Structural determinants for substrate binding and catalysis in triphosphate tunnel metalloenzymes

Journal of Biological Chemistry

Volumn 290, Issue 38, 2015, Pages 23348-23360

  Martinez, Jacobo ^a   Truffault, Vincent ^b   Hothorn, X Michael ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; BINDING SITES; BINS; CATALYSIS; CATALYST ACTIVITY; CYCLIZATION; ENZYMES; ESCHERICHIA COLI; MAMMALS; METALS; PHOSPHATES;

COFACTOR BINDING; ENZYMATIC REACTION; METAL BINDING SITES; POLYPHOSPHATES; STRUCTURAL COMPARISON; STRUCTURAL DETERMINANTS; SUBSTRATE BINDING; SUBSTRATE-BOUND;

SUBSTRATES;

ADENYLATE CYCLASE; MRNA CAPPING ENZYME; PHOSPHATASE; POLYPHOSPHATE POLYMERASE; THIAMINE TRIPHOSPHATASE; TRIPHOSPHATE TUNNEL METALLOENZYME; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; ESCHERICHIA COLI PROTEIN; INORGANIC PYROPHOSPHATASE; METALLOPROTEIN;

ARABIDOPSIS; ARTICLE; BINDING SITE; CATALYSIS; CONTROLLED STUDY; CRYSTALLOGRAPHY; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; CHEMISTRY; ENZYMOLOGY; GENETICS; MOLECULAR EVOLUTION; STRUCTURAL HOMOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; INORGANIC PYROPHOSPHATASE; METALLOPROTEINS; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84942890966     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.674473     Document Type: Article

References (46)

