Structural and functional implications of phosphorylation and acetylation in the regulation of the AAA+ protein p97

Biochemistry and Cell Biology

Volumn 88, Issue 1, 2010, Pages 41-48

  Ewens, Caroline A ^a   Kloppsteck, Patrik ^a   Förster, Andreas ^a   Zhang, Xiaodong ^a   Freemont, Paul S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Acetylation; P97; Phosphorylation

Indexed keywords

ADAPTOR PROTEINS; CELLULAR PROCESS; MEMBRANE FUSION; MISFOLDED PROTEINS; P97; POST-TRANSLATIONAL MODIFICATIONS; REGULATORY MECHANISM; SUBCELLULAR LOCALIZATIONS;

ACETYLATION; CELL MEMBRANES; LAWS AND LEGISLATION; TRANSCRIPTION FACTORS;

PHOSPHORYLATION;

ADAPTOR PROTEIN; ADENOSINE TRIPHOSPHATASE; HISTONE DEACETYLASE 6; PROTEIN P97; TRANSCRIPTION FACTOR; VALOSIN CONTAINING PROTEIN;

ACETYLATION; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONFERENCE PAPER; ENZYME ACTIVITY; MEMBRANE FUSION; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REGULATORY MECHANISM;

ACETYLATION; ADENOSINE TRIPHOSPHATASES; CELL CYCLE PROTEINS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HUMANS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 75349101096     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O09-128     Document Type: Conference Paper

References (45)

