Electron microscopy analysis of mammalian phosphofructokinase reveals an unusual 3-dimensional structure with significant implications for enzyme function

FASEB Journal

Volumn 24, Issue 12, 2010, Pages 4960-4968

  Arechaga, Ignacio ^a,b   Martínez Costa, Oscar H ^a   Ferreras, Cristina ^a,c   Carrascosa, José L ^a   Aragón, Juan J ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF CANTABRIA   (Spain)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

3 D reconstruction; Allostery; Enzyme regulation; Glycolysis; Structure function relationships

Indexed keywords

6 PHOSPHOFRUCTOKINASE; FRUCTOSE 6 PHOSPHATE;

ARTICLE; BACTERIAL CELL; BINDING SITE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE;

HUMANS; MICROSCOPY, ELECTRON, SCANNING; MODELS, MOLECULAR; MUSCLE PROTEINS; PHOSPHOFRUCTOKINASE-1, MUSCLE TYPE; PHOSPHOFRUCTOKINASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 78649736823     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-165845     Document Type: Article

References (57)

1. Uyeda, K. (1979) Phosphofructokinase. Adv. Enzymol. Relat. Areas. Mol. Biol. 48, 193-244
2. Sols, A. (1981) Multimodulation of enzyme activity. Curr. Top. Cell Regul. 19, 77-101
3. Kemp, R. G., and Foe, L. G. (1983) Allosteric regulatory properties of muscle phosphofructokinase. Mol. Cell. Biochem. 57, 147-154
4. Colombo, G., Tate, P. W., Girotti, A. W., and Kemp, R. G. (1975) Interaction of inhibitors with muscle phosphofructokinase. J. Biol. Chem. 250, 9404-9412
5. Van Schaftingen, E. (1987) Fructose 2,6-bisphosphate. Adv. Enzymol. Relat. Areas Mol. Biol. 59, 315-395
6. Reinhart, G. D., and Lardy, H. A. (1980) Rat liver phosphofructokinase: kinetic under near-physiological conditions. Biochemistry 19, 1477-1484
7. Aragón, J. J., and Sols, A. (1991) Regulation of enzyme activity in the cell: Effect of enzyme concentration. FASEB J. 5, 2945-2950
8. Blangy, D., Buc, H., and Monod, J. (1968) Kinetics of the allosteric interactions of phosphofructokinase from Escherichia coli. J. Mol. Biol. 31, 13-35
9. Foe, L. G., and Kemp, R. G. (1985) Isolation and characterization of phosphofructokinase C from rabbit brain. J. Biol. Chem. 260, 726-730
10. Sánchez-Martínez, C., Estévez, A. M., and Aragón, J. J. (2000) Phosphofructokinase C isozyme from ascites tumor cells: cloning, expression, and properties. Biochem. Biophys. Res. Commun. 271, 635-640
11. Dunaway, G. A., Kasten, T. P., Sebo, T., and Trapp, R. (1988) Analysis of the phosphofructokinase subunits and isoenzymes in human tissues. Biochem. J. 251, 677-683
12. Hesterberg, L. K., and Lee, J. C. (1980) Sedimentation study of a catalytically active form of rabbit muscle phosphofructokinase at pH 8.55. Biochemistry 19, 2030-2039
13. Schirmer, T., and Evans, P. R. (1990) Structural basis of the allosteric behaviour of phosphofructokinase. Nature 343, 140-145
14. Poorman, R. A., Randolph, A., Kemp, R. G., and Heinrikson, R. L. (1984) Evolution of phosphofructokinase-gene duplication and creation of new effector sites. Nature 309, 467-469
15. Heinisch, J. J., Boles, E., and Timple, C. (1996) A yeast phosphofructokinase insensitive to the allosteric activator fructose 2,6-bisphosphate. J. Biol. Chem. 271, 15928-15933
16. Li, Y., Rivera, D., Ru, W., Gunasekera, D., and Kemp, R. G. (1999) Identification of allosteric sites in rabbit phosphofructo-1-kinase. Biochemistry 38, 16407-16412
17. Kemp, R. G., and Gunasekera, D. (2002) Evolution of the allosteric ligand sites of mammalian phosphofructo-1-kinase. Biochemistry 41, 9426-9430
