The C1-C2 interface residue lysine 50 of pig kidney fructose-1,6- bisphosphatase has a crucial role in the cooperative signal transmission of the AMP inhibition

European Journal of Biochemistry

Volumn 267, Issue 8, 2000, Pages 2242-2251

  Cárcamo, Juan G ^a   Yañez, Alejandro J ^a   Ludwig, Heide C ^a   León, Oscar ^a   Pinto, Rodrigo O ^a   Reyes, Alejandro M ^a   Slebe, Juan C ^a  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

AMP inhibition; Cooperativity; FBPase; Fructose 1,6 bisphosphatase; Site directed mutagenesis

Indexed keywords

ADENOSINE PHOSPHATE; DNA FRAGMENT; FRUCTOSE BISPHOSPHATASE; LYSINE; MAGNESIUM ION; MUTANT PROTEIN;

ARTICLE; ENZYME PURIFICATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; KIDNEY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SWINE;

ADENOSINE MONOPHOSPHATE; ALLOSTERIC REGULATION; ANIMALS; BINDING SITES; ENZYME INHIBITORS; ENZYME STABILITY; ESCHERICHIA COLI; FRUCTOSE-BISPHOSPHATASE; FRUCTOSEDIPHOSPHATES; KIDNEY; KINETICS; MAGNESIUM; MUTAGENESIS, SITE-DIRECTED; RECOMBINANT PROTEINS; SWINE; TEMPERATURE;

ESCHERICHIA COLI; FELIS CATUS; SUS SCROFA;

EID: 0034096111     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01227.x     Document Type: Article

References (52)