1. An, Y., Chen, C.Y., Moyer, B., Rotkiewicz, P., Elsliger, M.A., Godzik, A., et al. 2009. Structural and functional analysis of the globular head domain of p115 provides insight into membrane tethering. J. Mol. Biol. 391(1): 26-41. doi:10.1016/j.jmb.2009. 04.062. PMID:19414022.
2. Bays, N.W., Wilhovsky, S.K., Goradia, A., Hodgkiss-Harlow, K., and Hampton, R.Y. 2001. HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol. Biol. Cell, 12(12): 4114-4128. PMID:11739805.
3. Bertram, C., von Neuhoff, N., Skawran, B., Steinemann, D., Schlegelberger, B., and Hass, R. 2008. The differentiation/retrodifferentiation program of human U937 leukemia cells is accompanied by changes of VCP/p97. BMC Cell Biol. 9(1): 12. doi:10.1186/1471-2121-9-12. PMID:18279508.
4. Conti, E., Uy, M., Leighton, L., Blobel, G., and Kuriyan, J. 1998. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell, 94(2): 193-204. doi:10.1016/S0092-8674(00)81419-1. PMID:9695948.
5. Dai, R.M., Chen, E., Longo, D.L., Gorbea, C.M., and Li, C.C. 1998. Involvement of valosin-containing protein, an ATPase Co-purified with IkappaBalpha and 26 S proteasome, in ubiquitin-proteasome-mediated degradation of IkappaBalpha. J. Biol. Chem. 273(6): 3562-3573. doi:10.1074/jbc.273.6. 3562. PMID: 9452483.
6. Davies, J.M., Brunger, A.T., and Weis, W.I. 2008. Improved structures of full-length p97, an AAA ATPase: implications for mechanisms of nucleotide-dependent conformational change. Structure, 16(5): 715-726. doi:10.1016/j.str.2008.02.010. PMID: 18462676.
7. Egerton, M., and Samelson, L.E. 1994. Biochemical characterization of valosin-containing protein, a protein tyrosine kinase substrate in hematopoietic cells. J. Biol. Chem. 269(15): 11435-11441. PMID:8157674.
8. Egerton, M., Ashe, O.R., Chen, D., Druker, B.J., Burgess, W.H., and Samelson, L.E. 1992. VCP, the mammalian homolog of cdc48, is tyrosine phosphorylated in response to T cell antigen receptor activation. EMBO J. 11(10): 3533-3540. PMID: 1382975.
9. Ficarro, S., Chertihin, O., Westbrook, V.A., White, F., Jayes, F., Kalab, P., et al. 2003. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinaseanchoring protein 3 and valosin-containing protein/p97 during capacitation. J. Biol. Chem. 278(13): 11579-11589. doi:10. 1074/jbc.M202325200. PMID:12509440.
10. Gallinari, P., Di Marco, S., Jones, P., Pallaoro, M., and Steinkühler, C. 2007. HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics. Cell Res. 17(3): 195-211. PMID:17325692.
11. Hozumi, A., Padma, P., Toda, T., Ide, H., and Inaba, K. 2008. Molecular characterization of axonemal proteins and signaling molecules responsible for chemoattractant-induced sperm activation in Ciona intestinalis. Cell Motil. Cytoskeleton, 65(3): 249-267. doi:10.1002/cm.20258. PMID:18189282.
12. Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., et al. 2002. HDAC6 is a microtubule-associated deacetylase. Nature, 417(6887): 455-458. doi:10.1038/417455a. PMID:12024216.
13. Huber, A.H., Nelson, W.J., and Weis, W.I. 1997. Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell, 90(5): 871-882. doi:10.1016/S0092-8674(00)80352-9. PMID:9298899.
14. Humphreys, D., Hume, P.J., and Koronakis, V. 2009. The Salmonella effector SptP dephosphorylates host AAA+ ATPase VCP to promote development of its intracellular replicative niche. Cell Host Microbe, 5(3): 225-233. doi:10.1016/j.chom.2009.01.010. PMID:19286132.
15. Huyton, T., Pye, V.E., Briggs, L.C., Flynn, T.C., Beuron, F., Kondo, H., et al. 2003. The crystal structure of murine p97/VCP at 3.6A. J. Struct. Biol. 144(3): 337-348. doi:10.1016/j. jsb.2003.10.007. PMID:14643202.
16. Imamura, S., Ojima, N., and Yamashita, M. 2003. Cold-inducible expression of the cell division cycle gene CDC48 and its promotion of cell proliferation during cold acclimation in zebrafish cells. FEBS Lett. 549(1-3): 14-20. doi:10.1016/S0014-5793(03) 00723-3. PMID:12914916.
17. Iyer, L.M., Koonin, E.V., and Aravind, L. 2004. Novel predicted peptidases with a potential role in the ubiquitin signaling pathway. Cell Cycle, 3(11): 1440-1450. PMID:15483401.
18. Kano, F., Tanaka, A.R., Yamauchi, S., Kondo, H., and Murata, M. 2004. Cdc2 kinase-dependent disassembly of endoplasmic reticulum (ER) exit sites inhibits ER-to-Golgi vesicular transport during mitosis. Mol. Biol. Cell, 15(9): 4289-4298. doi:10.1091/mbc.E03-11-0822. PMID:15254263.
19. Kawaguchi, Y., Kovacs, J.J., McLaurin, A., Vance, J.M., Ito, A., and Yao, T.P. 2003. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell, 115(6): 727-738. doi:10.1016/S0092-8674(03) 00939-5. PMID:14675537.
20. Klein, J.B., Barati, M.T., Wu, R., Gozal, D., Sachleben, L.R., Jr., Kausar, H., et al. 2005. Akt-mediated valosin-containing protein 97 phosphorylation regulates its association with ubiquitinated proteins. J. Biol. Chem. 280(36): 31870-31881. doi:10.1074/jbc. M501802200. PMID:16027165.
21. Kondo, H., Rabouille, C., Newman, R., Levine, T.P., Pappin, D., Freemont, P., and Warren, G. 1997. p47 is a cofactor for p97-mediated membrane fusion. Nature, 388(6637): 75-78. doi:10. 1038/40411. PMID:9214505.
22. Lavoie, C., Chevet, E., Roy, L., Tonks, N.K., Fazel, A., Posner, B.I., et al. 2000. Tyrosine phosphorylation of p97 regulates transitional endoplasmic reticulum assembly in vitro. Proc. Natl. Acad. Sci. U.S.A. 97(25): 13637-13642. doi:10.1073/pnas. 240278097. PMID:11087817.
