Structural basis for tumor pyruvate kinase M2 allosteric regulation and catalysis

Biochemistry

Volumn 44, Issue 27, 2005, Pages 9417-9429

  Dombrauckas, Jill D ^a   Santarsiero, Bernard D ^a   Mesecar, Andrew D ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMARKERS; CELLS; DIAGNOSIS; DISEASES; DRUG PRODUCTS; ENZYME INHIBITION; MAGNESIUM COMPOUNDS; POTASSIUM COMPOUNDS; TUMORS; X RAY ANALYSIS;

CANCER CELLS; HUMAN PLASMAS; ISOENZYMES; PYRUVATE KINASE;

ENZYMES;

ADENOSINE TRIPHOSPHATE; ISOENZYME; LIGAND; MAGNESIUM ION; PYRUVATE KINASE;

ALLOSTERISM; ARTICLE; CATALYSIS; CELL PROLIFERATION; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME STRUCTURE; ESCHERICHIA COLI; HEMOLYTIC ANEMIA; HUMAN; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; TUMOR CELL; X RAY DIFFRACTION;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; ANIMALS; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; ENZYME REACTIVATORS; ENZYME STABILITY; FRUCTOSEDIPHOSPHATES; HUMANS; KINETICS; LIGANDS; MODELS, MOLECULAR; NEOPLASM PROTEINS; OXALIC ACID; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PYRUVATE KINASE; RABBITS; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

ORYCTOLAGUS CUNICULUS;

EID: 21844468220     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0474923     Document Type: Article

References (73)

