NMR measurements of the rotational mobility of proteins in vivo

Biophysical Journal

Volumn 72, Issue 1, 1997, Pages 490-498

  Williams, Simon Peter ^a   Haggie, Peter M ^a   Brindle, Kevin M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORINE; GLYCOLYTIC ENZYME; HEXOKINASE; PHOSPHOGLYCERATE KINASE; PYRUVATE KINASE; RECOMBINANT PROTEIN;

ARTICLE; CALCULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; RELAXATION TIME; ROTATION; SACCHAROMYCES CEREVISIAE; CHEMISTRY; ENZYMOLOGY; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; THEORETICAL MODEL; VISCOSITY;

SACCHAROMYCES CEREVISIAE;

FLUORINE; HEXOKINASE; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, THEORETICAL; PHOSPHOGLYCERATE KINASE; PROTEIN CONFORMATION; PYRUVATE KINASE; RECOMBINANT PROTEINS; ROTATION; SACCHAROMYCES CEREVISIAE; VISCOSITY;

EID: 0030614424     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78690-9     Document Type: Article

References (84)

1. Abragam, A. 1961. The Principles of Nuclear Magnetism. Oxford University Press, Oxford, UK.
2. Aragon, J. J., and A. Sols. 1991. Regulation of enzyme activity in the intact cell: effect of enzyme concentration. FASEB J. 5:2945-2950.
3. Batke, J. 1989. Remarks on the supramolecular organization of the glycolytic system in vivo. FEBS Lett. 251:13-16.
4. Beeckmans, S., E. Van Driessche, and L. Kanarek. 1990. Clustering of sequential enzymes in the glycolytic pathway and the citric acid cycle. J. Cell. Biochem. 43:297-306.
5. Bicknese, S., N. Periasamy, S. B. Shohet, and A. S. Verkman. 1993. Cytoplasmic viscosity near the cell plasma membrane: measurement by evanescent field frequency-domain microfluorimetry. Biophys. J. 65: 1272-1282.
6. 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.
7. 31P NMR magnetization-transfer measurements of flux between inorganic phosphate and adenosine 5′-triphosphate in yeast cells genetically modified to overproduce phosphoglycerate kinase. Biochemistry. 27:6187-6196.
8. 31P-NMR saturation transfer measurements of phosphate consumption in Saccharomyces cerevisiae. Biochim. Biophys. Acta. 847:285-292.
9. 19F NMR detection of a fluorine-labelled enzyme in vivo. FEBS Lett. 255:121-124.
10. Brooks, S. P. J., and K. B. Storey. 1991a. A quantitative evaluation of the effect of enzyme complexes on the glycolytic rate in vivo: mathematical modeling of the glycolytic complex. J. Theor. Biol. 149:361-375.
11. Brooks, S. P. J., and K. B. Storey. 1991b. Where is the glycolytic complex? A critical evaluation of present data from muscle tissue. FEBS Lett. 278:135-138.
12. Burns, V. W. 1969. Measurement of viscosity in living cells by a fluorescence method. Biochem. Biophys. Res. Commun. 37:1008-1014.
13. 13C spin-lattice relaxation measurements by inversion recovery. J. Magn. Reson. 18: 199-204.
14. Cantor, C. R., and P. R. Shimmel. 1980. Biophysical Chemistry. W. H. Freeman & Co., San Francisco, CA.
15. Cerek, L., and B. Cerek. 1976. Effects of osmolarity, calcium and magnesium ions on the structuredness of cytoplasmic matrix. Radiat. Environ. Biophys. 13:9-12.
16. Cornish-Bowden, A. 1991. Failure of channelling to maintain low concentrations of metabolic intermediates. Eur. J. Biochem. 195:103-108.
17. Cousens, D. J., M. J. Wilson, and E. Hinchcliffe. 1990. Construction of a regulated PGK expression vector. Nucleic Acids Res. 18:1308.
18. CRC Handbook of Chemistry and Physics. R. C. Weast, editor. 1978. CRC Press, Inc., West Palm Beach, FL.
