Role of the D1-D2 Linker of Human VCP/p97 in the Asymmetry and ATPase Activity of the D1-domain

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Tang, Wai Kwan ^a   Xia, Di ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CDC48 PROTEIN; CELL CYCLE PROTEIN; PEPTIDE FRAGMENT; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; CHEMISTRY; CONSERVED SEQUENCE; ENZYME ACTIVATION; HUMAN; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN SUBUNIT;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CONSERVED SEQUENCE; ENZYME ACTIVATION; HUMANS; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS;

EID: 84956658622     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20037     Document Type: Article

References (34)

1. Meyer, H. & Weihl, C. C. The VCP/p97 system at a glance: connecting cellular function to disease pathogenesis. J Cell Sci 127, 3877-83 (2014).
2. DeLaBarre, B. & Brunger, A. T. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nat Struc Biol 10, 856-863 (2003).
3. Davies, J. M., Brunger, A. T. & Weis, W. I. Improved Structures of Full-Length p97, an AAA ATPase: Implications for Mechanisms of Nucleotide-Dependent Conformational Change. Structure 16, 715-26 (2008).
4. Huyton, T. et al. The crystal structure of murine p97/VCP at 3.6 Å. J Struc Biol 144, 337-348 (2003).
5. Tang, W. K. et al. A novel ATP-dependent conformation in p97 N-D1 fragment revealed by crystal structures of disease-related mutants. Embo J 29, 2217-29 (2010).
6. Tang, W. K. & Xia, D. Altered intersubunit communication is the molecular basis for functional defects of pathogenic p97 mutants. J Biol Chem 288, 36624-35 (2013).
7. Hanzelmann, P. & Schindelin, H. The structural and functional basis of the p97/valosin-containing protein (VCP)-interacting motif (VIM): mutually exclusive binding of cofactors to the N-terminal domain of p97. J Biol Chem 286, 38679-90 (2011).
8. Davies, J. M., Tsuruta, H., May, A. P. & Weis, W. I. Conformational changes of p97 during nucleotide hydrolysis determined by small-angle X-Ray scattering. Structure 13, 183-95 (2005).
9. Dreveny, I. et al. Structural basis of the interaction between the AAA ATPase p97/VCP and its adaptor protein p47. Embo J 23, 1030-9 (2004).
10. Zhang, X. et al. Structure of the AAA ATPase p97. Mol Cell 6, 1473-1484 (2000).
11. Song, C., Wang, Q. & 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, 3648-55 (2003).
12. Ye, Y., Meyer, H. H. & Rapoport, T. A. 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 (2003).
13. Chou, T. F. et al. Specific inhibition of p97/VCP ATPase and kinetic analysis demonstrate interaction between D1 and D2 ATPase domains. J Mol Biol 426, 2886-99 (2014).
14. Tang, W. K. & Xia, D. IBMPFD and p97, the structural and molecular basis for functional disruption. in Neuromuscular Disorders 155-174 (InTech, 2012).
15. Karata, K., Inagawa, T., Wilkinson, A. J., Tatsuta, T. & Ogura, T. Dissecting the role of a conserved motif (the second region of homology) in the AAA family of ATPases. Site-directed mutagenesis of the ATP-dependent protease FtsH. Journal of Biological Chemistry 274, 26225-26232 (1999).
16. Stinson, B. M., Baytshtok, V., Schmitz, K. R., Baker, T. A. & Sauer, R. T. Subunit asymmetry and roles of conformational switching in the hexameric AAA+ ring of ClpX. Nat Struct Mol Biol 22, 411-6 (2015).
17. Glynn, S. E., Martin, A., Nager, A. R., Baker, T. A. & Sauer, R. T. Structures of asymmetric ClpX hexamers reveal nucleotidedependent motions in a AAA+ protein-unfolding machine. Cell 139, 744-56 (2009).
18. Guo, F., Maurizi, M. R., Esser, L. & Xia, D. Crystal structure of ClpA, an HSP100 chaperone and regulator of ClpAP protease. J Biol Chem 277, 46743-46752 (2002).
19. Lee, S. et al. The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115, 229-240 (2003).
20. Sysoeva, T. A., Chowdhury, S., Guo, L. & Nixon, B. T. Nucleotide-induced asymmetry within ATPase activator ring drives sigma54-RNAP interaction and ATP hydrolysis. Genes Dev 27, 2500-11 (2013).
21. DeLaBarre, B. & Brunger, A. T. Nucleotide dependent motion and mechanism of action of p97/VCP. J Mol Biol 347, 437-452 (2005).
22. Briggs, L. C. et al. Analysis of nucleotide binding to P97 reveals the properties of a tandem AAA hexameric ATPase. J Biol Chem 283, 13745-52 (2008).
23. Tang, W. K. & Xia, D. Structural and functional deviations in disease-associated p97 mutants. J Struct Biol 179, 83-92 (2012).
24. Wang, Q. et al. Multifunctional roles of the conserved Arg residues in the second region of homology of p97/valosin-containing protein. J Biol Chem 280, 40515-23 (2005).
25. Li, G., Huang, C., Zhao, G. & Lennarz, W. J. Interprotomer motion-transmission mechanism for the hexameric AAA ATPase p97. Proc Natl Acad Sci USA 109, 3737-41 (2012).
26. Hess, H. H. & Derr, J. E. Assay of inorganic and organic phosphorus in the 0.1-5 nanomole range. Anal Biochem 63, 607-13 (1975).
27. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S. & Candia, O. A. An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100, 95-7 (1979).
28. DeLaBarre, B. & Brunger, A. T. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nat Struct Biol 10, 856-63 (2003).
29. Otwinowski, Z. & Minor, W. Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods in Enzymology 276, 307-326 (1997).
30. Strong, M. et al. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103, 8060-5 (2006).
31. Vagin, A. & Teplyakov, A. MOLREP: an automated program for molecular replacement. Journal of Applied Crystallography 30, 1022-1025 (1997).
32. CCP4. Collaborative Computational Project, Number 4, 1994. The CCP4 Suit: Programs for Protein Crystallography. Acta Crystallographica D50, 760-763 (1994).
33. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of Macromolecular Structures by the Maximum-likelihood Method. Acta Crystallographica D53, 240-255 (1997).
34. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Cryst. D60, 2126-2132 (2006).