Structural studies and protein engineering of inositol phosphate multikinase

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35360-35369

  Endo Streeter, Stuart ^a   Tsui, Man Kin Marco ^a   Odom, Audrey R ^a,b   Block, Jeremy ^a   York, John D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE ARCHITECTURE; ARABIDOPSIS THALIANA; BIOLOGICAL APPROACH; CELLULAR SIGNALING; GROWTH DEFECTS; IN-VIVO; INOSITOL PHOSPHATE; INOSITOL PHOSPHATE SIGNALING; METABOLIC LABELING; PHOSPHOLIPASE C ACTIVATIONS; PROTEIN ENGINEERING; SEQUENCE IDENTITY; STEADY-STATE KINETICS; STRUCTURAL COMPARISON; STRUCTURAL STUDIES; SUBSTRATE MODELING; SUBSTRATE SPECIFICITY; YEAST STRAIN;

ENZYMES; GENETIC ENGINEERING; PHOSPHORYLATION; PLANTS (BOTANY); SUBSTRATES; SUGARS; YEAST;

ALCOHOLS;

INOSITOL 1,3,4,5 TETRAKISPHOSPHATE; INOSITOL 1,3,4,6 TETRAKISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5,6 TETRAKISPHOSPHATE; INOSITOL PHOSPHATE; INOSITOL PHOSPHATE KINASE 2; INOSITOL PHOSPHATE MULTIKINASE; INOSITOL TRISPHOSPHATE 3 KINASE; POLYASPARTIC ACID; PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARABIDOPSIS; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTALLIZATION; DROSOPHILA MELANOGASTER; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; MALE; NITROGEN METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STEADY STATE; STRUCTURE ANALYSIS; SYNTHETIC BIOLOGY;

AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MUTATION, MISSENSE; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84867423671     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.365031     Document Type: Article

References (42)