19. Derechin, M., Y. M. Rustum, and E. A. Barnard. 1972. Dissociation of yeast hexokinase under the influence of its substrates. Biochemistry. 11:1793-1797.
20. Dix, J. A., and A. S. Verkman. 1990. Mapping of fluorescence anisotropy in living cells by ratio imaging. Application to cytoplasmic viscosity. Biophys. J. 57:231-240.
21. 13C n.m.r. Biochem. J. 216:655-660.
22. Fabry, M. E., and R. C. San George. 1983. Effect of magnetic susceptibilty on nuclear magnetic resonance signals arising from red cells: a warning. Biochemistry. 22:4119-4125.
23. Fifis, T., and R. K. Scopes. 1978. Purification of 3-phosphoglycerate kinase from diverse sources by affinity elution chromatography. Biochem. J. 175:311-319.
24. Freifelder, D. 1982. Physical Biochemistry. W. H. Freeman & Co., San Francisco, CA.
25. Fröhlich, K.-U., K.-D. Entian, and D. Mecke. 1985. The primary structure of the yeast hexokinase PII gene (HXK2) which is responsible for glucose repression. Gene. 36:105-111.
26. Fulton, A. B. 1982. How crowded is the cytoplasm? Cell. 30:345-347.
27. Fushimi, K., and A. S. Verkman. 1991. Low viscosity in the aqueous domain of cell cytoplasm measured by picosecond polarization microfluorimetry. J. Cell Biol. 112:719-725.
28. Gancedo, J. M., and C. Gancedo. 1973. Concentrations of intermediary metabolites in yeast. Biochimie. 55:205-211.
29. Gerig, J. T. 1994. Fluorine NMR of proteins. Prog. Nucl. Magn. Reson. Spectrosc. 26:293-370.
30. Gershon, N. L., K. R. Porter, and B. L. Trus. 1985. The cytomatrix - its volume and surface area and the diffusion of molecules through it. Proc. Natl. Acad. Sci. USA. 82:5030-5034.
31. Goodsell, D. S. 1991. Inside a living cell. Trends Biochem. Sci. 16: 203-206.
32. Hinnen, A., J. B. Hicks, and G. R. Fink. 1978. Transformation of yeast. Proc. Natl. Acad. Sci. USA. 75:1929-1933.
33. Ho, C., E. A. Pratt, and G. S. Rule. 1989. Membrane-bound D-lactate dehydrogenase of Escherichia coli: a model for protein interactions in membranes. Biochim. Biophys. Acta. 988:173-184.
34. Hoggett, J. G., and G. L. Kellett. 1976. Yeast hexokinase: substrate-induced association-dissociation reactions in the binding of glucose to hexokinase P-II. Eur. J. Biochem. 66:65-77.
35. Hou, L., F. Lanni, and K. Luby-Phelps. 1990. Tracer diffusion in F-actin and Ficoll mixtures. Biophys. J. 58:31-43.
36. Hubley, M. J., R. C. Rosanske, and T. S. Moerland. 1995. Diffusion coefficients of ATP and creatine phosphate in isolated muscle: pulsed gradient 31P NMR of small biological samples. Nucl. Magn. Reson. Biomed. 8:72-78.
37. 19F in multispin systems. Application to 19F labeled proteins. J. Chem. Phys. 63:867-880.
38. 19F nuclear spin relaxation mechanism in proteins. J. Mol. Biol. 98:121-153.
39. Jacob, L., V. Beecken, and P. Bartunik. 1991. Purification and crystallisation of yeast hexokinase isoenzymes - characterisation of different forms by chromatofocusing. J. Chromatogr. 587:85-92.
40. Jacobson, K., and J. Wojcieszyn. 1984. The translational mobility of substances within the cytoplasmic matrix. Proc. Natl. Acad. Sci. USA. 81:6747-6751.
41. Jones, E. W. 1990. Vacuolar proteases in yeast Saccharomyces cerevisiae. In Gene Expression Technology. D. V. Goeddel, editor. Academic Press, San Diego, CA. 372-386.
42. Kingsman, S. M., D. Cousens, C. A. Stanway, A. Chambers, W. M., and A. J. Kingsman. 1990. High efficiency yeast expression vectors based on the promoter of the phosphoglycetate kinase gene. In Gene Expression Technology. D. V. Goeddel, editor. Academic Press, San Diego, CA. 329-341.
