Specificity profiling of dual specificity phosphatase vaccinia VH1-related (VHR) reveals two distinct substrate binding modes

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6498-6510

  Luechapanichkul, Rinrada ^a   Chen, Xianwen ^a   Taha, Hashem A ^a   Vyas, Shubham ^a   Guan, Xiaoyan ^a   Freitas, Michael A ^b   Hadad, Christopher M ^a   Pei, Dehua ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE POCKET; BINDING MODES; CATALYTIC DOMAINS; CLASS I; CLASS II; COMBINATORIAL PEPTIDE LIBRARIES; CONSENSUS SEQUENCE; HYDROPHOBIC AMINO ACIDS; IN-VITRO; IN-VIVO; MOLECULAR MODELING STUDIES; N TERMINUS; PHOSPHOTYROSINE; PROTEIN SUBSTRATE; PROTEIN-TYROSINE PHOSPHATASE; SIDE-CHAINS; SITE DIRECTED MUTAGENESIS; SUBSTRATE BINDING; SUBSTRATE SPECIFICITY;

AMINO ACIDS; BINDING ENERGY; CARBOXYLATION; PEPTIDES; PHOSPHATASES;

SUBSTRATES;

CARBOXYLIC ACID; DUAL SPECIFICITY PHOSPHATASE; PHOSPHOTYROSINE; TYROSINE; UNCLASSIFIED DRUG; VACCINIA VH1 RELATED PHOSPHATASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; COMBINATORIAL LIBRARY; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROPHOBICITY; IN VITRO STUDY; MOLECULAR MODEL; PEPTIDE LIBRARY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN INTERACTION; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; DUAL SPECIFICITY PHOSPHATASE 3; HUMANS; MUTAGENESIS, SITE-DIRECTED; PEPTIDE LIBRARY; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

EID: 84874765509     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.449611     Document Type: Article

References (47)