1. Rao, N. N., Gómez-García, M. R., and Kornberg, A. (2009) Inorganic polyphosphate: essential for growth and survival. Annu. Rev. Biochem. 78, 605-647
2. Kornberg, S. R. (1957) Adenosine triphosphate synthesis from polyphosphate by an enzyme from Escherichia coli. Biochim. Biophys. Acta. 26, 294-300
3. Ahn, K., and Kornberg, A. (1990) Polyphosphate kinase from Escherichia coli: purification and demonstration of a phosphoenzyme intermediate. J. Biol. Chem. 265, 11734-11739
4. Hothorn, M., Neumann, H., Lenherr, E. D., Wehner, M., Rybin, V., and Hassa., P. O., Uttenweiler, A., Reinhardt, M., Schmidt, A., Seiler, J., Ladurner, A. G., Herrmann, C., Scheffzek, K., and Mayer, A. (2009) Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science 324, 513-516
5. Zhu, Y., Huang, W., Lee, S. S., and Xu, W. (2005) Crystal structure of a polyphosphate kinase and its implications for polyphosphate synthesis. EMBO Rep. 6, 681-687
6. Gerasimaite, R., Sharma, S., Desfougères, Y., Schmidt, A., and Mayer, A. (2014) Coupled synthesis and translocation restrains polyphosphate to acidocalcisome-like vacuoles and prevents its toxicity. J. Cell Sci. 127, 5093-5104
7. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H.-R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2008) The Pfam protein families database. Nucleic Acids Res. 36, D281-D288
8. Iyer, L. M., and Aravind, L. (2002) The catalytic domains of thiamine triphosphatase and CyaB-like adenylyl cyclase define a novel superfamily of domains that bind organic phosphates. BMC Genomics 3, 33
9. Gong, C., Smith, P., and Shuman, S. (2006) Structure-function analysis of Plasmodium RNA triphosphatase and description of a triphosphate tunnel metalloenzyme superfamily that includes Cet1-like RNA triphosphatases and CYTH proteins. RNA 12, 1468-1474
10. Bettendorff, L., and Wins, P. (2013) Thiamine triphosphatase and the CYTH superfamily of proteins. FEBS J. 280, 6443-6455
11. Lima, C. D., and Wang., L. K., and Shuman, S. (1999) Structure and mechanism of yeast RNA triphosphatase: an essential component of the mRNA capping apparatus. Cell 99, 533-543
12. Bisaillon, M., and Shuman, S. (2001) Structure-function analysis of the active site tunnel of yeast RNA triphosphatase. J. Biol. Chem. 276, 17261-17266
13. Gong, C., and Shuman, S. (2003) Mapping the active site of vaccinia virus RNA triphosphatase. Virology 309, 125-134
14. Gong, C., and Shuman, S. (2002) Chlorella virus RNA triphosphatase: mutational analysis and mechanism of inhibition by tripolyphosphate. J. Biol. Chem. 277, 15317-15324
15. Benarroch, D., Smith, P., and Shuman, S. (2008) Characterization of a trifunctional mimivirus mRNA capping enzyme and crystal structure of the RNA triphosphatase domain. Structure 16, 501-512
16. Kyrieleis, O. J., Chang, J., de la Peña, M., Shuman, S., and Cusack, S. (2014) Crystal structure of vaccinia virus mRNA capping enzyme provides insights into the mechanism and evolution of the capping apparatus. Structure 22, 452-465
17. Gallagher, D. T., and Smith., N. N., Kim, S.-K., Heroux, A., Robinson, H., and Reddy, P. T. (2006) Structure of the class IV adenylyl cyclase reveals a novel fold. J. Mol. Biol. 362, 114-122
18. Gallagher, D. T., Kim, S.-K., Robinson, H., and Reddy, P. T. (2011) Activesite structure of class IV adenylyl cyclase and transphyletic mechanism. J. Mol. Biol. 405, 787-803
19. Lakaye, B., and Makarchikov., A. F., Antunes, A. F., Zorzi, W., Coumans, B., De Pauw, E., Wins, P., Grisar, T., and Bettendorff, L. (2002) Molecular characterization of a specific thiamine triphosphatase widely expressed in mammalian tissues. J. Biol. Chem. 277, 13771-13777
20. Song, J., Bettendorff, L., Tonelli, M., and Markley, J. L. (2008) Structural basis for the catalytic mechanism ofmammalian 25-kDa thiamine triphosphatase. J. Biol. Chem. 283, 10939-10948
21. Delvaux, D., Kerff, F., Murty, M. R., Lakaye, B., Czerniecki, J., Kohn, G., Wins, P., Herman, R., Gabelica, V., Heuze, F., Tordoir, X., Marée, R., Matagne, A., Charlier, P., De Pauw, E., and Bettendorff, L. (2013) Structural determinants of specificity and catalytic mechanism in mammalian 25-kDa thiamine triphosphatase. Biochim. Biophys. Acta. 1830, 4513-4523
22. Jain, R., and Shuman, S. (2008) Polyphosphatase activity of CthTTM, a bacterial triphosphate tunnel metalloenzyme. J. Biol. Chem. 283, 31047-31057
23. Delvaux, D., and Murty., M. R., Gabelica, V., Lakaye, B., Lunin, V. V., Skarina, T., Onopriyenko, O., Kohn, G., Wins, P., De Pauw, E., and Bettendorff, L. (2011) A specific inorganic triphosphatase from Nitrosomonas europaea: Structure and catalytic mechanism. J. Biol. Chem. 286, 34023-34035
24. Keppetipola, N., Jain, R., and Shuman, S. (2007) Novel triphosphate phosphohydrolase activity of Clostridium thermocellum TTM, a member of the triphosphate tunnel metalloenzyme superfamily. J. Biol. Chem. 282, 11941-11949
25. Kohn, G., Delvaux, D., Lakaye, B., Servais, A.-C., Scholer, G., Fillet, M., Elias, B., Derochette, J.-M., Crommen, J., Wins, P., and Bettendorff, L. (2012) High inorganic triphosphatase activities in bacteria and mammalian cells: Identification of the enzymes involved. PLoS ONE 7, e43879
26. Moeder, W., Garcia-Petit, C., Ung, H., Fucile, G., Samuel, M. A., Christendat, D., and Yoshioka, K. (2013) Crystal structure and biochemical analyses reveal that the Arabidopsis triphosphate tunnel metalloenzyme AtTTM3 is a tripolyphosphatase involved in root development. Plant J. 76, 615-626
27. Larivière, L., Geiger, S., Hoeppner, S., Röther, S., Strässer, K., and Cramer, P. (2006) Structure and TBP binding of the Mediator head subcomplex Med8-Med18-Med20. Nat. Struct. Mol. Biol. 13, 895-901
28. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800
29. Sheldrick, G. M. (2008) A short history of SHELX. Acta Crystallogr. A. 64, 112-122
30. Bricogne, G., Vonrhein, C., Flensburg, C., Schiltz, M., and Paciorek, W. (2003) Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D. Biol. Crystallogr. 59, 2023-2030
31. Terwilliger, T. C. (2003) SOLVE and RESOLVE: automated structure solution and density modification. Methods Enzymol. 374, 22-37
32. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126-2132
33. Winn, M. D., Isupov, M. N, and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D. Biol. Crystallogr. 57, 122-133
34. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C, and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
35. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N, Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
36. 32P-labeled or unlabeled nucleoside 5'-triphosphates and thiamine triphosphate. Anal. Biochem. 322, 190-197
37. Baykov, A. A., and Evtushenko., O. A., and Avaeva, S. M. (1988) A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal. Biochem. 171, 266-270
38. Cummings, M. D., and Farnum., M. A., and Nelen, M. I. (2006) Universal screening methods and applications of ThermoFluor. J. Biomol. Screen. 11, 854-863
39. Pei, Y., Schwer, B., Hausmann, S., and Shuman, S. (2001) Characterization of Schizosaccharomyces pombe RNA triphosphatase. Nucleic Acids Res. 29, 387-396
40. Martins, A., and Shuman, S. (2003) Mapping the triphosphatase active site of baculovirus mRNA capping enzyme LEF4 and evidence for a two-metal mechanism. Nucleic Acids Res. 31, 1455-1463
41. Gong, C, Martins, A., and Shuman, S. (2003) Structure-function analysis of Trypanosoma brucei RNA triphosphatase and evidence for a two-metal mechanism. J. Biol. Chem. 278, 50843-50852
42. Holm, L., and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138
43. Lakaye, B., and Makarchikov., A. F., Wins, P., Margineanu, I., Roland, S., Lins, L., Aichour, R., Lebeau, L., El Moualij, B., Zorzi, W., Coumans, B., Grisar, T., and Bettendorff, L. (2004) Human recombinant thiamine triphosphatase: purification, secondary structure, and catalytic properties. Int. J. Biochem. Cell Biol. 36, 1348-1364
44. Tesmer, J. J., and Sunahara., R. K., Johnson, R. A., Gosselin, G., Gilman, A. G., and Sprang, S. R. (1999) Two-metal-ion catalysis in adenylyl cyclase. Science 285, 756-760
45. Steitz, T. A. (1998) Structural biology: a mechanism for all polymerases. Nature 391, 231-232
46. Castro, C, and Smidansky., E. D., Arnold, J. J., Maksimchuk, K. R., Moustafa, I., Uchida, A., Götte, M., Konigsberg, W., and Cameron, C. E. (2009) Nucleic acid polymerases use a general acid for nucleotidyl transfer. Nat. Struct. Mol. Biol. 16, 212-218