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Molecules and Cells

, Volume 33, Issue 2, pp 163–171 | Cite as

Dissection of the dimerization modes in the DJ-1 superfamily

  • Hoi Jong Jung
  • Sangok Kim
  • Yun Jae Kim
  • Min-Kyu Kim
  • Sung Gyun Kang
  • Jung-Hyun Lee
  • Wankyu Kim
  • Sun-Shin Cha
Article

Abstract

The DJ-1 superfamily (DJ-1/ThiJ/PfpI superfamily) is distributed across all three kingdoms of life. These proteins are involved in a highly diverse range of cellular functions, including chaperone and protease activity. DJ-1 proteins usually form dimers or hexamers in vivo and show at least four different binding orientations via distinct interface patches. Abnormal oligomerization of human DJ-1 is related to neurodegenerative disorders including Parkinson’s disease, suggesting important functional roles of quaternary structures. However, the quaternary structures of the DJ-1 superfamily have not been extensively studied. Here, we focus on the diverse oligomerization modes among the DJ-1 superfamily proteins and investigate the functional roles of quaternary structures both computationally and experimentally. The oligomerization modes are classified into 4 types (DJ-1, YhbO, Hsp, and YDR types) depending on the distinct interface patches (I-IV) upon dimerization. A unique, rotated interface via patch I is reported, which may potentially be related to higher order oligomerization. In general, the groups based on sequence similarity are consistent with the quaternary structural classes, but their biochemical functions cannot be directly inferred using sequence information alone. The observed phyletic pattern suggests the dynamic nature of quaternary structures in the course of evolution. The amino acid residues at the interfaces tend to show lower mutation rates than those of non-interfacial surfaces.

