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Identification of SUMOylated proteins in neuroblastoma cells after treatment with hydrogen peroxide or ascorbate

  • Grant, Melissa M. (School of Dentistry, University of Birmingham)
  • Received : 2010.04.15
  • Accepted : 2010.09.01
  • Published : 2010.11.30

Abstract

The small ubiquitin-like modifier (SUMO) proteins have been implicated in the pathology of a number of diseases, including neurodegenerative diseases. The conjugation machinery for SUMOylation consists of a number of proteins which are redox sensitive. Here, under oxidative stress ($100{\mu}M$ hydrogen peroxide), antioxidant ($100{\mu}M$ ascorbate) or control conditions 169 proteins were identified by electospray ionisation fourier transform ion cyclotron resonance mass spectrometry. The majority of these proteins (70%) were found to contain SUMOylation consensus sequences. From the remaining proteins a small number (12%) were found to contain possible SUMO interacting motifs. The proteins identified included DNA and RNA binding proteins, structural proteins and proteasomal proteins. Several of the proteins identified under oxidative stress conditions had previously been identified as SUMOylated proteins, thus validating the method presented.

Keywords

References

  1. Bayer, P., Arndt, A., Metzger, S., Mahajan, R., Melchior, F., Jaenicke, R. and Becker, J. (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 280, 275-286. https://doi.org/10.1006/jmbi.1998.1839
  2. Li, M., Guo, D., Isales, C. M., Eizirik, D. L., Atkinson, M., She, J. X. and Wang, C. Y. (2005) SUMO wrestling with type 1 diabetes. J. Mol. Med. 83, 504-513. https://doi.org/10.1007/s00109-005-0645-5
  3. Johnson, E. S. (2004) Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382. https://doi.org/10.1146/annurev.biochem.73.011303.074118
  4. Sekiyama, N., Ikegami, T., Yamane, T., Ikeguchi, M., Uchimura, Y., Baba, D., Ariyoshi, M., Tochio, H., Saitoh, H. and Shirakawa, M. (2008) Structure of the small ubiquitin-like modifier (SUMO)-interacting motif of MBD1-containing chromatin-associated factor 1 bound to SUMO-3. J. Biol. Chem. 283, 35966-35975. https://doi.org/10.1074/jbc.M802528200
  5. Pfander, B., Moldovan, G. L., Sacher, M., Hoege, C. and Jentsch, S. (2005) SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436, 428-433. https://doi.org/10.1038/nature03665
  6. Dorval, V. and Fraser, P. E. (2007) SUMO on the road to neurodegeneration. Biochim. Biophys. Acta. 1773, 694-706. https://doi.org/10.1016/j.bbamcr.2007.03.017
  7. Terashima, T., Kawai, H., Fujitani, M., Maeda, K. and Yasuda, H. (2002) SUMO-1 colocalized with mutant atrophin-1 with expanded polyglutamines accelerates intranuclear aggregation and cell death. Neuroreport. 13, 2359- 2364. https://doi.org/10.1097/00001756-200212030-00038
  8. Saitoh, H. and Hinchey, J. (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275, 6252-6258. https://doi.org/10.1074/jbc.275.9.6252
  9. Bossis, G. and Melchior, F. (2006) Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol. Cell 21, 349-357. https://doi.org/10.1016/j.molcel.2005.12.019
  10. Paulsen, C. E. and Carroll, K. S. (2010) Orchestrating redox signaling networks through regulatory cysteine switches. ACS. Chem. Biol. 5, 47-62. https://doi.org/10.1021/cb900258z
  11. Grant, M. M., Barber, V. S. and Griffiths, H. R. (2005) The presence of ascorbate induces expression of brain derived neurotrophic factor in SH-SY5Y neuroblastoma cells after peroxide insult, which is associated with increased survival. Proteomics. 5, 534-540. https://doi.org/10.1002/pmic.200300924