23. Li, G., Zhao, G., Schindelin, H., and Lennarz, W.J. 2008. Tyrosine phosphorylation of ATPase p97 regulates its activity during ERAD. Biochem. Biophys. Res. Commun. 375(2): 247-251. doi:10.1016/j.bbrc.2008.08.018. PMID:18706391.
24. Livingstone, M., Ruan, H., Weiner, J., Clauser, K.R., Strack, P., Jin, S., et al. 2005. Valosin-containing protein phosphorylation at Ser784 in response to DNA damage. Cancer Res. 65(17): 7533-7540. PMID:16140914.
25. Madeo, F., Schlauer, J., Zischka, H., Mecke, D., and Fröhlich, K.U. 1998. Tyrosine phosphorylation regulates cell cycle-dependent nuclear localization of Cdc48p. Mol. Biol. Cell, 9(1): 131-141. PMID:9436996.
26. Madsen, L., Seeger, M., Semple, C.A., and Hartmann-Petersen, R. 2009. New ATPase regulators-p97 goes to the PUB. Int. J. Biochem. Cell Biol., In press. doi:10.1016/j.biocel.2009.05.017. PMID:19497384.
27. Matsuyama, A., Shimazu, T., Sumida, Y., Saito, A., Yoshimatsu, Y., Seigneurin-Berny, D., et al. 2002. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21(24): 6820-6831. doi:10.1093/emboj/cdf682. PMID:12486003.
28. Meyer, H., and Popp, O. 2008. Role(s) of Cdc48/p97 in mitosis. Biochem. Soc. Trans. 36(Pt 1): 126-130. doi:10.1042/BST0360126. PMID:18208399.
29. Mori-Konya, C., Kato, N., Maeda, R., Yasuda, K., Higashimae, N., Noguchi, M., et al. 2009. p97/valosin-containing protein (VCP) is highly modulated by phosphorylation and acetylation. Genes Cells, 14(4): 483-497. doi:10.1111/j.1365-2443.2009.01286.x. PMID:19335618.
30. Mullally, J.E., Chernova, T., and Wilkinson, K.D. 2006. Doa1 is a Cdc48 adapter that possesses a novel ubiquitin binding domain. Mol. Cell. Biol. 26(3): 822-830. doi:10.1128/MCB.26.3.822-830.2006. PMID:16428438.
31. Peifer, M., Berg, S., and Reynolds, A.B. 1994. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell, 76(5): 789-791. doi:10.1016/0092-8674(94)90353-0. PMID: 7907279.
32. Qiu, L., Pashkova, N., Walker, J.R., Winistorfer, S., Allali-Hassani, A., Akutsu, M., et al. 2009. Structure and function of the PLAA/Doa1/Ufd3-p97/Cdc48 complex. J. Biol. Chem. Epub ahead of print.
33. Roy, L., Bergeron, J.J., Lavoie, C., Hendriks, R., Gushue, J., Fazel, A., et al. 2000. Role of p97 and syntaxin 5 in the assembly of transitional endoplasmic reticulum. Mol. Biol. Cell, 11(8): 2529-2542. PMID:10930451.
34. Seigneurin-Berny, D., Verdel, A., Curtet, S., Lemercier, C., Garin, J., Rousseaux, S., and Khochbin, S. 2001. Identification of components of the murine histone deacetylase 6 complex: link between acetylation and ubiquitination signaling pathways. Mol. Cell. Biol. 21(23): 8035-8044. doi:10.1128/MCB.21.23.8035-8044.2001. PMID:11689694.
35. Striegl, H., Roske, Y., Kümmel, D., Heinemann, U., and Hofmann, A. 2009. Unusual armadillo fold in the human general vesicular transport factor p115. PLoS One, 4(2): e4656. doi:10.1371/journal.pone.0004656. PMID:19247479.
36. Suzuki, T., Park, H., Till, E.A., and Lennarz, W.J. 2001. The PUB domain: a putative protein-protein interaction domain implicated in the ubiquitin-proteasome pathway. Biochem. Biophys. Res. Commun. 287(5): 1083-1087. doi:10.1006/bbrc.2001.5688. PMID:11587532.
37. Uchiyama, K., Jokitalo, E., Lindman, M., Jackman, M., Kano, F., Murata, M., et al. 2003. The localization and phosphorylation of p47 are important for Golgi disassembly-assembly during the cell cycle. J. Cell Biol. 161(6): 1067-1079. doi:10.1083/jcb. 200303048. PMID:12810701.
38. Uchiyama, K., Totsukawa, G., Puhka, M., Kaneko, Y., Jokitalo, E., Dreveny, I., et al. 2006. p37 is a p97 adaptor required for Golgi and ER biogenesis in interphase and at the end of mitosis. Dev. Cell, 11(6): 803-816. doi:10.1016/j.devcel.2006.10.016. PMID: 17141156.
39. Vandermoere, F., El Yazidi-Belkoura, I., Slomianny, C., Demont, Y., Bidaux, G., Adriaenssens, E., et al. 2006. The valosin-containing protein (VCP) is a target of Akt signaling required for cell survival. J. Biol. Chem. 281(20): 14307-14313. doi:10. 1074/jbc.M510003200. PMID:16551632.
40. Wang, Q., Song, C., and Li, C.C. 2004. Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions. J. Struct. Biol. 146(1-2): 44-57. doi:10. 1016/j.jsb.2003.11.014. PMID:15037236.
41. Ye, Y. 2006. Diverse functions with a common regulator: ubiquitin takes command of an AAA ATPase. J. Struct. Biol. 156(1): 29-40. PMID:16529947.
42. Yeung, H.O., Kloppsteck, P., Niwa, H., Isaacson, R.L., Matthews, S., Zhang, X., and Freemont, P.S. 2008. Insights into adaptor binding to the AAA protein p97. Biochem. Soc. Trans. 36(Pt 1): 62-67. doi:10.1042/ BST0360062. PMID:18208387.
43. Zhang, S.H., Liu, J., Kobayashi, R., and Tonks, N.K. 1999. Identification of the cell cycle regulator VCP (p97/CDC48) as a substrate of the band 4.1-related protein-tyrosine phosphatase PTPH1. J. Biol. Chem. 274(25): 17806-17812. doi:10.1074/jbc. 274.25.17806. PMID:10364224.
44. Zhang, H., Wang, Q., Kajino, K., and Greene, M.I. 2000. VCP, a weak ATPase involved in multiple cellular events, interacts physically with BRCA1 in the nucleus of living cells. DNA Cell Biol. 19(5): 253-263. doi:10.1089/10445490050021168. PMID: 10855792.
45. Zhao, G., Zhou, X., Wang, L., Li, G., Schindelin, H., and Lennarz, W.J. 2007. Studies on peptide:N-glycanase-p97 interaction suggest that p97 phosphorylation modulates endoplasmic reticulumassociated degradation. Proc. Natl. Acad. Sci. U.S.A. 104(21): 8785-8790. doi:10.1073/pnas.0702966104. PMID:17496150.