Keywords

DJ-1 superfamily DJ-1/ThiJ/PfpI superfamily quaternary structure 

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References

  1. Abdallah, J., Kern, R., Malki, A., Eckey, V., and Richarme, G. (2006). Cloning, expression, and purification of the general stress protein YhbO from Escherichia coli. Protein Expr. Purif. 47, 455–460.PubMedCrossRefGoogle Scholar
  2. Abdallah, J., Caldas, T., Kthiri, F., Kern, R., and Richarme, G. (2007). YhbO protects cells against multiple stresses. J. Bacteriol. 189, 9140–9144.PubMedCrossRefGoogle Scholar
  3. Bandyopadhyay, S., and Cookson, M.R. (2004). Evolutionary and functional relationships within the DJ1 superfamily. BMC Evol. Biol. 4, 6.PubMedCrossRefGoogle Scholar
  4. Bonifati, V., Rizzu, P., van Baren, M.J., Schaap, O., Breedveld, G.J., Krieger, E., Dekker, M.C., Squitieri, F., Ibanez, P., Joosse, M., et al. (2003). Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299, 256–259.PubMedCrossRefGoogle Scholar
  5. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. (1998). Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905–921.PubMedCrossRefGoogle Scholar
  6. Canet-Aviles, R.M., Wilson, M.A., Miller, D.W., Ahmad, R., Mc-Lendon, C., Bandyopadhyay, S., Baptista, M.J., Ringe, D., Petsko, G.A., and Cookson, M.R. (2004). The Parkinson’s disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc. Natl. Acad. Sci. USA 101, 9103–9108.PubMedCrossRefGoogle Scholar
  7. Cha, S.S., Jung, H.I., Jeon, H., An, Y.J., Kim, I.K., Yun, S., Ahn, H.J., Chung, K.C., Lee, S.H., Suh, P.G., et al. (2008). Crystal structure of filamentous aggregates of human DJ-1 formed in an inorganic phosphate-dependent manner. J. Biol. Chem. 283, 34069–34075.PubMedCrossRefGoogle Scholar
  8. Chen, J., Li, L., and Chin, L.S. (2010). Parkinson disease protein DJ-1 converts from a zymogen to a protease by carboxylterminal cleavage. Hum. Mol. Genet. 19, 2395–2408.PubMedCrossRefGoogle Scholar
  9. Du, X., Choi, I.G., Kim, R., Wang, W., Jancarik, J., Yokota, H., and Kim, S.H. (2000). Crystal structure of an intracellular protease from Pyrococcus horikoshii at 2-A resolution. Proc. Natl. Acad. Sci. USA 97, 14079–14084.PubMedCrossRefGoogle Scholar
  10. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010). Features and development of coot. Acta Crystallogr. D. Biol. Crystallogr. 66, 486–501.PubMedCrossRefGoogle Scholar
  11. Fioravanti, E., Dura, M.A., Lascoux, D., Micossi, E., Franzetti, B., and McSweeney, S. (2008). Structure of the stress response protein DR1199 from Deinococcus radiodurans: a member of the DJ-1 superfamily. Biochemistry 47, 11581–11589.PubMedCrossRefGoogle Scholar
  12. Gorner, K., Holtorf, E., Waak, J., Pham, T.T., Vogt-Weisenhorn, D.M., Wurst, W., Haass, C., and Kahle, P.J. (2007). Structural determinants of the C-terminal helix-kink-helix motif essential for protein stability and survival promoting activity of DJ-1. J. Biol. Chem. 282, 13680–13691.PubMedCrossRefGoogle Scholar
  13. Graille, M., Quevillon-Cheruel, S., Leulliot, N., Zhou, C.Z., de la Sierra Gallay, I.L., Jacquamet, L., Ferrer, J.L., Liger, D., Poupon, A., Janin, J., et al. (2004). Crystal structure of the YDR533c S. cerevisiae protein, a class II member of the Hsp31 family. Structure 12, 839–847.PubMedCrossRefGoogle Scholar
  14. Halio, S.B., Bauer, M.W., Mukund, S., Adams, M., and Kelly, R.M. (1997). Purification and characterization of two functional forms of intracellular protease PfpI from the hyperthermophilic archaeon pyrococcus furiosus. Appl. Environ. Microbiol. 63, 289–295.PubMedGoogle Scholar
  15. Horvath, M.M., and Grishin, N.V. (2001). The C-terminal domain of HPII catalase is a member of the type I glutamine amidotransferase superfamily. Proteins 42, 230–236.PubMedCrossRefGoogle Scholar
  16. Junn, E., Taniguchi, H., Jeong, B.S., Zhao, X., Ichijo, H., and Mouradian, M.M. (2005). Interaction of DJ-1 with Daxx inhibits apoptosis signal-regulating kinase 1 activity and cell death. Proc. Natl. Acad. Sci. USA 102, 9691–9696.PubMedCrossRefGoogle Scholar
  17. Kim, R.H., Peters, M., Jang, Y., Shi, W., Pintilie, M., Fletcher, G.C., DeLuca, C., Liepa, J., Zhou, L., Snow, B., et al. (2005). DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell 7, 263–273.PubMedCrossRefGoogle Scholar
  18. Kim, W.K., Henschel, A., Winter, C., and Schroeder, M. (2006). The many faces of protein-protein interactions: a compendium of interface geometry. PLoS Comput. Biol. 2, e124.PubMedCrossRefGoogle Scholar
  19. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.PubMedCrossRefGoogle Scholar
  20. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R., and Thornton, J.M. (1996). AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477–486.PubMedCrossRefGoogle Scholar
  21. Lee, S.J., Kim, S.J., Kim, I.K., Ko, J., Jeong, C.S., Kim, G.H., Park, C., Kang, S.O., Suh, P.G., Lee, H.S., et al. (2003). Crystal structures of human DJ-1 and Escherichia coli Hsp31, which share an evolutionarily conserved domain. J. Biol. Chem. 278, 44552–44559.PubMedCrossRefGoogle Scholar
  22. Li, Y.H., Wang, Y.Y., Zhong, S., Rong, Z.L., Ren, Y.M., Li, Z.Y., Zhang, S.P., Chang, Z.J., and Liu, L. (2009). Transmembrane helix of novel oncogene with kinase-domain (NOK) influences its oligomerization and limits the activation of RAS/MAPK signaling. Mol. Cells 27, 39–45.PubMedCrossRefGoogle Scholar