  12. Rosas-Acosta, G., Russell, W. K., Deyrieux, A., Russell, D. H. and Wilson, V. G. (2005) A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers. Mol. Cell Proteomics. 4, 56-72. https://doi.org/10.1074/mcp.M400149-MCP200
  13. Vertegaal, A. C., Andersen, J. S., Ogg, S. C., Hay, R. T., Mann, M. and Lamond, A. I. (2006) Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell Proteomics. 5, 2298-2310. https://doi.org/10.1074/mcp.M600212-MCP200
  14. Hannich, J. T., Lewis, A., Kroetz, M. B., Li, S. J., Heide, H., Emili, A. and Hochstrasser, M. (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280, 4102-4110. https://doi.org/10.1074/jbc.M413209200
  15. Wohlschlegel, J. A., Johnson, E. S., Reed, S. I. and Yates, J. R. 3rd. (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279, 45662-45668. https://doi.org/10.1074/jbc.M409203200
  16. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Séraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032. https://doi.org/10.1038/13732
  17. He, Y. and Smith, R. (2009) Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B. Cell Mol. Life Sci. 66, 1239-1256. https://doi.org/10.1007/s00018-008-8532-1
  18. Hay, R. T. (2005) SUMO: a history of modification. Mol. Cell 18, 1-12. https://doi.org/10.1016/j.molcel.2005.03.012
  19. Perry, J. J., Tainer, J. A. and Boddy, M. N. (2008) A SIMultaneous role for SUMO and ubiquitin. Trends Biochem. Sci. 33, 201-208. https://doi.org/10.1016/j.tibs.2008.02.001
  20. Hecker, C., Rabiller, M., Haglund, K., Bayer, P. and Dikic, I. (2006) Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 281, 16117-16127. https://doi.org/10.1074/jbc.M512757200
  21. Song, J., Zhang, Z., Hu, W. and Chen, Y. (2005) Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J. Biol. Chem. 280, 40122-40129. https://doi.org/10.1074/jbc.M507059200
  22. Jakobs, A., Koehnke, J., Himstedt, F., Funk, M., Korn, B., Gaestel, M. and Niedenthal, R. (2007) Ubc9 fusion- directed SUMOylation (UFDS): a method to analyze function of protein SUMOylation. Nat. Methods. 4, 245-250. https://doi.org/10.1038/nmeth1006
  23. Gutierrez, G. J. and Ronai, Z. (2006) Ubiquitin and SUMO systems in the regulation of mitotic checkpoints. Trends Biochem. Sci. 31, 324-332. https://doi.org/10.1016/j.tibs.2006.04.001
  24. Jakobs, A., Himstedt, F., Funk, M., Korn, B., Gaestel, M. and Niedenthal, R. (2007) Ubc9 fusion-directed SUMOylation identifies constitutive and inducible SUMOylation. Nucleic. Acids. Res. 35, e109. https://doi.org/10.1093/nar/gkm617
  25. Pollice, A., Vivo, M. and La Mantia, G. (2008) The promiscuity of ARF interactions with the proteasome. FEBS Lett. 582, 3257-3262. https://doi.org/10.1016/j.febslet.2008.09.026
  26. Gharahdaghi, F., Weinberg, C. R., Meagher, D. A., Imai, B. S. and Mische, S. M. (1999) Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20, 601-605. https://doi.org/10.1002/(SICI)1522-2683(19990301)20:3<601::AID-ELPS601>3.0.CO;2-6
  27. Creese, A. and Cooper, H. J. (2007) Liquid chromatography electron capture dissociation tandem mass spectrometry (LC-ECD-MS/MS) versus liquid chromatography collision-induced dissociation tandem mass spectrometry (LC-CID-MS/MS) for the identification of proteins. J. Am. Soc. Mass. Spectrom. 18, 891-897. https://doi.org/10.1016/j.jasms.2007.01.008
  28. Chow, S. and Ruskey, F. (2004) Drawing area-proportional Venn and Euler diagrams. Proc. of Graph. Drawing 2912, 466-477. https://doi.org/10.1007/978-3-540-24595-7_44
  29. Ren, J., Gao, X., Jin, C., Zhu, M., Wang, X., Shaw, A., Wen, L., Yao, X. and Xue, Y. (2009) Systematic study of protein sumoylation: development of a site-specific predictor of SUMOsp 2.0. Proteomics. 9, 3409-3412. https://doi.org/10.1002/pmic.200800646

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