Structural basis for the mechanism and substrate specificity of glycocyamine kinase, a phosphagen kinase family member

Biochemistry

Volumn 49, Issue 9, 2010, Pages 2031-2041

  Lim, Kap ^a   Pullalarevu, Sadhana ^a   Surabian, Karen Talin ^a   Howard, Andrew ^b   Suzuki, Tomohiko ^c   Moult, John ^a   Herzberg, Osnat ^a  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

^c KOCHI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ARGININE KINASE; BOUND STATE; COOPERATIVITY; CREATINE KINASE; DIMER INTERFACE; ENERGY HOMEOSTASIS; HETERODIMERS; HOMODIMER INTERFACE; INTERFACE FORMATION; KINASE FAMILY; LIGAND-FREE; N-TERMINALS; OPEN CONFORMATION; PHOSPHORYL GROUP TRANSFER; PHOSPHORYL GROUPS; POLYPEPTIDE CHAIN; PRE-MRNA; SEQUENCE HOMOLOGY; STRUCTURAL ASYMMETRY; STRUCTURAL BASIS; STRUCTURAL DETERMINANTS; SUBSTRATE SPECIFICITY; TRANSITION-STATE ANALOGUES; UNBOUND STATE;

AMINO ACIDS; BINDING SITES; CONFORMATIONS; DYES; ORGANIC ACIDS;

BINDING ENERGY;

ARGININE KINASE; CREATINE KINASE; GUANIDINOACETATE KINASE; PHOSPHAGEN KINASE; PHOSPHOTRANSFERASE; POLYPEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; HYDROGEN BOND; PRIORITY JOURNAL; WORM;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HUMANS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHOSPHOTRANSFERASES (NITROGENOUS GROUP ACCEPTOR); POLYCHAETA; RABBITS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

NAMALYCASTIS; SIPUNCULUS NUDUS;

EID: 77749289840     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi9020988     Document Type: Article

References (53)