  23. Lucas, J.I., and Marin, I. (2007). A new evolutionary paradigm for the Parkinson disease gene DJ-1. Mol. Biol. Evol. 24, 551–561.PubMedCrossRefGoogle Scholar
  24. Mizote, T., Tsuda, M., Smith, D.D., Nakayama, H., and Nakazawa, T. (1999). Cloning and characterization of the thiD/J gene of Escherichia coli encoding a thiamin-synthesizing bifunctional enzyme, hydroxymethylpyrimidine kinase/phosphomethylpyrimidine kinase. Microbiology 145, 495–501.PubMedCrossRefGoogle Scholar
  25. Moore, D.J., Zhang, L., Troncoso, J., Lee, M.K., Hattori, N., Mizuno, Y., Dawson, T.M., and Dawson, V.L. (2005). Association of DJ-1 and parkin mediated by pathogenic DJ-1 mutations and oxidative stress. Hum. Mol. Genet. 14, 71–84.PubMedCrossRefGoogle Scholar
  26. Mujacic, M., and Baneyx, F. (2007). Chaperone Hsp31 contributes to acid resistance in stationary-phase Escherichia coli. Appl. Environ. Microbiol. 73, 1014–1018.PubMedCrossRefGoogle Scholar
  27. Neumann, M., Muller, V., Gorner, K., Kretzschmar, H.A., Haass, C., and Kahle, P.J. (2004). Pathological properties of the Parkinson’s disease-associated protein DJ-1 in alpha-synucleinopathies and tauopathies: relevance for multiple system atrophy and Pick’s disease. Acta Neuropathol. 107, 489–496.PubMedCrossRefGoogle Scholar
  28. Notredame, C., Higgins, D.G., and Heringa, J. (2000). T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205–217.PubMedCrossRefGoogle Scholar
  29. Ollis, D.L., Cheah, E., Cygler, M., Dijkstra, B., Frolow, F., Franken, S.M., Harel, M., Remington, S.J., Silman, I., Schrag, J., et al. (1992). The alpha/beta hydrolase fold. Protein Eng. 5, 197–211.PubMedCrossRefGoogle Scholar
  30. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol. 276, 307–326.CrossRefGoogle Scholar
  31. Pupko, T., Bell, R.E., Mayrose, I., Glaser, F., and Ben-Tal, N. (2002). Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues. Bioinformatics 18, S71–77.PubMedCrossRefGoogle Scholar
  32. Quigley, P.M., Korotkov, K., Baneyx, F., and Hol, W.G. (2003). The 1.6-A crystal structure of the class of chaperones represented by Escherichia coli Hsp31 reveals a putative catalytic triad. Proc. Natl. Acad. Sci. USA 100, 3137–3142.PubMedCrossRefGoogle Scholar
  33. Sastry, M.S., Korotkov, K., Brodsky, Y., and Baneyx, F. (2002). Hsp31, the Escherichia coli yedU gene product, is a molecular chaperone whose activity is inhibited by ATP at high temperatures. J. Biol. Chem. 277, 46026–46034.PubMedCrossRefGoogle Scholar
  34. Shendelman, S., Jonason, A., Martinat, C., Leete, T., and Abeliovich, A. (2004). DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol. 2, e362.PubMedCrossRefGoogle Scholar
  35. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.PubMedCrossRefGoogle Scholar
  36. Vagin, A., and Teplyakov, A. (2010). Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22–25.PubMedCrossRefGoogle Scholar
  37. Wei, Y., Ringe, D., Wilson, M.A., and Ondrechen, M.J. (2007). Identification of functional subclasses in the DJ-1 superfamily proteins. PLoS Comput. Biol. 3, e10.PubMedCrossRefGoogle Scholar
  38. Wilson, M.A., St Amour, C.V., Collins, J.L., Ringe, D., and Petsko, G.A. (2004). The 1.8-A resolution crystal structure of YDR533Cp from Saccharomyces cerevisiae: a member of the DJ-1/ThiJ/ PfpI superfamily. Proc. Natl. Acad. Sci. USA 101, 1531–1536.PubMedCrossRefGoogle Scholar
  39. Wilson, M.A., Ringe, D., and Petsko, G.A. (2005). The atomic resolution crystal structure of the YajL (ThiJ) protein from Escherichia coli: a close prokaryotic homologue of the Parkinsonismassociated protein DJ-1. J. Mol. Biol. 353, 678–691.PubMedCrossRefGoogle Scholar
  40. Winter, C., Henschel, A., Kim, W.K., and Schroeder, M. (2006). SCOPPI: a structural classification of protein-protein interfaces. Nucleic Acids Res. 34, D310–314.PubMedCrossRefGoogle Scholar
  41. Witt, A.C., Lakshminarasimhan, M., Remington, B.C., Hasim, S., Pozharski, E., and Wilson, M.A. (2008). Cysteine pKa depression by a protonated glutamic acid in human DJ-1. Biochemistry 47, 7430–7440.PubMedCrossRefGoogle Scholar
  42. Yang, Y., Gehrke, S., Haque, M.E., Imai, Y., Kosek, J., Yang, L., Beal, M.F., Nishimura, I., Wakamatsu, K., Ito, S., et al. (2005). Inactivation of Drosophila DJ-1 leads to impairments of oxidative stress response and phosphatidylinositol 3-kinase/Akt signaling. Proc. Natl. Acad. Sci. USA 102, 13670–13675.PubMedCrossRefGoogle Scholar

Copyright information

© The Korean Society for Molecular and Cellular Biology and Springer Netherlands 2012

Authors and Affiliations

  • Hoi Jong Jung
    • 1
  • Sangok Kim
    • 2
  • Yun Jae Kim
    • 1
  • Min-Kyu Kim
    • 1
  • Sung Gyun Kang
    • 1
    • 3
  • Jung-Hyun Lee
    • 1
    • 3
  • Wankyu Kim
    • 2
  • Sun-Shin Cha
    • 1
    • 3
  1. 1.Marine Biotechnology Research CenterKorea Ocean Research and Development InstituteAnsanKorea
  2. 2.Ewha Research Center for Systems Biology, Division of Molecular and Life SciencesEwha Womans UniversitySeoulKorea
  3. 3.Department of Marine BiotechnologyUniversity of Science and TechnologyDaejeonKorea

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