Identification of phosphorylation sites of TOPORS and a role for serine 98 in the regulation of ubiquitin but not SUMO E3 ligase activity

Biochemistry

Volumn 47, Issue 52, 2008, Pages 13887-13896

  Park, Hye Jin ^a   Zheng, Haiyan ^a   Kulkarni, Diptee ^a   Kerrigan, John ^a   Pungaliya, Pooja ^a   Saleem, Ahamed ^a   Rubin, Eric H ^a  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACIDS; BINARY SWITCH; CONSERVED REGIONS; E3 LIGASE; IN-CELL; IN-VITRO; LIGASE ACTIVITY; LIGASES; MOLECULAR MODELING STUDIES; N-TERMINALS; PHOSPHORYLATION SITES; POST-TRANSLATIONAL MODIFICATIONS; SUMOYLATION; UBIQUITIN; UBIQUITIN LIGASES; UBIQUITINATION; WILD TYPES;

AMINO ACIDS; MASS SPECTROMETRY; ORGANIC ACIDS; PHOSPHATASES; PHOSPHORYLATION;

PROTEINS;

ASPARTIC ACID; NUCLEAR PROTEIN; SERINE; SUMO PROTEIN; TOPORS; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; TOPORS PROTEIN, HUMAN; TUMOR PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CANCER CELL CULTURE; CELL STRAIN HEK293; CONTROLLED STUDY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR MODEL; MUTATION; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; RING FINGER MOTIF; SUMOYLATION; UBIQUITINATION; BINDING SITE; GENETICS; METABOLISM; MISSENSE MUTATION; PHOSPHORYLATION; PROTEIN BINDING; TUMOR CELL LINE;

BINDING SITES; CELL LINE, TUMOR; HUMANS; MASS SPECTROMETRY; MUTATION, MISSENSE; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SERINE; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 58849137633     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi801904q     Document Type: Article

References (51)

