Central Pore Residues Mediate the p97/VCP Activity Required for ERAD

Molecular Cell

Volumn 22, Issue 4, 2006, Pages 451-462

  DeLaBarre, Byron ^a,b   Christianson, John C ^a   Kopito, Ron R ^a   Brunger, Axel T ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

Author keywords

CELLBIO; PROTEINS

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARGININE; HISTIDINE; MUTANT PROTEIN; PROTEIN P97; SYNAPTOTAGMIN;

ANIMAL CELL; ARTICLE; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PROTEIN DEGRADATION; TIGHT JUNCTION; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; ENDOPLASMIC RETICULUM; KINETICS; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; PROTEIN STRUCTURE, QUATERNARY; RATS; RECOMBINANT PROTEINS; SYNAPTOTAGMIN I; TRANSFECTION;

ANIMALIA;

EID: 33646535590     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.03.036     Document Type: Article

References (55)

1. Beuron F., Flynn T.C., Ma J., Kondo H., Zhang X., and Freemont P.S. Motions and negative cooperativity between p97 domains revealed by cryo-electron microscopy and quantised elastic deformational model. J. Mol. Biol. 327 (2003) 619-629
2. Beyer A. Sequence analysis of the AAA protein family. Protein Sci. 6 (1997) 2043-2058
3. Bienvenut W.V., Deon C., Pasquarello C., Campbell J.M., Sanchez J.C., Vestal M.L., and Hochstrasser D.F. Matrix-assisted laser desorption/ionization-tandem mass spectrometry with high resolution and sensitivity for identification and characterization of proteins. Proteomics 2 (2002) 868-876
4. Bowen M.E., Weninger K., Ernst J., Chu S., and Brunger A.T. Single-molecule studies of synaptotagmin and complexin binding to the SNARE complex. Biophys. J. 89 (2005) 690-702
5. Christianson J.C., and Green W.N. Regulation of nicotinic receptor expression by the ubiquitin-proteasome system. EMBO J. 23 (2004) 4156-4165
6. Dalal S., Rosser M.F., Cyr D.M., and Hanson P.I. Distinct roles for the AAA ATPases NSF and p97 in the secretory pathway. Mol. Biol. Cell 15 (2004) 637-648
7. Davies J.M., Tsuruta H., May A.P., and Weis W.I. Conformational changes of p97 during nucleotide hydrolysis determined by small-angle X-ray scattering. Structure (Camb) 13 (2005) 183-195
8. DeLaBarre B., and Brunger A.T. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nat. Struct. Biol. 10 (2003) 856-863
9. DeLaBarre B., and Brunger A.T. Nucleotide dependent motion and mechanism of action of p97/VCP. J. Mol. Biol. 347 (2005) 437-452
10. Ernst J.A., and Brunger A.T. High resolution structure, stability, and synaptotagmin binding of a truncated neuronal SNARE complex. J. Biol. Chem. 278 (2003) 8630-8636
11. Feiler H.S., Desprez T., Santoni V., Kronenberger J., Caboche M., and Traas J. The higher plant Arabidopsis thaliana encodes a functional CDC48 homologue which is highly expressed in dividing and expanding cells. EMBO J. 14 (1995) 5626-5637
12. Fiebiger E., Hirsch C., Vyas J.M., Gordon E., Ploegh H.L., and Tortorella D. Dissection of the dislocation pathway for type I membrane proteins with a new small molecule inhibitor, eeyarestatin. Mol. Biol. Cell 15 (2004) 1635-1646
13. Frohlich K.U., Fries H.W., Rudiger M., Erdmann R., Botstein D., and Mecke D. Yeast cell cycle protein CDC48p shows full-length homology to the mammalian protein VCP and is a member of a protein family involved in secretion, peroxisome formation, and gene expression. J. Cell Biol. 114 (1991) 443-453
14. Greene Jr. R.F., and Pace C.N. Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and beta-lactoglobulin. J. Biol. Chem. 249 (1974) 5388-5393
15. Han W., Rhee J.S., Maximov A., Lao Y., Mashimo T., Rosenmund C., and Südhof T.C. N-glycosylation is essential for vesicular targeting of synaptotagmin 1. Neuron 41 (2004) 85-99
16. Hinnerwisch J., Reid B.G., Fenton W.A., and Horwich A.L. Roles of the N-domains of the ClpA unfoldase in binding substrate proteins and in stable complex formation with the ClpP protease. J. Biol. Chem. 280 (2005) 40838-40844
17. Huppa J.B., and Ploegh H.L. The alpha chain of the T cell antigen receptor is degraded in the cytosol. Immunity 7 (1997) 113-122
18. Huyton T., Pye V.E., Briggs L.C., Flynn T.C., Beuron F., Kondo H., Ma J., Zhang X., and Freemont P.S. The crystal structure of murine p97/VCP at 3.6Å. J. Struct. Biol. 144 (2003) 337-348
19. Jarosch E., Taxis C., Volkwein C., Bordallo J., Finley D., Wolf D.H., and Sommer T. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 4 (2002) 134-139
20. Jiménez C.R., Huang L., Qiu Y., and Burlingame A.L. In-gel digestion of proteins for MALDI-MS fingerprint mapping. In: Chanda V.B. (Ed). Current Protocols in Protein Science (1998), John Wiley & Sons, New York 16.4.1-16.4.5
21. Kojima S., Vignjevic D., and Borisy G.G. Improved silencing vector co-expressing GFP and small hairpin RNA. Biotechniques 36 (2004) 74-79
22. Kopito R.R. ER quality control: the cytoplasmic connection. Cell 88 (1997) 427-430
23. Kozutsumi Y., Segal M., Normington K., Gething M.J., and Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332 (1988) 462-464