1. Drin, G., and Scarlata, S. (2007) Stimulation of phospholipase Cβ by membrane interactions, interdomain movement, and G protein binding-how many ways can you activate an enzyme? Cell Signal. 19, 1383-1392 (Pubitemid 46818926)
2. Gonzales, M. L., and Anderson, R. A. (2006) Nuclear phosphoinositide kinases and inositol phospholipids. J. Cell Biochem. 97, 252-260 (Pubitemid 43167143)
3. Irvine, R. F. (2005) Inositide evolution-towards turtle domination? J. Physiol. 566, 295-300
4. Blazer-Yost, B. L., and Nofziger, C. (2005) Phosphoinositide lipid second messengers: New paradigms for transepithelial signal transduction. Pflugers Arch. 450, 75-82 (Pubitemid 40674731)
5. Hatch, A. J., and York, J. D. (2010) SnapShot: Inositol phosphates. Cell 143, 1030-1030.e1
6. York, J. D. (2006) Regulation of nuclear processes by inositol polyphosphates. Biochim. Biophys. Acta 1761, 552-559
7. Seeds, A. M., Bastidas, R. J., and York, J. D. (2005) Molecular definition of a novel inositol polyphosphate metabolic pathway initiated by inositol 1,4,5-trisphosphate 3-kinase activity in Saccharomyces cerevisiae. J. Biol. Chem. 280, 27654-27661 (Pubitemid 41076878)
8. Bechet, J., Greenson, M., and Wiame, J. M. (1970) Mutations affecting the repressibility of arginine biosynthetic enzymes in Saccharomyces cerevisiae. Eur. J. Biochem. 12, 31-39
9. Dubois, E., and Messenguy, F. (1994) Pleiotropic function of ArgRIIIp (Arg82p), one of the regulators of arginine metabolism in Saccharomyces cerevisiae. Role in expression of cell-type-specific genes. Mol. Gen. Genet. 243, 315-324 (Pubitemid 24151991)
10. Messenguy, F., Dubois, E., and Boonchird, C. (1991) Determination of the DNA-binding sequences of ARGR proteins to arginine anabolic and catabolic promoters. Mol. Cell Biol. 11, 2852-2863 (Pubitemid 21895667)
11. Dubois, E., and Messenguy, F. (1985) Isolation and characterization of the yeast ARGRII gene involved in regulating both anabolism and catabolism of arginine. Mol. Gen. Genet. 198, 283-289 (Pubitemid 15141829)
12. Odom, A. R., Stahlberg, A., Wente, S. R., and York, J. D. (2000) A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 287, 2026-2029 (Pubitemid 30158681)
13. York, J. D., Odom, A. R., Murphy, R., Ives, E. B., and Wente, S. R. (1999) A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 285, 96-100 (Pubitemid 29307573)
14. Stevenson-Paulik, J., Odom, A. R., and York, J. D. (2002) Molecular and biochemical characterization of two plant inositol polyphosphate 6-/3-/5-kinases. J. Biol. Chem. 277, 42711-42718 (Pubitemid 35285642)
15. Stevenson-Paulik, J., Bastidas, R. J., Chiou, S. T., Frye, R. A., and York, J. D. (2005) Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc. Natl. Acad. Sci. U.S.A. 102, 12612-12617 (Pubitemid 41266407)
16. Holmes, W., and Jogl, G. (2006) Crystal structure of inositol phosphate multikinase 2 and implications for substrate specificity. J. Biol. Chem. 281, 38109-38116 (Pubitemid 46042114)
17. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L., and Clardy, J. (1993) XDS atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105-124 (Pubitemid 23037917)
18. Kabsch, W. (1993) XDS automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Cryst. 26, 795-800
19. Sheldrick, G. M. (1997) SHELX97 Manual, University of Gottingen, Germany
20. Brünger, 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., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography &NMRsystem: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
21. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New York
22. Chamberlain, P. P., Sandberg, M. L., Sauer, K., Cooke, M. P., Lesley, S. A., and Spraggon, G. (2005) Structural insights into enzyme regulation for inositol 1,4,5-trisphosphate 3-kinase B. Biochemistry 44, 14486-14493 (Pubitemid 41567457)
23. Miller, G. J., and Hurley, J. H. (2004) Crystal structure of the catalytic core of inositol 1,4,5-trisphosphate 3-kinase. Mol. Cell 15, 703-711 (Pubitemid 39194901)
24. González, B., Schell, M. J., Letcher, A. J., Veprintsev, D. B., Irvine, R. F., and Williams, R. L. (2004) Structure of a human inositol 1,4,5-trisphosphate 3-kinase: Substrate binding reveals why it is not a phosphoinositide 3-kinase. Mol. Cell 15, 689-701 (Pubitemid 39194900)
25. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr.DBiol. Crystallogr. 50, 760-763
26. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119
27. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
28. Lovell, S. C., Davis, I. W., Arendall, W. B., 3rd, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry: φ, ψ, and Cβ deviation. Proteins 50, 437-450
29. 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 (Pubitemid 32062682)
30. Davis, I. W., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2004) MOLPROBITY: Structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32, W615-619 (Pubitemid 38997409)
31. Kleywegt, G. J. (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D Biol. Crystallogr. 52, 842-857
32. Seeds, A. M., Sandquist, J. C., Spana, E. P., and York, J. D. (2004) A molecular basis for inositol polyphosphate synthesis in Drosophila melanogaster. J. Biol. Chem. 279, 47222-47232 (Pubitemid 39518379)
33. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168 (Pubitemid 13119852)
34. Stolz, L. E., Huynh, C. V., Thorner, J., and York, J. D. (1998) Identification and characterization of an essential family of inositol polyphosphate 5-phosphatases (INP51, INP52, and INP53 gene products) in the yeast Saccharomyces cerevisiae. Genetics 148, 1715-1729 (Pubitemid 28180699)
35. Matthews, B. W. (1968) Solvent content of protein crystals. J. Mol. Biol. 33, 491-497
36. Murzin, A. G. (1996) Structural classification of proteins: New superfamilies. Curr. Opin. Struct. Biol. 6, 386-394
37. Fan, C., Moews, P. C., Shi, Y., Walsh, C. T., and Knox, J. R. (1995) A common fold for peptide synthetases cleaving ATP to ADP: Glutathione synthetase and D-alanine:D-alanine ligase of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92, 1172-1176
38. Chang, S. C., and Majerus, P. W. (2006) Inositol polyphosphate multikinase regulates inositol 1,4,5,6-tetrakisphosphate. Biochem. Biophys. Res. Commun. 339, 209-216
39. Ongusaha, P. P., Hughes, P. J., Davey, J., and Michell, R. H. (1998) Inositol hexakisphosphate in Schizosaccharomyces pombe: Synthesis from Ins(1,4,5)P3 and osmotic regulation. Biochem. J. 335, 671-679 (Pubitemid 28515423)
40. Ives, E. B., Nichols, J., Wente, S. R., and York, J. D. (2000) Biochemical and functional characterization of inositol 1,3,4,5,6- pentakisphosphate 2-kinases. J. Biol. Chem. 275, 36575-36583 (Pubitemid 32002056)
41. Dubois, E., Dewaste, V., Erneux, C., and Messenguy, F. (2000) Inositol polyphosphate kinase activity of Arg82/ArgRIII is not required for the regulation of the arginine metabolism in yeast. FEBS Lett. 486, 300-304
42. Watson, P. J., Fairall, L., Santos, G. M., and Schwabe, J. W. (2012) Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature 481, 335-340