1. Haluska, P., Jr., Saleem, A., Rasheed, Z., Ahmed, F., Su, E. W., Liu, L. F., and Rubin, E. H. (1999) Interaction between human topoisomerase I and a novel RING finger/arginine-serine protein. Nucleic Acids Res. 27, 2538-2544.
2. Lin, L., Ozaki, T., Takada, Y., Kageyama, H., Nakamura, Y., Hata, A., Zhang, J. H., Simonds, W. F., Nakagawara, A., and Koseki, H. (2005) topors, a p53 and topoisomerase I-binding RING finger protein, is a coactivator of p53 in growth suppression induced by DNA damage. Oncogene 24, 3385-3396.
3. Saleem, A., Dutta, J., Malegaonkar, D., Rasheed, F., Rasheed, Z., Rajendra, R., Marshall, H., Luo, M., Li, H., and Rubin, E. H. (2004) The topoisomerase I- and p53-binding protein topors is differentially expressed in normal and malignant human tissues and may function as a tumor suppressor. Oncogene 23, 5293-5300.
4. Oyanagi, H., Takenaka, K., Ishikawa, S., Kawano, Y., Adachi, Y., Ueda, K., Wada, H., and Tanaka, F. (2004) Expression of LUN gene that encodes a novel RING finger protein is correlated with development and progression of non-small cell lung cancer. Lung Cancer 46, 21-28.
5. Bredel, M., Bredel, C., Juric, D., Harsh, G. R., Vogel, H., Recht, L. D., and Sikic, B. I. (2005) High-resolution genome-wide mapping of genetic alterations in human glial brain tumors. Cancer Res. 65, 4088-4096.
6. Rajendra, R., Malegaonkar, D., Pungaliya, P., Marshall, H., Rasheed, Z., Brownell, J., Liu, L. F., Lutzker, S., Saleem, A., and Rubin, E. H. (2004) Topors functions as an E3 ubiquitin ligase with specific E2 enzymes and ubiquitinates p53. J. Biol. Chem. 279, 36440-36444.
7. Weger, S., Hammer, E., and Heilbronn, R. (2005) Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett. 579, 5007-5012.
8. Johnson, E. S. (2004) Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382.
9. Muller, S., Matunis, M. J., and Dejean, A. (1998) Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17, 61-70.
10. Melchior, F., and Hengst, L. (2002) SUMO-1 and p53. Cell Cycle 1, 245-249.
11. Weger, S., Hammer, E., and Engstler, M. (2003) The DNA topoisomerase I binding protein topors as a novel cellular target for SUMO-1 modification: characterization of domains necessary for subcellular localization and sumolation. Exp. Cell Res. 290, 13-27.
12. Swaminathan, G., and Tsygankov, A. Y. (2006) The Cb1 family proteins: ring leaders in regulation of cell signaling. J. Cell. Physiol. 209, 21-113
13. Kassenbrock, C. K., Hunter, S., Garl, P., Johnson, G. L., and Anderson, S. M. (2002) Inhibition of Src family kinases blocks epidermal growth factor (EGF)-induced activation of Akt, phosphorylation of c-Cbl, and ubiquitination of the EGF receptor. J. Biol. Chem. 277, 24967-24975.
14. Khurana, A., Nakayama, K., Williams, S., Davis, R. J., Mustelin, T., and Ronai, Z. (2006) Regulation of the ring finger E3 ligase Siah2 by p38 MAPK. J. Biol. Chem. 281, 35316-35326.
15. He, H., Tan, M., Pamarthy, D., Wang, C., Ahmed, K., and Sun, Y. (2007) CK2 phosphorylation of SAG at ThrlO regulates SAG stability, but not its E3 ligase activity. Mol. Cell. Biochem. 295, 179-188.
16. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P., and Dikic, I. (2006) Specification of SUMOl- and SUM02-interacting motifs. J. Biol. Chem. 281, 16117-16127.
17. Zheng, N., Wang, P., Jeffrey, P. D., and Pavletich, N. P. (2000) Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 102, 533-539.
18. Winkler, G. S., Albert, T. K., Dominguez, C., Legtenberg, Y. I., Boelens, R., and Timmers, H. T. (2004) An altered-specificity ubiquitin-conjugating enzyme/ubiquitin-protein ligase pair. J. Mol. Biol. 337, 157-165.
19. Yokouchi, M., Kondo, T., Sanjay, A., Houghton, A., Yoshimura, A., Komiya, S., Zhang, H., and Baron, R. (2001) Src-catalyzed phosphorylation of c-Cbl leads to the interdependent ubiquitination of both proteins. J. Biol. Chem. 276, 35185-35193.
20. Kassenbrock, C. K., and Anderson, S. M. (2004) Regulation of ubiquitin protein ligase activity in c-Cbl by phosphorylationinduced conformational change and constitutive activation by tyrosine to glutamate point mutations. J. Biol. Chem. 279, 28017-28027.
21. Levkowitz, C., Waterman, H., Ettenberg, S. A., Katz, M., Tsygankov, A. Y., Alroy, I., Lavi, S., Iwai, K., Reiss, Y., Ciechanover, A., Lipkowitz, S., and Yarden, Y. (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4, 1029-1040.
22. Roscic, A., Moller, A., Calzado, M. A., Renner, F., Wimmer, V. C, Gresko, E., Ludi, K. S., and Schmitz, M. L. (2006) Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Mol. Cell 24, 77-89.
23. Guan, B., Pungaliya, P., Li, X., Uquillas, C., Mutton, L. N., Rubin, E. H., and Bieberich, C. J. (2008) Ubiquitination by TOPORS Regulates the Prostate Tumor Suppressor NKX3.1. J. Biol. Chem. 283, 4834-4840.