18. Martínez-Costa, O. H., Sánchez-Martínez, C., Sánchez, V., and Aragón, J. J. (2007) Chimeric phosphofructokinases involving exchange of the N- and C-terminal halves of mammalian isozymes: implications for ligand binding sites. FEBS Lett. 581, 3033-3038
19. Ferreras, C., Hernández, E. D., Martínez-Costa, O. H., and Aragón, J. J. (2009) Subunit interactions and composition of the fructose 6-phosphate catalytic site and the fructose 2,6-bisphosphate allosteric site of mammalian phosphofructokinase. J. Biol. Chem. 284, 9124-9131
20. Auzat, I., Byrnes, W. M., Garel, J.-R., and Chang, S. (1995) Role of residue 161 in the allosteric transitions of two bacterial phosphofructokinases. Biochemistry 34, 7062-7068
21. Auzat, I., Le Bras, G., and Garel, J.-R. (1997) Allosteric activation increases the maximum velocity of E. coli phosphofructokinase. J. Mol. Biol. 267, 476-480
22. Ortigosa, A. D., Kimmel, J. L., and Reinhart, G. D. (2004) Disentangling the web of allosteric communication in a homotetramer: heterotropic inhibition of phosphofructokinase from Bacillus stearothermophilus. Biochemistry 43, 577-586
23. Martinez-Oyanedel, J., McNae, I. W., Nowicki, M. W., Keillor, J. W., Michels, P. A., Fothergill-Gilmore, L. A., and Walkinshaw, M. D. (2007) The first crystal structure of phosphofructokinase from a eukaryote: Trypanosoma brucei. J. Mol. Biol. 366, 1185-1198
24. Ruiz, T., Kopperschläger, G., and Radermacher, M. (2001) The first three-dimensional structure of phosphofructokinase from Saccharomyces cerevisiae determined by electron microscopy of single particles. J. Struct. Biol. 136, 167-180
25. Ruiz, T., Mechin, I., Bär, J., Rypniewski, W., Kopperschläger, G., and Radermacher, M. (2003) The 10.8-A structure of Saccharomyces cerevisiae phosphofructokinase determined by cryoelectron microscopy: localization of the putative fructose 6-phosphate binding sites. J. Struct. Biol. 143, 124-134
26. Bárcena, M., Radermacher, M., Bär, J., Kopperschläger, G., and Ruiz, T. (2007) The structure of the ATP-bound state of S. cerevisiae phosphofructokinase determined by cryo-electron microscopy. J. Struct. Biol. 159, 135-143
27. Foe, L. G., and Trujillo, J. L. (1980) Quaternary structure of pig liver phosphofructokinase. J. Biol. Chem. 255, 10537-10541
28. Hesterberg, L. K., Lee, J. C., and Erickson, H. P. (1981) Structural properties of an active form of rabbit muscle phosphofructokinase. J. Biol. Chem. 256, 9724-9730
29. Martínez-Costa, O. H., Hermida, C., Sánchez- Martínez, C., Santamaria, B., and Aragón, J. J. (2004) Identification of C-terminal motifs responsible for transmission of inhibition by ATP of mammalian phosphofructokinase, and their contribution to other allosteric effects. Biochem. J. 377, 77-84
30. Santamaría, B., Estévez, A. M., Martínez-Costa, O. H., and Aragón, J. J. (2002) Creation of an allosteric phosphofructokinase starting with a nonallosteric enzyme. The case of Dictyostelium discoideum phosphofructokinase. J. Biol. Chem. 277, 1210-1216
31. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
32. Mindell, J. A., and Grigorieff, N. (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347
33. Heymann, J. B. (2001) Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133, 156-169
34. Sorzano, C. O., Marabini, R., Velazquez-Muriel, J., Bilbao-Castro, J. R., Scheres, S. H., Carazo, J. M., and Pascual-Montano, A. (2004) XMIPP: a new generation of an open-source image processing package for electron microscopy. J. Struct. Biol. 148, 194-204
35. Scheres, S. H., Nunez-Ramirez, R., Sorzano, C. O., Carazo, J. M., and Marabini, R. (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc. 3, 977-990