1. Tiganis, T., and Bennett, A. M. (2007) Protein tyrosine phosphatase function: the substrate perspective. Biochem. J. 402, 1-15
2. Tonks, N. K., and Neel, B. G. (2001) Combinatorial control of the specificity of protein tyrosine phosphatases. Curr. Opin. Cell Biol. 13, 182-195
3. Zhang, Z.-Y., Maclean, D., McNamara, D. J., Sawyer, T. K., and Dixon, J. E. (1994) Protein tyrosine phosphatase substrate specificity: size and phosphotyrosine positioning requirements in peptide substrates. Biochemistry 33, 2285-2290
4. Vetter, S. W., Keng, Y.-F., Lawrence, D. S., and Zhang, Z.-Y. (2000) Assessment of protein-tyrosine phosphatase 1B substrate specificity using "inverse alanine scanning." J. Biol. Chem. 275, 2265-2268
5. Wälchli, S., Espanel, X., Harrenga, A., Rossi, M., Cesareni, G., and Hooft van Huijsduijnen, R. (2004) Probing protein-tyrosine phosphatase substrate specificity using a phosphotyrosine-containing phage library. J. Biol. Chem. 279, 311-318
6. Ren, L., Chen, X., Luechapanichkul, R., Selner, N. G., Meyer, T. M., Wavreille, A.-S., Chan, R., Iorio, C., Zhou, X., Neel, B. G., and Pei, D. (2011) Substrate specificity of protein tyrosine phosphatases 1B, RPTPα, SHP-1, and SHP-2. Biochemistry 50, 2339-2356
7. Bayon, Y., and Alonso, A. (2010) in Emerging Signaling Pathways in Tumor Biology (Lazo, P. A., ed) pp. 185-208, Transworld Research Network, Kerala, India
8. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., 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
9. Ishibashi, T., Bottaro, D. P., Chan, A., Miki, T., and Aaronson, S. A. (1992) Expression cloning of a human dual-specificity phosphatase. Proc. Natl. Acad. Sci. U.S.A. 89, 12170-12174
10. Rahmouni, S., Cerignoli, F., Alonso, A., Tsutji, T., Henkens, R., Zhu, C., Louis-dit-Sully, C., Moutschen, M., Jiang, W., and Mustelin, T. (2006) Loss of the VHR dual-specific phosphatase causes cell-cycle arrest and senescence. Nat. Cell Biol. 8, 524-531
11. Arnoldussen, Y. J., Lorenzo, P. I., Pretorius, M. E., Waehre, H., Risberg, B., Maelandsmo, G. M., Danielsen, H. E., and Saatcioglu, F. (2008) The mitogen- activated protein kinase phosphatase vaccinia H1-related protein inhibits apoptosis in prostate cancer cells and is overexpressed in prostate cancer. Cancer Res. 68, 9255-9264
12. Hao, L., and ElShamy, W. M. (2007) BRCA1-IRIS activates cyclin D1 expression in breast cancer cells by downregulating the JNK phosphatase DUSP3/VHR. Int. J. Cancer. 121, 39-46
13. Henkens, R., Delvenne, P., Arafa, M., Moutschen, M., Zeddou, M., Tautz, L., Boniver, J., Mustelin, T., and Rahmouni, S. (2008) Cervix carcinoma is associated with an up-regulation and nuclear localization of the dualspecificity protein phosphatase VHR. BMC Cancer 8, 147-155
14. Todd, J. L., Tanner, K. G., and Denu, J. M. (1999) Extracellular regulated kinases (ERK) 1 and ERK2 are authentic substrates for the dual-specificity protein-tyrosine phosphatase VHR. A novel role in down-regulating the ERK pathway. J. Biol. Chem. 274, 13271-13280
15. Todd, J. L., Rigas, J. D., Rafty, L. A., and Denu, J. M. (2002) Dual-specificity protein tyrosine phosphatase VHR down-regulates c-Jun N-terminal kinase (JNK). Oncogene 21, 2573-2583
16. Alonso, A., Saxena, M., Williams, S., and Mustelin, T. (2001) Inhibitory role for dual specificity phosphatase VHR in T cell antigen receptor and CD28-induced Erk and Jnk activation. J. Biol. Chem. 276, 4766-4771
17. Zhou, B., Wang, Z.-X., Zhao, Y., Brautigan, D. L., and Zhang, Z.-Y. (2002) The specificity of extracellular signal-regulated kinase 2 dephosphorylation by protein phosphatases. J. Biol. Chem. 277, 31818-31825
18. Hoyt, R., Zhu, W., Cerignoli, F., Alonso, A., Mustelin, T., and David, M. (2007) Cutting edge: selective tyrosine dephosphorylation of interferonactivated nuclear STAT5 by the VHR phosphatase. J. Immunol. 179, 3402-3406
19. Wang, J.-Y., Yeh, C.-L., Chou, H.-C., Yang, C.-H., Fu, Y.-N., Chen, Y.-T., Cheng, H.-W., Huang, C.-Y., Liu, H.-P., Huang, S.-F., and Chen, Y.-R. (2011) Vaccinia H1-related phosphatase is a phosphatase of ErbB receptors and is down-regulated in non-small cell lung cancer. J. Biol. Chem. 286, 10177-10184
20. Alonso, A., Rahmouni, S., Williams, S., van Stipdonk, M., Jaroszewski, L., Godzik, A., Abraham, R. T., Schoenberger, S. P., and Mustelin, T. (2003) Tyrosine phosphorylation of VHR phosphatase by ZAP-70. Nat. Immunol. 4, 44-48
21. Jardin, C., and Sticht, H. (2012) Identification of the structural features that mediate binding specificity in the recognition of STAT proteins by dual-specificity phosphatases. J. Biomol. Struct. Dyn. 29, 777-792