1. Larsen, T. M., Benning, M. M., Rayment, I., and Reed, G. H. (1998) Structure of the bis(Mg2+)-ATP-oxalate complex of the rabbit muscle pyruvate kinase at 2.1 Å resolution: ATP binding over a barrel, Biochemistry 37, 6247-55.
2. Mazurek, S., Boschek, C. B., and Eigenbrodt, E. (1997) The role of phosphometabolites in cell proliferation, energy metabolism, and tumor therapy, J. Bioenerg. Biomembr. 29, 315-30.
3. Mazurek, S., Grimm, H., Boschek, C. B., Vaupel, P., and Eigenbrodt, E. (2002) Pyruvate kinase type M2: a crossroad in the tumor metabolome, Br. J. Nutr. 87 (Suppl. 1), S23-9.
4. Eigenbrodt, E., Reinacher, M., Scheefers-Borchel, U., Scheefers, H., and Friis, R. (1992) Double role for pyruvate kinase type M2 in the expansion of phosphometabolite pools found in tumor cells, Crit. Rev. Oncog. 3, 91-115.
5. Noguchi, T., Yamada, K., Inoue, H., Matsuda, T., and Tanaka, T. (1987) The L- and R-type isozymes of rat pyruvate kinase are produced from a single gene by use of different promoters, J. Biol. Chem. 262, 14366-71.
6. Cotton, F., Bianchi, P., Zanella, A., Van Den Bogaert, N., Ferster, A., Hansen, V., Van Herreweghe, I., Vertongen, F., and Gulbis, B. (2001) A novel mutation causing pyruvate kinase deficiency responsible for a severe neonatal respiratory distress syndrome and jaundice, Eur. J. Pediatr. 160, 523-4.
7. Larochelle, A., Magny, P., Tremblay, S., and Medicis, E. E. (1999) Erythropoiesis: pyruvate kinase deficiency which causes nonspherocytic hemolytic anemia: the gene and its mutations, Hematology 4, 77-87.
8. Noguchi, T., Inoue, H., and Tanaka, T. (1986) The M1- and M2-type isozymes of rat pyruvate kinase are produced from the same gene by alternative RNA splicing, J. Biol. Chem. 261, 13807-12.
9. Yamada, K., and Noguchi, T. (1995) Alteration of isozyme gene expression during cell differentiation and oncogenesis, Nippon Rinsho 53, 1112-8.
10. Kato, H., Fukuda, T., Parkison, C., McPhie, P., and Cheng, S. Y. (1989) Cytosolic thyroid hormone-binding protein is a monomer of pyruvate kinase, Proc. Natl. Acad. Sci. U.S.A. 86, 7861-5.
11. Obata, T., Fukuda, T., Willingham, M. C., Liang, C. M., and Cheng, S. Y. (1989) A cytoplasmic thyroid hormone binding protein: characterization using monoclonal antibodies, Biochemistry 28, 617-23.
12. Staal, G. E., and Rijksen, G. (1985) Regulation of Carbohydrate Metabolism 1, CRC Press, Boca Raton, FL.
13. Bena-Boupda, N. F., Rezai, S. S., Klett, R., Eigenbrodt, E., and Bauer, R. (2003) Value of tumor M2-PK in thyroid carcinoma: a pilot study, Anticancer Res. 23, 5237-40.
14. Hardt, P. D., Toepler, M., Ngoumou, B., Rupp, J., and Kloer, H. U. (2003) Measurement of fecal pyruvate kinase type M2 (tumor M2-PK) concentrations in patients with gastric cancer, colorectal cancer, colorectal adenomas and controls, Anticancer Res. 23, 851-3.
15. Schneider, J., Neu, K., Velcovsky, H. G., Morr, H., and Eigenbrodt, E. (2003) Tumor M2-pyruvate kinase in the follow-up of inoperable lung cancer patients: a pilot study, Cancer Lett. 193, 91-8.
16. Kim, C. W., Kim, J. I., Park, S. H., Han, J. Y., Kim, J. K., Chung, K. W., and Sun, H. S. (2003) Usefulness of plasma tumor M2-pyruvate kinase in the diagnosis of gastrointestinal cancer, Korean J. Gastroenterol. 42, 387-93.
17. Hoopmann, M., Warm, M., Mallmann, P., Thomas, A., Gohring, U. J., and Schondorf, T. (2002) Tumor M2 pyruvate kinase-determination in breast cancer patients receiving trastuzumab therapy, Cancer Lett. 187, 223-8.
18. Luftner, D., Mesterharm, J., Akrivakis, C., Geppert, R., Petrides, P. E., Wernecke, K. D., and Possinger, K. (2000) Tumor type M2 pyruvate kinase expression in advanced breast cancer, Anticancer Res. 20, 5077-82.
19. Schneider, J., Peltri, G., Bitterlich, N., Neu, K., Velcovsky, H. G., Morr, H., Katz, N., and Eigenbrodt, E. (2003) Fuzzy logic-based tumor marker profiles including a new marker tumor M2-PK improved sensitivity to the detection of progression in lung cancer patients. Anticancer Res. 23, 899-906.
