Atomic structure of dual-specificity phosphatase 26, a novel p53 phosphatase

Biochemistry

Volumn 52, Issue 5, 2013, Pages 938-948

  Lokareddy, Ravi Kumar ^a   Bhardwaj, Anshul ^a   Cingolani, Gino ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE POCKET; BASIC SURFACE; BINDING LOOP; CATALYTIC CYSTEINES; CONFORMATIONAL CHANGE; GEL-FILTRATION CHROMATOGRAPHY; HYDRODYNAMIC RADIUS; INACTIVE MUTANTS; MAIN CHAINS; MONOMERIC PROTEINS; N-TERMINALS; NEUROBLASTOMAS; PROTEIN-TYROSINE PHOSPHATASE; SEDIMENTATION ANALYSIS; SIDE-CHAINS; STRUCTURAL CHARACTERIZATION; TRANSACTIVATION DOMAIN; VACCINIA VIRUS; WATER MOLECULE;

AMINO ACIDS; BIOACTIVITY; CRYSTAL ATOMIC STRUCTURE; GEL PERMEATION CHROMATOGRAPHY; PHOSPHORYLATION; PROTEINS; VIRUSES;

PHOSPHATASES;

DUAL SPECIFICITY PHOSPHATASE 26; PHOSPHATASE; UNCLASSIFIED DRUG; WATER;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STRUCTURE; GEL FILTRATION CHROMATOGRAPHY; HYDRODYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; SEDIMENTATION RATE; VACCINIA VIRUS;

CATALYTIC DOMAIN; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; DUAL-SPECIFICITY PHOSPHATASES; ENZYME ACTIVATION; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; MODELS, MOLECULAR; NEUROBLASTOMA; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; TUMOR SUPPRESSOR PROTEIN P53; VACCINIA VIRUS;

EID: 84873371088     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301476m     Document Type: Article

References (56)