1. 1. Benkovic, S.J. & de Maine, M.M. (1982) Mechanism of action of fructose 1,6-bisphosphatase. Adv. Enzymol. 53, 45-82.
2. 2. Tejwani, G.A. (1983) Regulation of fructose-1,6-bisphosphatase activity. Adv. Enzymol. 54, 121-194.
3. 3. Marcus, F., Edelstein, I., Reardon, I. & Heinrikson, R.L. (1982) Complete amino acid sequence of pig kidney fructose-1,6-bisphosphatase. Proc. Natl Acad. Sci. USA 79, 7161-7165.
4. 4. Williams, M.K. & Kantrowitz, E.R. (1992) Isolation and sequence analysis of the cDNA for pig kidney fructose 1,6-bisphosphatase. Proc. Natl Acad. Sci. USA 89, 3080-3082.
5. 5. Pilkis, S.J. & Claus, T.H. (1991) Hepatic gluconeogenesis/glycolysis: regulation and structure/function relationships of substrate cycle enzymes. Annu. Rev. Nutr. 11, 465-515.
6. 6. Taketa, K. & Pogell, B.M. (1965) Allosteric inhibition of rat liver fructose 1,6-diphosphatase by adenosine 5'-monophosphate. J. Biol. Chem. 240, 651-662.
7. 7. Ke, H.M., Thorpe, C.M., Seaton, B.A., Lipscomb, W.N. & Marcus, F. (1990) Structure refinement of fructose-1,6-bisphosphatase and its fructose 2,6-bisphosphate complex at 2.8 Å resolution. J. Mol. Biol. 212, 513-539.
8. 8. Zhang, Y., Liang, J.-Y., Huang, S. & Lipscomb, W.N. (1994) Toward a mechanism for the allosteric transition of pig kidney fructose-1,6-bisphosphatase. J. Mol. Biol. 244, 609-624.
9. 9. Pilkis, S.J., El-Maghrabi, M.R., Pilkis, J. & Claus, T. (1981) Inhibition of fructose-1,6-bisphosphatase by fructose-2,6-bisphosphate. J. Biol. Chem. 256, 3619-3622.
10. 10. Van Schaftingen, E. & Hers, H.-G. (1981) Inhibition of fructose-1,6-bisphosphatase by fructose-2,6-bisphosphate. Proc. Natl Acad. Sci. USA 78, 2861-2863.
11. 11. Pilkis, S.J., El-Maghrabi, M.R. & Claus, T.H. (1988) Hormonal regulation of hepatic gluconeogenesis and glycolysis. Annu. Rev. Biochem. 57, 755-783.
12. 12. Nimmo, H.G. & Tipton, K.F. (1975) The allosteric properties of beef liver fructose-1,6-bisphosphatase. Eur. J. Biochem. 58, 575-585.
13. 13. Scheffler. J.E. & Fromm, H.J. (1986) Regulation of rabbit liver fructose-1,6-bisphosphatase by metals, nucleotides, and fructose-2,6-bisphosphate as determined from fluorescence studies. Biochemistry 25, 6659-6665.
14. 14. Liu, F. & Fromm, H.J. (1990) Kinetic studies on the mechanism and regulation of rabbit liver fructose-1,6-bisphosphatase. J. Biol. Chem. 265, 7401-7406.
15. 15. Ke, H., Liang, J.-Y., Zhang, Y. & Lipscomb, W.N. (1991) Conformational transition of fructose-1,6-bisphosphatase: structure comparison between the AMP complex (T form) and the fructose 6-phosphate complex (R form). Biochemistry 30, 4412-4420.
16. 16. Ke, H., Zhang, Y & Lipscomb, W.N. (1990) Crystal structure of fructose-1,6-bisphosphatase complexed with fructose 6-phosphate, AMP, and magnesium. Proc. Natl Acad. Sci. USA 87, 5243-5247.
17. 17. Villeret, V., Huang, S., Zhang, Y. & Lipscomb, W.N. (1995) Structural aspects of allosteric inhibition of fructose-1,6-bisphosphatase by AMP: the binding of both the substrate analogue 2,5-anhydroglucitol-1,6-bisphosphate and catalytic metal ions monitored by X-ray crystallography. Biochemistry 34, 4307-4315.
18. 18. Lu, G., Stec, B., Giroux, E.L. & Kantrowitz, E.R. (1996) Evidence for an active T-state pig kidney fructose-1,6-bisphosphatase: interface residue Lys-42 is important for allosteric inhibition and AMP cooperativity. Protein Sci. 5, 2333-2342.
19. 19. Lu, G., Giroux, E.L. & Kantrowitz, E.R. (1997) Importance of the dimer-dimer interface for allosteric signal transduction and AMP cooperativity of pig kidney fructose-1,6-bisphosphatase. J. Biol. Chem. 272, 5076-5081.
20. 20. Shyur, L.-F., Aleshin, A.E., Honzatko, R.B. & Fromm, H.J. (1996) Sitedirected mutagenesis of residues at subunits interfaces of porcine fructose-1,6-bisphosphatase. J. Biol. Chem. 271, 3005-3010.
21. 21. Shyur, L.-F., Aleshin, A.E., Honzatko, R.B. & Fromm, H.J. (1996) Biochemical properties of mutant and wild-type fructose-1,6-bisphosphatase are consistent with the coupling of intra-and intersubunits conformational changes in the T-and R-state transition. J. Biol. Chem. 271, 33301-33307.
22. 22. Shyur, L.-F., Poland, B.W., Honzatko, R.B. & Fromm, H.J. (1997) Major changes in the kinetic mechanism of AMP inhibition and AMP cooperativity attend the mutation of Arg49 in fructose-1,6-bisphosphatase. J. Biol. Chem. 272, 26295-26299.
23. 23. Lu, G., Williams, M.K., Giroux, L.E. & Kantrowitz, E.R. (1995) Fructose-1,6-bisphosphatase: arginine-22 is involved in stabilization of the T allosteric state. Biochemistry 34, 13272-13277.
24. 2+ affinities. Biochemistry 35, 7492-7498.
25. 25. Gidh-Jain, M., Zhang, Y., van Poelje, P.D., Liang, J., Huang, S., Kim, J., Elliot, J.T., Erion, M.D., Pilkis, S.J., El-Maghrabi, M.R. & Lipscomb, W.N. (1994) The allosteric site of human liver fructose-1,6-bisphosphatase. Analysis of six AMP site mutants based on the crystal structure. J. Biol. Chem. 269, 27732-27738.