20. Oremek, G. M., Muller, R., Sapoutzis, N., and Wigand, R. (2003) Pyruvate kinase type tumor M2 plasma levels in patients afflicted with rheumatic diseases, Anticancer Res. 23, 1131-4.
21. Schulze, G. (2000) The tumor marker tumor M2-PK: an application in the diagnosis of gastrointestinal cancer, Anticancer Res. 20, 4961-4.
22. Yilmaz, S., Ozan, S., and Ozercan, I. H. (2003) Comparison of pyruvate kinase variants from breast tumor and normal breast, Arch. Med. Res. 34, 315-24.
23. Roigas, J., Deger, S., Schroeder, J., Wille, A., Turk, I., Brux, B., Jung, K., Schnorr, D., and Loening, S. A. (2003) Tumor type M2 pyruvate kinase expression in metastatic renal cell carcinoma, Urol. Res. 31, 358-62.
24. Pezzilli, R., Migliori, M., Morselli-Labate, A. M., Campana, D., Ventrucci, M., Tomassetti, P., and Corinaldesi, R. (2003) Diagnostic value of tumor M2-pyruvate kinase in neuroendocrine tumors. A comparative study with chromogranin A, Anticancer Res. 23, 2969-72.
25. Oremek, G. M., Rutner, F., Sapoutzis, N., and Sauer-Eppel, H. (2003) Tumor marker pyruvate kinase type tumor M2 in patients suffering from diabetic nephropathy, Anticancer Res. 23, 1155-8.
26. Varga, Z., Hegele, A., Stief, T., Heidenreich, A., and Hofmann, R. (2002) Determination of pyruvate kinase type tumor M2 in human renal cell carcinoma: a suitable tumor marker?, Urol. Res. 30, 122-5.
27. Hegele, A., Varga, Z., Kosche, B., Stief, T., Heidenreich, A., and Hofmann, R. (2003) Pyruvate kinase type tumor M2 in urological malignancies, Urol. Int. 70, 55-8.
28. Oremek, G. M., Rox, S., Mitrou, P., Sapoutzis, N., and Sauer-Eppel, H. (2003) Tumor M2-PK levels in haematological malignancies, Anticancer Res. 23, 1135-8.
29. DeDecker, B. S. (2000) Allosteric drugs: thinking outside the active-site box, Chem. Biol. 7, R103-7.
30. Ashizawa, K., Willingham, M. C., Liang, C. M., and Cheng, S. Y. (1991) In vivo regulation of monomer-tetramer conversion of pyruvate kinase subtype M2 by glucose is mediated via fructose 1,6-bisphosphate, J. Biol. Chem. 266, 16842-6.
31. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein, Protein Sci. 4, 2411-23.
32. Imamura, K., and Tanaka, T. (1982) Pyruvate kinase isozymes from rat, Methods Enzymol. 90, 150-65.
33. Kissinger, C. R., Gehlhaar, D. K., and Fogel, D. B. (1999) Rapid automated molecular replacement by evolutionary search, Acta Crystallogr., Sect. D 55, 484-91.
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 & NMR system: a new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D 54, 905-21.
35. 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., Sect. A 47, 110-9.
36. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Calpha geometry: phi, psi and Cbeta deviation, Proteins 50, 437-50.
37. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-86.
38. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program, J. Mol. Graphics 8, 52-6, 29.
39. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The protein data bank, Nucleic Acids Res. 28, 235-42.
40. Accelrys Software, Inc. (2001-2004) http://www.accelrys.com.
41. Babsky, A., Hekmatyar, S. K., Wehrli, S., Nelson, D., and Bansal, N. (2004) Effects of temperature on intracellular sodium, pH and cellular energy status in RIF-1 tumor cells, NMR Biomed. 17, 33-42.
42. Ford, S. R., and Robinson, J. L. (1976) The proton-transfer reactions catalyzed by yeast pyruvate kinase, Biochim. Biophys. Acta 438, 119-30.
43. Kuczenski, R. T., and Suelter, C. H. (1971) Fructose 1,6-diphosphate enhances inactivation of yeast pyruvate kinase at 23°. Evidence for a stabilized dimer intermediate, Biochemistry 10, 2867-72.
44. Buc, H., Demaugre, F., and Leroux, J. P. (1978) The kinetic effects of oxalate on liver and erythrocyte pyruvate kinases, Biochem. Biophys. Res. Commun. 85, 774-9.
45. Jurica, M. S., Mesecar, A., Heath, P. J., Shi, W., Nowak, T., and Stoddard, B. L. (1998) The allosteric regulation of pyruvate kinase by fructose-1,6-bisphosphate, Structure 6, 195-210.
46. Ruwart, M. J., and Suelter, C. H. (1971) Activation of yeast pyruvate kinase by natural and artificial cryoprotectants, J. Biol. Chem. 246, 5990-3.