1. Ellington, W. R. (2001) Evolution and physiological roles of phosphagen systems. Annu. Rev. Physiol. 63, 289-325.
2. McLeish, M. J., and Kenyon, G. L. (2005) Relating structure to mechanism in creatine kinase, Crit. Rev. Biochem. Mol. Biol. 40, 1-20.
3. 3.Suzuki,T.,andFurukohri,T.(1994)Evolution,ofPhosphagenkinase: primarystructureofglycocyaminekinaseandargininekinasefrom,invertebrates.J.Mol. Biol.237,353-357.(Pubitemid124002103)
4. Morrison, J. F. (1973) Arginine kinase and other invertebrate guanidino kinases, in The Enzymes (Boyer, P. C., Ed.) pp 457-486, Academic Press, New York.
5. Van Thoai, N. (1968) Homologous Phosphagen phosphokinases, in Homologous Enzymes and Biochemical Evolution (Van Thoai, N., and Roche, J., Eds.) pp 199-229, Gordon and Breach, New York.
6. 6. Ellington, W. R., Yamashita, D., and Suzuki, T. (2004) Alternative splicing produces transcripts coding for alpha and beta chains of a hetero-dimeric Phosphagen kinase. Gene 334, 167-174. (Pubitemid 38902726)
7. Ellington, W. R. (1989) Phosphocreatine represents a thermodynamic and functional improvement over other muscle Phosphagens. J. Exp. Biol. 143, 144-194.
8. 8. Arndt, C., and Schiedek, D. (1997) Nephtys hombergii, a free-living predator in marine sediments: energy production under environmental stress. Mar- Biol. 129, 643-650. (Pubitemid 27486548)
9. 9. Sona, S., Suzuki, T., and Ellington, W. R. (2004) Cloning and expression of mitochondrial and protoflagellar creatine kinases from a marine sponge: implications for the origin of intracellular energy transport systems, Biochem. Biophys. Res. Commun. 317, 1207-1214. (Pubitemid 38496439)
10. Tanaka, K., Uda, K., Shimada, M., Takahashi, K., Gamou, S., Ellington, W. R., and Suzuki, T. (2007) Evolution of the cytoplasmic and mitochondrial Phosphagen kinases unique to annelid groups. J. Mol. Evol. 65, 616-625. (Pubitemid 350115442)
11. Suzuki, T., Kamidochi, M., Inoue, N., Kawamichi, H., Yazawa, Y., Furukohri, T., and Ellington, W. R. (1999) Arginine kinase evolved twice: evidence that echinoderm arginine kinase originated from creatine kinase, Biochem. J. 340, 671-675. (Pubitemid 29312863)
12. Suzuki, T., Mizuta, C., Uda, K., Ishida, K., Mizuta, K., Sona, S., Compaan, D. M., and Ellington, W. R. (2004) Evolution and divergence of the genes for cytoplasmic, mitochondrial, and flagellar creatine kinases. J. Mol. Evol. 59, 218-226. (Pubitemid 39128344)
13. Pineda, A. O., and Ellington, W. R. (1999) Structural and functional implications of the amino acid sequences of dimeric, cytoplasmic and octameric mitochondrial creatine kinases from a protostome invertebrate. Eur J. Biochem. 264, 67-73.
14. Kaldis, P., and Wallimann, T. (1995) Functional differences between dimeric and octameric mitochondrial creatine kinase, Biochem. J. 308, 623-627.
15. Eder,M.,Schlatter,U.,Becker,A.,Wallimann,T.,Kabsch,W.,andFritz-Wolf,K. (1999)Crystalstructureofbrain-typecreatinekinaseat1.41Åresolution, ProteinSci.8,2258-2269.(Pubitemid29536392)
16. Lahiri, S. D., Wang, P. F., Babbitt, P. C., MicLeish, M. J., Kenyon, G. L., and Allen, K. N. (2001) The 2.1 Å structure of Torpedo californica creatine kinase complexed with, the ADP-Mg(2+)-NO(3)(-)-creatine transition-state analogue complex, Biochemistry 41, 13861-13867.
17. Ohren, J. F., Kundracik, M. L., Borders, C. L., Edmiston, P., and Viola, R. E. (2007) Structural, asymmetry and intersubunit communication in muscle creatine kinase, Acta Crystallogr. D63, 381-389. (Pubitemid 46438531)
18. Rao, J. K., Bujacz, G., and Wlodawer, A. (1998) Crystal structure of rabbit muscle creatine kinase. FEBS Lett. 439, 133-137. (Pubitemid 28537879)
19. Shen,Y.Q.,Tang,L.,Zhou,H.M.,andLin,Z.J.(2001) Structureofhumanmusclecreatinekinase.ActaCrystallogr.57,1196-1200. (Pubitemid32739543)
20. 20. Tisi, D., Bax, B., and Loew, A. (2001) The three-dimensional structure of cytosolic bovine retinal creatine kinase. Acta Crystallogr. 57, 187-193. (Pubitemid 32145396)
21. --creatine transitionstate analogue complex. FEBS Lett. 582, 3959-3965.
22. Degani, C., and Degani, Y. (1980) Further evidence for nonsymmetric subunit association and intersubunit cooperativity in creatine kinase. Subunit-selective modifications by 2,4-dinitrophenylthiocyanate. J. Biol. Chem. 255, 8221-8228.
23. Degani, Y., and Degani, C. (1979) Subunit-selective chemical modifications of creatine kinase. Evidence for asymmetrical association of the subunits. Biochemistry 18, 5917-5923.
24. 24. Homemann, T., Rutishauser, D., and Wallimann, T. (2000) Why is creatine kinase a dimer? Evidence for cooperativity between, the two subunits. Biochim. Biophys. Acta 1480, 365-373. (Pubitemid 30427414)
25. 25. Nevinsky, G. A., Ankilova, V. N., Lavrik, O. I., Mkrtchyan, Z. S., Nersesova, L. S., and Akopyan, J. I. (1982) Functional non-identity of creatine kinase subunits of rabbit skeletal muscle. FEBS Lett. 149, 36-40. (Pubitemid 13177095)