22. Kang, T.-H., and Kim, K.-T. (2006) Negative regulation of ERK activity by VRK3-mediated activation of VHR phosphatase. Nat. Cell Biol. 8, 863-869
23. Denu, J. M., Zhou, G., Wu, L., Zhao, R., Yuvaniyama, J., Saper, M. A., and Dixon, J. E. (1995) The purification and characterization of a human dualspecific protein tyrosine phosphatase. J. Biol. Chem. 270, 3796-3803
24. Schumacher, M. A., Todd, J. L., Rice, A. E., Tanner, K. G., and Denu, J. M. (2002) Structural basis for the recognition of a bisphosphorylated MAP kinase peptide by human VHR protein phosphatase. Biochemistry 41, 3009-3017
25. Gopishetty, B., Ren, L., Waller, T. M., Wavreille, A. S., Lopez, M., Thakkar, A., Zhu, J., and Pei, D. (2008) Synthesis of 3,5-difluorotyrosine- containing peptides: application in substrate profiling of protein tyrosine phosphatases. Org. Lett. 10, 4605-4608
26. Chen, X., Ren, L., Kim, S., Carpino, N., Daniel, J. L., Kunapuli, S. P., Tsygankov, A. Y., and Pei, D. (2010) Determination of the substrate specificity of protein-tyrosine phosphatase TULA-2 and identification of Syk as a TULA-2 substrate. J. Biol. Chem. 285, 31268-31276
27. Li, S., and Zeng, D. (2007) Chemoenzymatic enrichment of phosphotyrosine- containing peptides. Angew. Chem. Int. Ed. Engl. 46, 4751-4753
28. Thakkar, A., Wavreille, A. S., and Pei, D. (2006) Traceless capping agent for peptide sequencing by partial Edman degradation and mass spectrometry. Anal. Chem. 78, 5935-5939
29. Zhang, Z.-Y., Maclean, D., Thieme-Sefler, A. M., Roeske, R. W., and Dixon, J. E. (1993) A continuous spectrophotometric and fluorimetric assay for protein tyrosine phosphatase using phosphotyrosine-containing peptides. Anal. Biochem. 211, 7-15
30. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
31. 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
32. Mahoney, M. W., and Jorgensen, W. L. (2000) A five-site model for liquid water and the reproduction of the density anomaly by rigid, nonpolarizable potential functions. J. Chem. Phys. 112, 8910-8922
33. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-993
34. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T., Caldwell, J., Wang, J., and Kollman, P. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24, 1999-2012
35. Sharp, S. K., and Honig, B. (1994) Accurate calculation of hydration freeenergies using macroscopic solvent models. J. Phys. Chem. 98, 1978-1988
36. Luo, R., David, L., Gilson, M. K. (2002) Accelerated Poisson-Boltzmann calculations for static and dynamic systems. J. Comput. Chem. 23, 1244-1253
37. Fogolari, F., Brigo, A., and Molinari, H. (2003) Protocol for MM/PBSA molecular dynamics simulations of proteins. Biophys. J. 85, 159-166
38. Sigalov, G., Onufriev, P., and Scheffel, P. (2005) Incorporating variable dielectric environments into the generalized Born model. J. Chem. Phys. 122, 94511-99451
39. Garaud, M., and Pei, D. (2007) Substrate profiling of protein tyrosine phosphatase PTP1B by screening a combinatorial peptide library. J. Am. Chem. Soc. 129, 5366-5367
40. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19, 1639-1662
41. Bradshaw, R. A., Brickey, W. W., and Walker, K. W. (1998) N-terminal processing: the methionine aminopeptidase and Nα-acetyl transferase families. Trends Biochem. Sci. 23, 263-267
42. Bashaw, G. J., Kidd, T., Murray, D., Pawson, T., and Goodman, C. S. (2000) Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101, 703-715
43. Lin, Y. H., Park, Z.-Y., Lin, D., Brahmbhatt, A. A., Rio, M.-C., Yates, J. R., 3rd, and Klemke, R. L. (2004) Regulation of cell migration and survival by focal adhesion targeting of Lasp-1. J. Cell Biol. 165, 421-432
44. Srinivasula, S. M., Hegde, R., Saleh, A., Datta, P., Shiozaki, E., Chai, J., Lee, R. A., Robbins, P. D., Fernandes-Alnemri, T., Shi, Y., and Alnemri, E. S. (2001) A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 410, 112-116
45. Du, C., Fang, M., Li, Y., Li, L., and Wang, X. (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102, 33-42
46. Verhagen, A. M., Silke, J., Ekert, P. G., Pakusch, M., Kaufmann, H., Connolly, L. M., Day, C. L., Tikoo, A., Burke, R., Wrobel, C., Moritz, R. L., Simpson, R. J., and Vaux, D. L. (2002) HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J. Biol. Chem. 277, 445-454
47. Hegde, R., Srinivasula, S. M., Datta, P., Madesh, M., Wassell, R., Zhang, Z., Cheong, N., Nejmeh, J., Fernandes-Alnemri, T., Hoshino, S., and Alnemri, E. S. (2003) The polypeptide chain-releasing factor GSPT1/eRF3 is proteolytically processed into an IAP-binding protein. J. Biol. Chem. 278, 38699-38706.