Abstract
The regulation of nucleotide-regulated inorganic pyrophosphatases at a molecular level has been extensively studied in order to establish the mechanism of signal transduction between the active and regulatory sites of these enzymes. However, this issue cannot be ultimately addressed because of the lack of reliable structural data on the full-length protein and its interactions with ligands. The low-resolution structure of nucleotide-regulated pyrophosphatase from Desulfitobacterium hafniense was determined for the first time by small-angle X-ray scattering. The structural changes in the full-length enzyme upon binding of adenosine monophosphate and diadenosine tetraphosphate were revealed. In dilute solutions the protein was found to exist as a stable homotetramer, the structure of which depends on the nature of the bound ligand. The structural data are important for an understanding of the molecular basis for regulation of this family of enzymes.
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REFERENCES
J. Heinonen, Biological Role of Inorganic Pyrophosphate (Kluwer Academic Publishers, Moscow, 2001).
T. Shintani, T. Uchiumi, T. Yonezawa, et al., FEBS Lett. 439, 263 (1998).
T. Young, N. Kuhn, A. Wadeson, et al., Microbiology 144, 2563 (1998).
V. A. Anashkin, V. A. Aksenova, A. Salminen, et al., Biochem. Biophys. Res. Commun. 517, 266 (2015).
A. A. Baykov, V. A. Anashkin, A. Salminen, et al., FEBS Lett. 591, 3225 (2017).
M. Merckel, I. Fabrichniy, A. Salminen, et al., Structure 94, 289 (2001).
S. Ahn, A. Milner, K. Fütterer, et al., J. Mol. Biol. 313, 797 (2001).
M. Rantanen, L. Lehtiö, L. Rajagopal, et al., Acta Crystallogr. D 63, 738 (2007).
L. Aravind and E. Koonin, Trends Cell Biol. 23, 17 (1998).
S. Ignoul and J. Eggermont, Am. J. Physiol. Cell Physiol. 289, 1369 (2005).
J. Ereno-Orbea, I. Oyenarte, and L. A. Martınez-Cruz, Arch. Biochem. Biophys. 540, 70 (2013).
J. Jamsen, H. Tuominen, A. Salminen, et al., Biochem. J. 408, 327 (2007).
V. A. Anashkin, A. Salminen, H. K. Tuominen, et al., J. Biol. Chem. 290, 27594 (2015).
A. Salminen, V. A. Anashkin, M. Lahti, et al., J. Biol. Chem. 289, 22865 (2014).
H. Tuominen, A. Salminen, E. Oksanen, et al., J. Mol. Biol. 398, 400 (2010).
V. A. Anashkin, A. Salminen, E. Osipova, et al., ACS Omega 4, 15549 (2019).
V. A. Anashkin, A. Salminen, N. N. Vorobjeva, et al., Biochem. J. 473, 2097 (2016).
D. I. Svergun, M. H. J. Koch, P. A. Timmins, et al., Small Angle X-Ray and Neutron Scattering from Solutions of Biological Macromolecules (Oxford Univ. Press, Oxford, 2013).
D. A. Korasick and J. J. Tanner, Protein Sci. 27, 814 (2018).
A. Parfenyev, A. Salminen, P. Halonen, et al., J. Biol. Chem. 276, 24511 (2001).
E. Gasteiger, C. Hoogland, A. Gattiker, et al., The Proteomics Protocols Handbook (Humana, New York, 2005).
C. M. Jeffries, M. A. Graewert, D. I. Svergun, et al., J. Synchr. Radiat. 22, 273 (2015).
P. V. Konarev, V. V. Volkov, A. V. Sokolova, et al., J. Appl. Crystallogr. 36, 1277 (2003).
N. R. Hajizadeh, D. Franke, C. M. Jeffries, et al., Sci. Rep. 8, 7204 (2018).
G. Porod, O. Glatter, O. Kratky, et al., Small Angle X-Ray Scattering (Academic, London, 1982).
D. Franke, M. V. Petoukhov, P. V. Konarev, et al., J. Appl. Crystallogr. 50, 1212 (2017).
D. I. Svergun, J. Appl. Crystallogr. 25, 495 (1992).
D. I. Svergun, Biophys. J. 76, 2879 (1999).
M. V. Petoukhov and D. I. Svergun, Acta Crystallogr. D 71, 1051 (2015).
D. A. Jacques, J. M. Guss, D. I. Svergun, et al., Acta Crystallogr. D 68, 620 (2012).
P. V. Konarev and D. I. Svergun, IUCr J. 2, 352 (2015).
ACKNOWLEDGMENTS
We thank Professor R Lahti (University of Turku, Turku, Finland) for providing the plasmid bearing the gene encoding dh-PPase.
Funding
The study was supported by the Russian Foundation for Basic Research (project no. 18-34-00918) and the Ministry of Science and Higher Education of the Russian Federation within the framework of the State assignment of the Federal Scientific Research Centre “Crystallography and Photonics” of the Russian Academy of Sciences.
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Dadinova, L.A., Anashkin, V.A. & Shtykova, E.V. Small-Angle X-ray Scattering Study of Changes in the Quaternary Structure of Nucleotide-Regulated Pyrophosphatase from Desulfitobacterium hafniense upon Ligand Binding in Solution. Crystallogr. Rep. 65, 749–754 (2020). https://doi.org/10.1134/S1063774520050053
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DOI: https://doi.org/10.1134/S1063774520050053