26. 26. Chen, M., Chen, L. & Fromm, H.J. (1994) Replacement of glutamic acid 29 with glutamine leads to a loss of cooperativity for AMP with porcine fructose-1,6-bisphosphatase. J. Biol. Chem. 269, 5554-5558.
27. 27. Kurbanov, F.T., Choe, J.-Y., Honzatko, R.B. & Fromm, H.J. (1998) Directed mutations in the poorly defined region of porcine liver fructose-1,6-bisphosphatase significantly affect catalysis and the mechanism of AMP inhibition. J. Biol. Chem. 213, 17511-17516.
28. 28. Slebe, J.C., Herrera, R., Hubert, E., Ojeda, A. & Maccioni, R.B. (1983) Fructose 1,6-bisphosphatase: dissociation of cooperativity and AMP inhibition by carbamylation. J. Protein Chem. 2, 437-443.
29. 29. Ludwig, H., Herrera, R., Reyes, A., Hubert, E. & Slebe, J.C. (1999) Suppression of kinetic AMP cooperativity of fructose-1,6-bisphosphatase by carbamoylation of Lys50. J. Protein Chem. 18, 533-545.
30. 30. Cárcamo, J.G., Reyes, A. & Slebe, J.C. (1990) Chemical modification of fructose-1,6-bisphosphatase with phenylglyoxal. Arch. Biol. Med. Exp. 23, R371.
31. 31. Cárcamo, J.G. & Slebe, J.C. (1998) Changes in the kinetic mechanism of AMP inhibition of fructose-1,6-bisphosphatase induced by site-directed mutagenesis. Noticiero de Biología 6, R65.
32. 32. Cárcamo, J.G., Yañez, A.J., Ludwig, H.C., León, O., Pinto, R.O., Reyes, A.M. & Slebe, J.C. (1999) The C1-C2 interface of fructose-1,6-bisphosphatase is critical for allosteric inhibition and AMP cooperativity. FASEB J. 13, A-1532 (1154).
33. 33. Burton, V.A., Chen, M.C., Ong, W.-C., Ling, T., Fromm, H.J. & Stayton, M.M. (1993) High-level expression of porcine fructose-1,6-bisphosphatase in Escherichia coli: purification and characterization of the enzyme. Biochem. Biophys. Res. Commun. 192, 511-517.
34. 34. Reyes, A.M., Burgos, M.E., Hubert, E. & Slebe, J.C. (1987) Selective thiol group modification renders fructose-1,6-bisphosphatase insensitive to fructose 2,6-bisphosphate inhibition. J. Biol. Chem. 262, 8451-8454.
35. 35. Segel, I.H. (1975) Enzyme Kinetics. Wiley-Interscience, New York.
36. 36. Leatherbarrow, R.J. (1987) ENZFITTER: a Non-Linear Regression Data Analysis Program for the IBM PC, pp. 13-75. Elsevier Science, Cambridge, UK.
37. 37. Siano, D.B., Zyskind, J.W. & Fromm, H.J. (1975) A computer program for fitting and statistically analyzing initial rate data applied to bovine hexokinase type III isozyme. Arch. Biochem. Biophys. 170, 587-600.
38. 38. Mannervik, B. (1982) Regression analysis, experimental error, and statistical criteria in design and analysis of experiments for discrimination between rival kinetic models. Methods Enzymol. 87, 370-390.
39. 39. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
40. 40. Ulm, E.H., Pogell, B.M., de Maine, M.M., Libby, C.B. & Benkovic, S.J. (1975) Fructose-1,6-diphosphatase from rabbit liver. Methods Enzymol. 42, 369-374.
41. 41. Nimmo, H.G. & Tipton, K.F. (1975) The purification of fructose 1,6-bisphosphatase from ox liver and its activation by ethylene-diaminetetra-acetate. Biochem. J. 145, 323-334.
42. 42. Nimmo, H.G. & Tipton, K.F. (1975) The effect of pH on the kinetics of beef liver fructose-1,6-bisphosphatase. Eur. J. Biochem. 58, 567-574.
43. 43. Choe, J.-Y., Poland, B.W., Fromm, H.J. & Honzatko, R.B. (1998) Role of dynamic loop in cation activation and allosteric regulation of recombinant porcine fructose-1,6-bisphosphatase. Biochemistry 37, 11441-11450.
44. 44. Slebe, J.C., Ojeda, A., Hubert, E. & Maccioni, R. (1981). Molecular Approaches to Gene Expression and Protein Structure (Siddiqui, M.A.Q., Krauskopf, M. & Weissbach, H., eds), pp. 329-363. Academic Press, New York.
45. 45. Mellado, R.G., Cárcamo, J.G. & Slebe, J.C. (1992) Loss of cooperativity toward AMP in a fructose 1,6-bisphosphatase-phenylglyoxal derivate sensitive at the nucleotide. Arch. Biol. Med. Exp. 24, R-108.
46. 46. Fersht, A. (1999) Structure and Mechanism in Proteins Science. W. H. Freeman, New York.
47. 47. Schmidt, D.E. Jr & Westheimer, F.H. (1971) pK of the lysine amino group at the active site of acetoacetate descarboxylase. Biochemistry 10, 1249-1253.
48. 48. Slebe, J.C. & Martinez-Carrión, M. (1976) Carbamylation of aspartate transaminase and the pK value of the active site lysyl residue. J. Biol. Chem. 251, 5663-5669.
49. 19F-NMR in the assignment of a pK value to the active site lysyl residue in aspartate transaminase. J. Biol. Chem. 253, 2093-2097.
50. 50. Jones, T.A. (1982). Computational Crystallography (Sayer, D., ed.), pp. 303-317. Oxford University Press, London.
51. 51. Giudici-Orticoni, M.T., Buc, J., Bidaud, M. & Ricard, J. (1990) Thermodynamics of information transfer between subunits in oligomeric enzymes and kinetic cooperativity. Eur. J. Biochem. 194, 483-490.
52. 52. Marcus, F. & Haley, B.E. (1979) Inhibition of fructose-1,6-bisphosphatase by the photoaffinity AMP analog, 8-azidoadenosine 5'-monophosphate. J. Biol. Chem. 254, 259-261.