24. Lamb J.R., Fu V., Wirtz E., and Bangs J.D. Functional analysis of the trypanosomal AAA protein TbVCP with trans-dominant ATP hydrolysis mutants. J. Biol. Chem. 276 (2001) 21512-21520
25. Lee R.J., Liu C.W., Harty C., McCracken A.A., Latterich M., Romisch K., DeMartino G.N., Thomas P.J., and Brodsky J.L. Uncoupling retro-translocation and degradation in the ER-associated degradation of a soluble protein. EMBO J. 23 (2004) 2206-2215
26. Lilley B.N., and Ploegh H.L. A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429 (2004) 834-840
27. Lum R., Tkach J.M., Vierling E., and Glover J.R. Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J. Biol. Chem. 279 (2004) 29139-29146
28. Lupas A.N., and Martin J. AAA proteins. Curr. Opin. Struct. Biol. 12 (2002) 746-753
29. Mason P.E., Neilson G.W., Dempsey C.E., Barnes A.C., and Cruickshank J.M. The hydration structure of guanidinium and thiocyanate ions: implications for protein stability in aqueous solution. Proc. Natl. Acad. Sci. USA 100 (2003) 4557-4561
30. Meyer H.H., Kondo H., and Warren G. The p47 co-factor regulates the ATPase activity of the membrane fusion protein, p97. FEBS Lett. 437 (1998) 255-257
31. Meyer H.H., Shorter J.G., Seemann J., Pappin D., and Warren G. A complex of mammalian ufd1 and npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways. EMBO J. 19 (2000) 2181-2192
32. Miller, K.G. (1993). The proteins of synaptic vesicles: descriptive and functional studies. PhD thesis, Stanford University, Stanford, California.
33. Neet K.E. Cooperativity in enzyme function: equilibrium and kinetic aspects. In: Purich D.L. (Ed). Contemporary Enzyme Kinetics and Mechanism (1996), Academic Press, San Diego 133-182
34. +: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9 (1999) 27-43
35. Ogura T., Whiteheart S.W., and Wilkinson A.J. Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA(+) ATPases. J. Struct. Biol. 146 (2004) 106-112
36. Pinter M., Jekely G., Szepesi R.J., Farkas A., Theopold U., Meyer H.E., Lindholm D., Nassel D.R., Hultmark D., and Friedrich P. TER94, a Drosophila homolog of the membrane fusion protein CDC48/p97, is accumulated in nonproliferating cells: in the reproductive organs and in the brain of the imago. Insect Biochem. Mol. Biol. 28 (1998) 91-98
37. Rabinovich E., Kerem A., Frohlich K.U., Diamant N., and Bar-Nun S. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 22 (2002) 626-634
38. Roggy J.L., and Bangs J.D. Molecular cloning and biochemical characterization of a VCP homolog in African trypanosomes. Mol. Biochem. Parasitol. 98 (1999) 1-15
39. Rumpf S., and Jentsch S. Functional division of substrate processing cofactors of the ubiquitin-selective Cdc48 chaperone. Mol. Cell 21 (2006) 261-269
40. Sinz A. Chemical cross-linking and mass spectrometry for mapping three-dimensional structures of proteins and protein complexes. J. Mass Spectrom. 38 (2003) 1225-1237
41. Song C., Wang Q., and Li C.C. 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 (2003) 3648-3655
42. Sousa M.C., Trame C.B., Tsuruta H., Wilbanks S.M., Reddy V.S., and McKay D.B. Crystal and solution structures of an HslUV protease-chaperone complex. Cell 103 (2000) 633-643
43. 2A domains of synaptotagmins. Biochemistry 39 (2000) 2940-2949
44. 2+/phospholipid-binding fold. Cell 80 (1995) 929-938
45. Tiwari S., and Weissman A.M. Endoplasmic reticulum (ER)-associated degradation of T cell receptor subunits: involvement of ER-associated ubiquitin-conjugating enzymes (E2s). J. Biol. Chem. 276 (2001) 16193-16200
46. Wang Q., Song C., and Li C.C. Hexamerization of p97-VCP is promoted by ATP binding to the D1 domain and required for ATPase and biological activities. Biochem. Biophys. Res. Commun. 300 (2003) 253-260
47. Webb M.R. A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc. Natl. Acad. Sci. USA 89 (1992) 4884-4887
48. Weibezahn J., Tessarz P., Schlieker C., Zahn R., Maglica Z., Lee S., Zentgraf H., Weber-Ban E.U., Dougan D.A., Tsai F.T., et al. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119 (2004) 653-665
49. Wojcik C., Yano M., and DeMartino G.N. RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. J. Cell Sci. 117 (2004) 281-292
50. Ye Y., Meyer H.H., and Rapoport T.A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414 (2001) 652-656
51. Ye Y.H., Shibata Y., Yun C., Ron D., and Rapoport T.A. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429 (2004) 841-847
52. Yu H., and Kopito R.R. The role of multiubiquitination in dislocation and degradation of the alpha subunit of the T cell antigen receptor. J. Biol. Chem. 274 (1999) 36852-36858
53. Yu H., Kaung G., Kobayashi S., and Kopito R.R. Cytosolic degradation of T-cell receptor alpha chains by the proteasome. J. Biol. Chem. 272 (1997) 20800-20804
54. Zalk R., and Shoshan-Barmatz V. ATP-binding sites in brain p97/VCP (valosin-containing protein), a multifunctional AAA ATPase. Biochem. J. 374 (2003) 473-480
55. Zhong X., Shen Y., Ballar P., Apostolou A., Agami R., and Fang S. AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J. Biol. Chem. 279 (2004) 45676-45684