36. Pascual-Montano, A., Donate, L. E., Valle, M., Barcena, M., Pascual-Marqui, R. D., and Carazo, J. M. (2001) A novel neural network technique for analysis and classification of EM single-particle images. J. Struct. Biol. 133, 233-245
37. Scheres, S. H., Valle, M., Nunez-Ramirez, R., Sorzano, C. O., Marabini, R., Herman, G. T., and Carazo, J. M. (2005) Maximum-likelihood multi-reference refinement for electron microscopy images. J. Mol. Biol. 348, 139-149
38. Scheres, S. H., Nunez-Ramirez, R., Gomez-Llorente, Y., San Martin, C., Eggermont, P. P., and Carazo, J. M. (2007) Modeling experimental image formation for likelihood-based classification of electron microscopy data. Structure 15, 1167-1177
39. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97
40. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera -a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
41. Evans, P. R., Farrants, G. W., and Hudson, P. J. (1981) Phosphofructokinase: structure and control. Philos. Trans. R. Soc. Lond. B Biol. Sci. 293, 53-62
42. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
43. Wriggers, W., Milligan, R. A., and McCammon, J. A. (1999) Situs: A package for docking crystal structures into low-resolution maps from electron microscopy. J. Struct. Biol. 125, 185-195
44. Parmeggiani, A., Luft, J. H., Love, D. S., and Krebs, E. G. (1966) Crystallization and properties of rabbit skeletal muscle phosphofructokinase. J. Biol. Chem. 241, 4625-4637
45. Telford, J. N., Lad, P. M., and Hammes, G. G. (1975) Electron microscope study of native and crosslinked rabbit muscle phosphofructokinase. Proc. Natl. Acad. Sci. U. S. A. 72, 3054-3056
46. Kono, N., Uyeda, K., and Oliver, R. M. (1973) Chicken liver phosphofructokinase. I. Crystallization and physicochemical properties. J. Biol. Chem. 248, 8592-8602
47. Karadsheh, N. S., Uyeda, K., and Oliver, R. M. (1977) Studies on structure of human erythrocyte phosphofructokinase. J. Biol. Chem. 252, 3515-3524
48. Martínez-Costa, O. H., Estévez, A. M., Sánchez, V., and Aragón, J. J. (1994) Purification and properties of phosphofructokinase from Dictyostelium discoideum. Eur. J. Biochem. 226, 1007-1017
49. Kemp, R. G., and Krebs, E. G. (1967) Binding of metabolites by phosphofructokinase. Biochemistry 6, 423-434
50. Hill, D. E., and Hammes, G. G. (1975) An equilibrium binding study of the interaction of fructose 6-phosphate and fructose 1,6-bisphosphate with rabbit muscle phosphofructokinase. Biochemistry 14, 203-213
51. Kitajima, S., and Uyeda, K. (1983) A binding study of the interaction of beta-D-fructose 2,6-bisphosphate with phosphofructokinase and fructose-1,6-bisphosphatase. J. Biol. Chem. 258, 7352-7357
52. Monod, J., Wyman, J., and Changeux, J.-P. (1965) On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118
53. Benjamin, S., Radermacher, M., Bär, J., Edelmann, A., and Ruiz, T. (2007) Structures of S. pombe phosphofructokinase in the F6P-bound and ATP-bound states. J. Struct. Biol. 159, 498-506
54. Benjamin, S., Radermacher, M., Kirchberger, J., Schöneberg, T., Edelmann, A., and Ruiz, T. (2009) 3D structure of phosphofructokinase from Pichia pastoris: Localization of the novel gamma-subunits. J. Struct. Biol. 168, 345-351
55. Kopperschläger, G., Freyer, R., Diezel, W., and Hofmann, E. (1968) Some kinetic and molecular properties of yeast phosphofructokinase. FEBS Lett. 1, 137-141
56. Bañuelos, M., Gancedo, C., and Gancedo, J. M. (1977) Activation by phosphate of yeast phosphofructokinase. J. Biol. Chem. 252, 6394-6398
57. Frieden, C., Gilbert, H. R., and Bock, P. (1976) E. Phosphofructokinase. III. Correlation of the regulatory kinetic and molecular properties of the rabbit muscle enzyme. J. Biol. Chem. 251, 5644-5647