26. 26. Mazon, H., Marcillat, O., Forest, E., and Vial, C. (2003) Changes in MM-CK conformational mobility upon formation of the ADP-Mg(2+)-NO(3)(-)-creatine transition state analogue complex as detected by hydrogen/deuterium exchange, Biochemistry 42, 13596-13604. (Pubitemid 37444910)
27. Wang, X. C., Zhou, H. M., Wang, Z. X., and Tsou, C. L. (1990) Is the subunit the minimal function unit of creatine kinase? Biochim. Biophys. Acta 1039, 313-317.
28. Nallamsetty, S., Austin, B. P., Penrose, K. J., and Waugh, D. S. (2005) Gateway vectors for the production of combinatorially-tagged His6MBP fusion proteins in the cytoplasm and periplasm of Escherichia coli. Protein Sci. 14, 2964-2971.
29. 29. Mizuta, C., Tanaka, K., and Suzuki, T. (2005) Isolation, characterization, and cDNA-derived amino acid sequence of glycocyamine kinase from the tropical marine worm Namalycastis sp. Comp. Biochem. Physiol. B 140, 387-393. (Pubitemid 40208274)
30. 30. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
31. Howard, A. J. (2000) Data processing in macromolecular crystallography, in Crystallographic Computing 7: Proceedings from the Macromolecular Crystallographic Computing School (Bourne, P. E., and Watenpaugh, K. D., Eds.) Oxford University Press, Oxford.
32. MicCoy, A. J., Grosse-Kunstleve, R. W., Storoni, L. C., and Read, R. J. (2005) Likelihood-enhanced fast translation functions, Acta Cystallogr. D61, 458-464.
33. Storoni, L. C., McCoy, A. J., and Read, R. J. (2004) Likelihoodenhanced fast rotation functions, Acta Crystallogr. D60, 432-438.
34. 34. 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., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921. (Pubitemid 28443603)
35. Winn, M., D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement, Acta Crystallogr, D57, 122-133.
36. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination, Acta Crystallogr. D58, 1948-1954.
37. Jones, T. A. (2004) Interactive electron-density map interpretation: from INTER to O. Acta Crystallogr. D60, 2115-2125.
38. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. 60, 2126-2132. (Pubitemid 41742764)
39. Kraulis, P. J. (1991) A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
40. Bacon, D. J. (1988) A fast algorithm for rendering space-filling molecule pictures. J.Mol. Graphics 6, 219-220.
41. Merritt, E. A., and Bacon, D. J. (1997) Raster3D: Photorealistic molecular graphics. Methods Enzymol. 277, 505-524.
42. 42. Hayward, S., and Berendsen, H. J. (1998) Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 30, 144-154. (Pubitemid 28080149)
43. 43. Held, B. C., Wright-Weber, B., and Grossman, S. H. (2007) Kinetic analysis of two purified forms of arginine kinase: absence of cooperativity in substrate binding of dimeric Phosphagen kinase. Comp. Biochem. Physiol. B 148, 6-13. (Pubitemid 47089047)
44. Milner-White, E. J., and Watts, D. C. (1971) Inhibition of adenosine 5'-triphosphate-creatine phosphotransferase by substrate-anion complexes, Biochem. J. 122, 727-740.
45. 45. Borders, C. L., Snider, M., J., Wolfenden, R., and Edmiston, P. L. (2002) Determination of the affinity of each component of a composite quaternary transition-state analogue complex of creatine kinase. Biochemistry 41, 6995-7000. (Pubitemid 34575671)
46. 46. Yousef, M. S., Clark, S. A., Pruett, P. K., Somasundaram, T., Ellington, W. R., and Chapman, M. S. (2003) Induced fit in guanidino kinases-comparison of substrate-free and transition state analog structures of arginine kinase, Protein Sci. 12, 103-111. (Pubitemid 36020139)
47. 47. Yousef, M. S., Fabiola, F., Gattis, J. L., Somasundaram, T., and Chapman, M.S. (2002) Refinement of the arginine kinase transitionstate analogue complex at 1.2 Å resolution: mechanistic insights. Acta Cystallogr. 58, 2009-2017. (Pubitemid 35450822)
48. 48. Zhou, G., Somasundaram, T., Blanc, E., Parthasarathy, G., Ellington, W. R., and Chapman, M. S. (1998) Transition, state structure of arginine kinase: implications for catalysis of bimolecular reactions. Proc. Natl. Acad. Sci. U.S.A. 95, 8449-8454. (Pubitemid 28350508)
49. Knowles, J. R. (1980) Enzyme-catalyzed phosphoryl transfer reactions, Annu. Rev. Biochem. 49, 877-919.
50. Wang, P. F., Flynn, A. J., McLeish, M. J., and Kenyon, G. L. (2005) Loop movement and catalysis in creatine kinase. IUBMB Life 57, 355-362.
51. 51. Jourden, M. J., Clarke, C. N., Palmer, A. K., Barth, E. J., Prada, R. C. Hale, R. N., Fraga, D., Snider, M. J., and Edmiston, P. L. (2007) Changing the substrate specificity of creatine kinase from creatine to glycocyamine: evidence for a highly evolved active site. Biochim. Biophys. Acta 1774, 1519-1527. (Pubitemid 350235350)
52. 52. Azzi, A., Clark, S. A., Ellington, W. R., and Chapman, M. S. (2004) The role of Phosphagen specificity loops in arginine kinase, Protein Sci-13, 575-585. (Pubitemid 38252554)
53. Sonnhammer, E. L., and Hollich, V. (2005) Scoredist: a simple and robust protein sequence distance estimator. BMC Bioinf. 6, 108.