc finger domain of Npl4. J Biol Chem 278:20225-20234. (Pubitemid 36799220)
26. Briggs LC, et al. (2008) Analysis of nucleotide binding to P97 reveals the properties of a tandem AAA hexameric ATPase. J Biol Chem 283:13745-13752.
27. Rouiller I, et al. (2002) Conformational changes of the multifunction p97 AAA ATPase during its ATPase cycle. Nat Struct Biol 9:950-957. (Pubitemid 35417066)
28. Beuron F, et al. (2003) Motions and negative cooperativity between p97 domains revealed by cryo-electron microscopy and quantized elastic deformational model. J Mol Biol 327:619-629. (Pubitemid 36299068)
29. Davies JM, Tsuruta H, May AP, Weis WI (2005) Conformational changes of p97 during nucleotide hydrolysis determined by small-angle X-Ray scattering. Structure 13:183-195. (Pubitemid 40247696)
30. DeLaBarre B, Brunger AT (2005) Nucleotide dependent motion and mechanism of action of p97/VCP. J Mol Biol 347:437-452. (Pubitemid 40312469)
31. DeLaBarre B, Christianson JC, Kopito RR, Brunger AT (2006) Central pore residues mediate the p97/VCP activity required for ERAD. Mol Cell 22:451-462.
32. Rothballer A, Tzvetkov N, Zwickl P (2007) Mutations in p97/VCP induce unfolding activity. FEBS Lett 581:1197-1201. (Pubitemid 46385945)
33. Ogura T, et al. (2008) From the common molecular basis of the AAA protein to various energy-dependent and -independent activities of AAA proteins. Biochem Soc Trans 36:68-71. (Pubitemid 351269624)
34. Matsushita-Ishiodori Y, Yamanaka K, Hashimoto H, Esaki M, Ogura T (2009) Conserved aromatic and basic amino acid residues in the pore region of Caenorhabditis elegans spastin play critical roles in microtubule severing. Genes Cells 14:925-940.
35. Wendler P, et al. (2009) Motor mechanism for protein threading through Hsp104. Mol Cell 34:81-92.
36. Lee S, Choi JM, Tsai FT (2007) Visualizing the ATPase cycle in a protein disaggregating machine: structural basis for substrate binding by ClpB. Mol Cell 25:261-271. (Pubitemid 46109613)
37. Park S, Isaacson R, Kim HT, Silver PA, Wagner G (2005) Ufd1 exhibits the AAA-ATPase fold with two distinct ubiquitin interaction sites. Structure 13:995-1005. (Pubitemid 40943331)
38. Hänzelmann P, Buchberger A, Schindelin H (2011) Hierarchical binding of cofactors to the AAA ATPase p97. Structure 19:833-843.
39. Pye VE, et al. (2006) Going through the motions: the ATPase cycle of p97. J Struct Biol 156:12-28. (Pubitemid 44486059)
40. Radermacher M (1988) Three-dimensional reconstruction of single particles from random and nonrandom tilt series. J Electron Micro Tech 9:359-394.
41. van Heel M, Schatz M (2005) Fourier shell correlation threshold criteria. J Struct Biol 151:250-262.
42. Harauz G, Ottensmeyer FP (1984) Direct three-dimensional reconstruction for macromolecular complexes from electron-micrographs. Ultramicroscopy 12:309-320.
43. Beuron F, et al. (2006) Conformational changes in the AAA ATPase p97-p47 adaptor complex. EMBO J 25:1967-1976.
44. Alexandru G, et al. (2008) UBXD7 binds multiple ubiquitin ligases and implicates p97 in HIF1alpha turnover. Cell 134:804-816.
45. Richly H, et al. (2005) A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 120:73-84. (Pubitemid 40094604)
46. Tang WK, et al. (2010) A novel ATP-dependent conformation in p97 N-D1 fragment revealed by crystal structures of disease-related mutants. EMBO J 29:2217-2229.
47. Davies JM, Brunger AT,WeisWI (2008) Improved structures of full-length p97, an AAA ATPase: implications for mechanisms of nucleotide-dependent conformational change. Structure 16:715-726. (Pubitemid 351615011)
48. Dai RM, Li CC (2001) Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat Cell Biol 3:740-744. (Pubitemid 32734252)
49. Meyer HH, Wang Y, Warren G (2002) Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1-Npl4. EMBO J 21:5645-5652. (Pubitemid 35315264)
50. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116:17-24. (Pubitemid 26093118)
51. Pettersen EF, et al. (2004) UCSF Chimera-A visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612.