24. Jerkic, M., Rodriguez-Barbero, A., Prieto, M., Toporsian, M., Pericacho, M., Rivas-Elena, J. V., Obreo, J., Wang, A., PerezBarriocanal, F., Arevalo, M., Bernabeu, C., Letarte, M., and LopezNovoa, J. M. (2006) Reduced angiogenic responses in adult Endoglin heterozygous mice. Cardio vase. Res. 69, 845-854.
25. Rasheed, Z. A., Saleem, A., Ravee, Y., Pandolfi, P. P., and Rubin, E. H. (2002) The topoisomerase I-binding RING protein, topors, is associated with promyelocytic leukemia nuclear bodies. Exp. Cell Res. 277, 152-160.
26. Barlow, P. N., Luisi, B., Milner, A., Elliott, M., and Everett, R. (1994) Structure of the C3HC4 domain by IH-nuclear magnetic resonance spectroscopy. A new structural class of zinc-finger. J. Mol. Biol. 237, 201-211.
27. Marti-Renom, M. A., Madhusudhan, M. S., Fiser, A., Rost, B., and Sali, A. (2002) Reliability of assessment of protein structure prediction methods. Structure (Cambridge) 10, 435-440.
28. Marti-Renom, M. A., Smart, A. C., Fiser, A., Sanchez, R., Melo, F., and Sali, A. (2000) Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29, 291-325.
29. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815.
30. Dodd, R. B., and Read, R. J. (2006)Structures of two human ubiquitin-conjugating enzymes from twinned crystals, unpublished.
31. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD - Visual Molecular Dynamics. J. Mol. Graphics Modell. 14.1, 33-38.
32. Case, D. A., Cheatham III, T. E., Darden, T., Gohlke, H., Luo, H., Merz, K. M., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. (2005) The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688.
33. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, C., hang, 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.
34. Pang, Y. P., Xu, K., Yazal, J. E., and Prendergas, F. C (2000) Successful molecular dynamics simulation of the zinc-bound farnesyltransferase using the cationic dummy atom approach. Protein Sei. 9, 1857-1865.
35. Berendsen, H. J., Grigera, J., and Straatsma, T. (1987) The missing term in effective pair potentials. J. Phys. Chem. 91, 6269-6271.
36. Darden, T., York, D., and Pedersen, L. (1993) Particle Mesh Ewald: An N-log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092.
37. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. (1995) A smooth particle mesh ewald potential. J. Chem. Phys. 103, 8577-8592.
38. Miyamoto, S., and Kollman, P. (1992) SETTLE: An Analytical Version of the SHAKE and RATTLE Algorithms for Rigid Water Models. J. Comput. Chem. 13, 952-962.
39. Pettersen, E., Goddard, T., Huang, C., Couch, C., Greenblatt, D., Meng, E., and Ferrin, T. E. (2004) UCSF Chimera - A Visualization System for Exploratory Research and Analysis. J. Comput. Chem. 25, 1605-1612.
40. Beausoleil, S. A., Jedrychowski, M., Schwartz, D., Elias, J. E., Villen, J., Li, J., Cohn, M. A., Cantley, L. C., and Gygi, S. P. (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. U.S.A. 101, 12130-12135.
41. Beausoleil, S. A., Villen, J., Gerber, S. A., Rush, J., and Gygi, S. P. (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292.
42. Hammer, E., Heilbronn, R., and Weger, S. (2007) The E3 ligase Topors induces the accumulation of polysumoylated forms of DNA topoisomerase I in vitro and in vivo. FEBS Lett. 581, 5418-5424.
43. Joazeiro, C. A., and Weissman, A. M. (2000) RING finger proteins: mediators of ubiquitin ligase activity. Cell 102, 549-552.
44. Freemont, P. S. (2000) RING for destruction. Curr. Biol. 10, R84-87.
45. Ma, C. T., Velazquez-Dones, A., Hagopian, J. C., Ghosh, C., Fu, X. D., and Adams, J. A. (2008) Ordered multi-site phosphorylation of the splicing factor ASF/SF2 by SRPK1. J. Mol. Biol. 376, 55-68.
46. Mao, D. Y., Ceccarelli, D. F., and Sicheri, F. (2008) "Unraveling the tail" of how SRPK1 phosphorylates ASF/SF2. Mol. Cell 29, 535-537.
47. Joazeiro, C. A., Wing, S. S., Huang, H., Leverson, J. D., Hunter, T., and Liu, Y. C. (1999) The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286, 309-312.
48. Seol, J. H., Feldman, R. M., Zachariae, W., Shevchenko, A., Correll, C. C., Lyapina, S., Chi, Y., Galova, M., Claypool, J., Sandmeyer, S., Nasmyth, K., Deshaies, R. J., Shevchenko, A., and Deshaies, R. J. (1999) Cdc53/cullin and the essential Hrtl RINGH2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev. 13, 1614-1626.
49. Eletr, Z. M., and Kuhlman, B. (2007) Sequence determinants of E2-E6AP binding affinity and specificity. J. Mol. Biol. 369, 419-428.
50. Kannan, N., and Neuwald, A. F. (2004) Evolutionary constraints associated with functional specificity of the CMGC protein kinases MAPK, CDK, GSK, SRPK, DYRK, and CK2alpha. Protein Sci. 2059-2077.
51. Mylonis, I., Chachami, C., Samiotaki, M., Panayotou, C., Paraskeva, E., Kalousi, A., Georgatsou, E., Bonanou, S., and Simos, G. (2006) Identification of MAPK phosphorylation sites and their role in the localization and activity of hypoxia-inducible factor-1alpha. J. Biol. Chem. 281, 33095-33106.