1. Denu, J. M., Stuckey, J. A., Saper, M. A., and Dixon, J. E. (1996) Form and function in protein dephosphorylation Cell 87, 361-364 (Pubitemid 26374310)
2. Zhang, Z. Y. (2002) Protein tyrosine phosphatases: Structure and function, substrate specificity, and inhibitor development Annu. Rev. Pharmacol. Toxicol. 42, 209-234
3. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Osterman, A., Godzik, A., Hunter, T., Dixon, J., and Mustelin, T. (2004) Protein tyrosine phosphatases in the human genome Cell 117, 699-711 (Pubitemid 38748887)
4. Ducruet, A. P., Vogt, A., Wipf, P., and Lazo, J. S. (2005) Dual specificity protein phosphatases: Therapeutic targets for cancer and Alzheimer's disease Annu. Rev. Pharmacol. Toxicol. 45, 725-750 (Pubitemid 40261823)
5. Patterson, K. I., Brummer, T., O'Brien, P. M., and Daly, R. J. (2009) Dual-specificity phosphatases: Critical regulators with diverse cellular targets Biochem. J. 418, 475-489
6. Guan, K. L., Broyles, S. S., and Dixon, J. E. (1991) A Tyr/Ser protein phosphatase encoded by vaccinia virus Nature 350, 359-362 (Pubitemid 21912232)
7. Phan, J., Tropea, J. E., and Waugh, D. S. (2007) Structure-assisted discovery of Variola major H1 phosphatase inhibitors Acta Crystallogr. D63, 698-704 (Pubitemid 46795121)
8. Jackson, M. D. and Denu, J. M. (2001) Molecular reactions of protein phosphatases: Insights from structure and chemistry Chem. Rev. 101, 2313-2340 (Pubitemid 35373021)
9. Alonso, A., Burkhalter, S., Sasin, J., Tautz, L., Bogetz, J., Huynh, H., Bremer, M. C., Holsinger, L. J., Godzik, A., and Mustelin, T. (2004) The minimal essential core of a cysteine-based protein-tyrosine phosphatase revealed by a novel 16-kDa VH1-like phosphatase, VHZ J. Biol. Chem. 279, 35768-35774 (Pubitemid 39100582)
10. Maehama, T., Taylor, G. S., and Dixon, J. E. (2001) PTEN and myotubularin: Novel phosphoinositide phosphatases Annu. Rev. Biochem. 70, 247-279 (Pubitemid 32662211)
11. Deshpande, T., Takagi, T., Hao, L., Buratowski, S., and Charbonneau, H. (1999) Human PIR1 of the protein-tyrosine phosphatase superfamily has RNA 5′-triphosphatase and diphosphatase activities J. Biol. Chem. 274, 16590-16594
12. Tagliabracci, V. S., Turnbull, J., Wang, W., Girard, J. M., Zhao, X., Skurat, A. V., Delgado-Escueta, A. V., Minassian, B. A., Depaoli-Roach, A. A., and Roach, P. J. (2007) Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo Proc. Natl. Acad. Sci. U.S.A. 104, 19262-19266
13. Koksal, A. C., Nardozzi, J. D., and Cingolani, G. (2009) Dimeric quaternary structure of the prototypical dual specificity phosphatase VH1 J. Biol. Chem. 284, 10129-10137
14. Koksal, A. C. and Cingolani, G. (2011) Dimerization of Vaccinia Virus VH1 Is Essential for Dephosphorylation of STAT1 at Tyrosine 701 J. Biol. Chem. 286, 14373-14382
15. Vasudevan, S. A., Skoko, J., Wang, K., Burlingame, S. M., Patel, P. N., Lazo, J. S., Nuchtern, J. G., and Yang, J. (2005) MKP-8, a novel MAPK phosphatase that inhibits p38 kinase Biochem. Biophys. Res. Commun. 330, 511-518 (Pubitemid 40417674)
16. Takagaki, K., Shima, H., Tanuma, N., Nomura, M., Satoh, T., Watanabe, M., and Kikuchi, K. (2007) Characterization of a novel low-molecular-mass dual specificity phosphatase-4 (LDP-4) expressed in brain Mol. Cell. Biochem. 296, 177-184
17. Hu, Y. and Mivechi, N. F. (2006) Association and regulation of heat shock transcription factor 4b with both extracellular signal-regulated kinase mitogen-activated protein kinase and dual-specificity tyrosine phosphatase DUSP26 Mol. Cell. Biol. 26, 3282-3294
18. Wang, J. Y., Lin, C. H., Yang, C. H., Tan, T. H., and Chen, Y. R. (2006) Biochemical and biological characterization of a neuroendocrine-associated phosphatase J. Neurochem. 98, 89-101
19. Yu, W., Imoto, I., Inoue, J., Onda, M., Emi, M., and Inazawa, J. (2007) A novel amplification target, DUSP26, promotes anaplastic thyroid cancer cell growth by inhibiting p38 MAPK activity Oncogene 26, 1178-1187
20. Tanuma, N., Nomura, M., Ikeda, M., Kasugai, I., Tsubaki, Y., Takagaki, K., Kawamura, T., Yamashita, Y., Sato, I., Sato, M., Katakura, R., Kikuchi, K., and Shima, H. (2009) Protein phosphatase Dusp26 associates with KIF3 motor and promotes N-cadherin-mediated cell-cell adhesion Oncogene 28, 752-761
21. Shang, X., Vasudevan, S. A., Yu, Y., Ge, N., Ludwig, A. D., Wesson, C. L., Wang, K., Burlingame, S. M., Zhao, Y. J., Rao, P. H., Lu, X., Russell, H. V., Okcu, M. F., Hicks, M. J., Shohet, J. M., Donehower, L. A., Nuchtern, J. G., and Yang, J. (2010) Dual-specificity phosphatase 26 is a novel p53 phosphatase and inhibits p53 tumor suppressor functions in human neuroblastoma Oncogene 29, 4938-4946
22. Cabre, F., Canela, E. I., and Canela, M. A. (1989) Accuracy and precision in the determination of Stokes radii and molecular masses of proteins by gel filtration chromatography J. Chromatogr. 472, 347-356 (Pubitemid 19170251)
23. Lee, W. L., Ostap, E. M., Zot, H. G., and Pollard, T. D. (1999) Organization and ligand binding properties of the tail of Acanthamoeba myosin-IA. Identification of an actin-binding site in the basic (tail homology-1) domain J. Biol. Chem. 274, 35159-35171 (Pubitemid 129509572)