43. Knull, H. R., and J. L. Walsh. 1992. Association of glycolytic enzymes with the cytoskeleton. Curr. Top. Cell Regul. 33:15-46.
44. Kovac, L., B. D. Nelson, and L. Ernster. 1986. A method for determining the intracellular distribution of enzymes in yeast provide no evidence for the association of hexokinae with mitochondria. Biochem. Biophys. Res. Commun. 134:285-291.
45. Kuchel, P. W., and B. E. Chapman. 1991. Translational diffusion of hemoglobin in erythrocytes and hemolysates. J. Magn. Reson. 94: 574-580.
46. Kvassman, J., and G. Petterson. 1989. Mechanism of 1,3-bisphosphoglycerate transfer from phosphoglycerate kinase to glyceraldehyde-3-phosphate dehydrogenase. Eur. J. Biochem. 186:265-272.
47. Lehotzky, A., M. Telegdi, K. Liliom, and J. Ov‡di. 1993. Interaction of phosphofructokinase with tubulin and microtubules. J. Biol. Chem. 268:10,888-10,894.
48. Lindmo, T., and H. B. Steen. 1977. Flow cytometric measurements of the polarization of fluorescence from intracellular fluorescein in mammalian cells. Biophys. J. 18:173-187.
49. Livingston, D. J., G. N. La Mar, and W. D. Brown. 1983. Myoglobin diffusion in bovine heart muscle. Science. 220:71-73.
50. Luby-Phelps, K. 1994. Physical properties of the cytoplasm. Curr. Opin. Cell Biol. 6:3-9.
51. Luby-Phelps, K., P. E. Castle, D. L. Taylor, and F. Lanni. 1987. Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells. Proc. Natl. Acad. Sci. USA. 84:4910-4913.
52. Luby-Phelps, K., F. Lanni, and D. L. Taylor. 1985. Behaviour of a fluorescent analogue of calmodulin in living 3T3 cells. J. Cell Biol. 101:1245-1256.
53. Luby-Phelps, K., S. Mujumdar, R. B. Mujumdar, L. A. Ernst, W. Galbraith, and A. S. Waggoner. 1993. A novel fluorescence ratiometric method confirms the low solvent viscosity of the cytoplasm. Biophys. J. 65: 236-242.
54. Lynch, R. M., K. E. Fogarty, and F. S. Fay. 1991. Modulation of hexokinase association with mitochondria analyzed with quantitative three-dimensional confocal microscopy. J. Cell Biol. 12:385-395.
55. Mastro, A. M., M. A. Babich, W. D. Taylor, and A. D. Keith. 1984. Diffusion of a small molecule in the cytoplasm of mammalian cells. Proc. Natl. Acad. Sci. USA. 81:3414-3418.
56. McNally, T., I. J. Purvis, L. A. Fothergill-Gilmore, and A. J. P. Brown. 1989. The yeast pyruvate kinase gene does not contain a string of non-preferred codons: revised nucleotide sequence. FEBS Lett. 247: 312-316.
57. Mendes, P., D. B. Kell, and H. V. Westerhoff. 1992. Channelling can decrease pool size. Eur. J. Biochem. 204:257-266.
58. Minton, A. P. 1992. Confinement as a determinant of macromolecular structure and reactivity. Biophys. J. 63:1090-1100.
59. Muirhead, H., D. A. Clayden, D. Barford, C. G. Lorimer, L. A. Fothergill-Gilmore, E. Schiltz, and W. Schmitt. 1986. The structure of cat muscle pyruvate kinase. EMBO J. 5:475-481.
60. Murcott, T. H. L., H. Gutfreund, and H. Muirhead. 1992. The cooperative binding of fructose-1,6-bisphosphate to yeast pyruvate kinase. EMBO J. 11:3811-3814.
61. Murcott, T. H. L., T. McNally, S. C. Allen, L. A. Fothergill-Gilmore, and H. Muirhead. 1991. Purification, characterisation and mutagenesis of highly expressed recombinant yeast pyruvate kinase. Eur. J. Biochem. 198:513-519.
62. Nefsky, B., and A. Bretscher. 1992. Yeast actin is relatively well behaved. Eur. J. Biochem. 206:949-955.
63. Ng, R., and J. Abelson. 1980. Isolation and sequence of the gene for actin in Saccharmoyces cerevisiae. Proc. Natl. Acad. Sci. USA. 77: 3912-3916.