24. Bhardwaj, A., Olia, A. S., Walker-Kopp, N., and Cingolani, G. (2007) Domain organization and polarity of tail needle GP26 in the portal vertex structure of bacteriophage P22 J. Mol. Biol. 371, 374-387 (Pubitemid 47048275)
25. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
26. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
27. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132 (Pubitemid 41742764)
28. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2004) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
29. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255 (Pubitemid 27235885)
30. Collaborative Computational Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
31. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
32. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32, W665-W667 (Pubitemid 38997419)
33. Laskowski, R. A. (2009) PDBsum new things Nucleic Acids Res. 37, D355-D359
34. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
35. Ortega, A., Amoros, D., and Garcia de la Torre, J. (2011) Prediction of hydrodynamic and other solution properties of rigid proteins from atomic- and residue-level models Biophys. J. 101, 892-898
36. Lountos, G. T., Tropea, J. E., and Waugh, D. S. (2011) Structure of human dual-specificity phosphatase 27 at 2.38 Å resolution Acta Crystallogr. D67, 471-479
37. Yuvaniyama, J., Denu, J. M., Dixon, J. E., and Saper, M. A. (1996) Crystal structure of the dual specificity protein phosphatase VHR Science 272, 1328-1331 (Pubitemid 26199971)
38. Jeong, D. G., Yoon, T. S., Jung, S. K., Park, B. C., Park, H., Ryu, S. E., and Kim, S. J. (2011) Exploring binding sites other than the catalytic core in the crystal structure of the catalytic domain of MKP-4 Acta Crystallogr. D67, 25-31
39. Lee, C. W., Martinez-Yamout, M. A., Dyson, H. J., and Wright, P. E. (2010) Structure of the p53 transactivation domain in complex with the nuclear receptor coactivator binding domain of CREB binding protein Biochemistry 49, 9964-9971
40. Kruse, J. P. and Gu, W. (2009) Modes of p53 regulation Cell 137, 609-622
41. Levine, A. J. (1997) p53, the cellular gatekeeper for growth and division Cell 88, 323-331 (Pubitemid 27131374)
42. Meek, D. W. (2009) Tumour suppression by p53: A role for the DNA damage response? Nat. Rev. Cancer 9, 714-723
43. Dornan, D. and Hupp, T. R. (2001) Inhibition of p53-dependent transcription by BOX-I phospho-peptide mimetics that bind to p300 EMBO Rep. 2, 139-144 (Pubitemid 32229741)
44. Dornan, D., Shimizu, H., Perkins, N. D., and Hupp, T. R. (2003) DNA-dependent acetylation of p53 by the transcription coactivator p300 J. Biol. Chem. 278, 13431-13441 (Pubitemid 36800117)
45. Dornan, D., Shimizu, H., Burch, L., Smith, A. J., and Hupp, T. R. (2003) The proline repeat domain of p53 binds directly to the transcriptional coactivator p300 and allosterically controls DNA-dependent acetylation of p53 Mol. Cell. Biol. 23, 8846-8861 (Pubitemid 37433384)
46. Tweddle, D. A., Malcolm, A. J., Bown, N., Pearson, A. D., and Lunec, J. (2001) Evidence for the development of p53 mutations after cytotoxic therapy in a neuroblastoma cell line Cancer Res. 61, 8-13 (Pubitemid 32095689)
47. Maclaine, N. J. and Hupp, T. R. (2009) The regulation of p53 by phosphorylation: A model for how distinct signals integrate into the p53 pathway Aging 1, 490-502
48. Moll, U. M., Ostermeyer, A. G., Ahomadegbe, J. C., Mathieu, M. C., and Riou, G. (1995) p53 mediated tumor cell response to chemotherapeutic DNA damage: A preliminary study in matched pairs of breast cancer biopsies Hum. Pathol. 26, 1293-1301 (Pubitemid 26001589)
49. Moll, U. M., LaQuaglia, M., Benard, J., and Riou, G. (1995) Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors Proc. Natl. Acad. Sci. U.S.A. 92, 4407-4411
50. Vousden, K. H. and Lu, X. (2002) Live or let die: The cell's response to p53 Nat. Rev. Cancer 2, 594-604 (Pubitemid 37328926)
51. Liu, Y., Wang, Y., Wu, C., Liu, Y., and Zheng, P. (2006) Dimerization of laforin is required for its optimal phosphatase activity, regulation of GSK3β phosphorylation, and Wnt signaling J. Biol. Chem. 281, 34768-34774 (Pubitemid 46043246)
52. Berger, P., Schaffitzel, C., Berger, I., Ban, N., and Suter, U. (2003) Membrane association of myotubularin-related protein 2 is mediated by a pleckstrin homology-GRAM domain and a coiled-coil dimerization module Proc. Natl. Acad. Sci. U.S.A. 100, 12177-12182 (Pubitemid 37271534)
53. Camps, M., Nichols, A., Gillieron, C., Antonsson, B., Muda, M., Chabert, C., Boschert, U., and Arkinstall, S. (1998) Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase Science 280, 1262-1265 (Pubitemid 28269620)
54. Lazo, J. S. and Wipf, P. (2009) Phosphatases as targets for cancer treatment Curr. Opin. Invest. Drugs 10, 1297-1304
55. Bakan, A., Lazo, J. S., Wipf, P., Brummond, K. M., and Bahar, I. (2008) Toward a molecular understanding of the interaction of dual specificity phosphatases with substrates: Insights from structure-based modeling and high throughput screening Curr. Med. Chem. 15, 2536-2544
56. Ubersax, J. A. and Ferrell, J. E., Jr. (2007) Mechanisms of specificity in protein phosphorylation Nat. Rev. Mol. Cell Biol. 8, 530-541 (Pubitemid 46985383)