64. Pagliaro, L., and D. L. Taylor. 1992. 2-deoxyglucose and cytochalasin D modulate aldolase mobility in living 3T3 cells. J. Cell Biol. 118: 859-863.
65. Post, J. F. M., P. F. Cottam, V. Simplaceanu, and C. Ho. 1984. Fluorine-19 nuclear magnetic resonance study of 5-fluorotryptophan-labeled histidine-binding protein J of Salmonella typhimurium. J. Mol. Biol. 179: 729-743.
66. Rule, G. S., E. A. Pratt, V. Simplaceanu, and C. Ho. 1987. Nuclear magnetic resonance and molecular genetic studies of the membrane-bound D-lactate dehydrogenase of Escherichia coli. Biochemistry. 26: 549-556.
67. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
68. Shearwin, K., C. Nanhua, and C. Masters. 1990. Interactions between glycolytic enzymes and cytoskeletal structure - the influence of ionic strength and molecular crowding. Biochem. Int. 21:53-60.
69. Shill, J. P., B. A. Peters, and K. E. Neet. 1974. Monomer-dimer equilibria of yeast hexokinase during reacting enzyme sedimentation. Biochemistry. 13:3864-3871.
70. Srere, P. A., and J. Ovadi. 1990. Enzyme-enzyme interactions and their metabolic role. FEBS Lett. 268:360-364.
71. Srivastava, D. K., and S. A. Bernhard. 1986. Enzyme-enzyme interactions and the regulation of metabolic reaction pathways. Curr. Top. Cell. Regul. 28:1-68.
72. Stejskal, E. O., and J. E. Tanner. 1965. Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J. Chem. Phys. 42:288-292.
73. Tao, T. 1969. Time-dependent fluorescence depolarization and Brownian rotational diffusion coefficients of macromolecules. Biopolymers. 8:609-632.
74. Van Holde, K. E. 1971. Physical Biochemistry. Prentice-Hall, Inc., Englewood Cliffs, NJ.
75. Vas, M., and J. Batke. 1990. Kinetic misinterpretaion of a coupled enzyme reaction can lead to the assumption of an enzyme-enzyme interaction. The example of 3-phospho-D-glycerate kinase and glyceraldehyde-3-phosphate dehydrogenase couple. Eur. J. Biochem. 191:679-683.
76. Walsh, J. L., T. J. Keith, and H. R. Knull. 1989. Glycolytic enzyme interactions with tubulin and microtubules. Biochim. Biophys. Acta. 999:64-70.
77. Watson, H. C., N. P. C. Walker, P. J. Shaw, T. N. Bryant, P. L. Wendell, L. A. Fothergill, R. E. Perkins, S. C. Conroy, M. J. Dobson, M. F. Tuite, A. J. Kingsman, and S. M. Kingsman. 1982. Sequence and structure of yeast phosphoglycerate kinase. EMBO J. 1:1635-1640.
78. Welch, M. D., D. A. Holtzman, and D. G. Drubin. 1994. The yeast actin cytoskeleton. Curr. Opin. Cell Biol. 6:110-119.
79. 19F NMR studies of fluorine-labeled yeast phosphoglycerate kinase in vivo. Biochemistry. 32: 4895-4902.
80. Wilson, H. R., R. J. P. Williams, J. A. Littlechild, and H. C. Watson. 1988. NMR analysis of the interdomain region of yeast phosphoglycerate kinase. Eur. J. Biochem. 170:529-538.
81. Wittebort, R. J., and A. Szabo. 1978. Theory of NMR relaxation in macromolecules: restricted diffusion and jump models for multiple internal rotations of amino acid side chains. J. Chem. Phys. 69: 1722-1736.
82. Woessner, D. T. 1962. Nuclear spin relaxation in ellipsoids undergoing rotational Brownian motion. J. Chem. Phys. 37:647-654.
83. Wojcieszyn, J. W., R. A. Schlegel, E. S. Wu, and K. A. Jacobson. 1981. Diffusion of injected macromolecules within the intact cell. Proc. Natl. Acad. Sci. USA. 78:4407-4410.
84. Wu, X., H. Gutfreund, S. Lakatos, and P. B. Chock. 1991. Substrate channeling in glycolysis: a phantom phenomenon. Proc. Natl. Acad. Sci. USA. 88:497-501.