47. Robinson, J. L., and Rose, I. A. (1972) The proton-transfer reactions of muscle pyruvate kinase, J. Biol. Chem. 247, 1096-105.
48. Bollenbach, T. J., Mesecar, A. D., and Nowak, T. (1999) Role of lysine 240 in the mechanism of yeast pyruvate kinase catalysis, Biochemistry 38, 9137-45.
49. Lodato, D. T., and Reed, G. H. (1987) Structure of the oxalate-ATP complex with pyruvate kinase: ATP as a bridging ligand for the two divalent cations, Biochemistry 26, 2243-50.
50. Baranowska, B., and Baranowski, T. (1975) Pyruvate kinase from human skeletal muscle, Mol. Cell. Biochem. 6, 197-201.
51. Kuczek, M. (2002) Influence of inorganic pyrophosphate on the kinetics of muscle pyruvate kinase: a simple nonallosteric feedback model, Biosystems 66, 11-20.
52. Nowak, T. (1978) Structure of the fluorophosphate-pyruvate kinase complex investigated by 31P relaxation rate studies, Arch. Biochem. Biophys. 186, 343-50.
53. Nowak, T. (1978) Structural changes at the active site of pyruvate kinase during activation and catalysis, J. Biol. Chem. 253, 1998-2004.
54. Tietz, A., and Ochoa, S. (1958) Fluorokinase and pyruvic kinase, Arch. Biochem. Biophys. 78, 477-93.
55. +, and pyruvate, Biochemistry 33, 6301-9.
56. Valentini, G., Chiarelli, L. R., Fortin, R., Dolzan, M., Galizzi, A., Abraham, D. J., Wang, C., Bianchi, P., Zanella, A., and Mattevi, A. (2002) Structure and function of human erythrocyte pyruvate kinase. Molecular basis of nonspherocytic hemolytic anemia, J. Biol. Chem. 277, 23807-14.
57. Gerstein, M., and Krebs, W. (1995) Database of macromolecular movements, http//molmovdb.org.
58. Lee, R. A., Razaz, M., and Hayward, S. (2003) The DynDom database of protein domain motions, Bioinformatics 19, 1290-1.
59. 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, 144-54.
60. Susan-Resiga, D., and Nowak, T. (2003) The proton-transfer step catalyzed by yeast pyruvate kinase, J. Biol. Chem. 278, 12660-71.
61. Rose, I. A. (1970) Stereochemistry of pyruvate kinase, pyruvate carboxylase, and malate enzyme reactions, J. Biol. Chem. 245, 6052-6.
62. Rose, I. A., and Kuo, D. J. (1989) The substrate proton of the pyruvate kinase reaction, Biochemistry 28, 9579-85.
63. Rose, I. A., Kuo, D. J., and Warms, J. V. (1991) A rate-determining proton relay in the pyruvate kinase reaction, Biochemistry 30, 722-6.
64. Susan-Resiga, D., and Nowak, T. (2004) Proton donor in yeast pyruvate kinase: chemical and kinetic properties of the active site Thr 298 to Cys mutant, Biochemistry 43, 15230-45.
65. Bond, C. J., Jurica, M. S., Mesecar, A., and Stoddard, B. L. (2000) Determinants of allosteric activation of yeast pyruvate kinase and identification of novel effectors using computational screening, Biochemistry 39, 15333-43.
66. Ikeda, Y., Taniguchi, N., and Noguchi, T. (2000) Dominant negative role of the glutamic acid residue conserved in the pyruvate kinase M(1) isozyme in the heterotropic allosteric effect involving fructose-1,6-bisphosphate, J. Biol. Chem. 275, 9150-6.
67. Bollenbach, T. J., and Nowak, T. (2001) Kinetic linked-function analysis of the multiligand interactions on Mg(2+)-activated yeast pyruvate kinase, Biochemistry 40, 13097-106.
68. Mesecar, A. D., and Nowak, T. (1997) Metal-ion-mediated allosteric triggering of yeast pyruvate kinase. 1. A multidimensional kinetic linked-function analysis, Biochemistry 36, 6792-802.
69. Mesecar, A. D., and Nowak, T. (1997) Metal-ion-mediated allosteric triggering of yeast pyruvate kinase. 2. A multidimensional thermodynamic linked-function analysis, Biochemistry 36, 6803-13.
70. Nowak, T., and Suelter, C. (1981) Pyruvate kinase: activation by and catalytic role of the monovalent and divalent cations, Mol. Cell. Biochem. 35, 65-75.
71. Mattos, C., and Ringe, D. (1996) Locating and characterizing binding sites on proteins, Nat. Biotechnol. 14, 595-9.
72. Safo, M. K., Moure, C. M., Burnett, J. C., Joshi, G. S., and Abraham, D. J. (2001) High-resolution crystal structure of deoxy hemoglobin complexed with a potent allosteric effector, Protein Sci. 10, 951-7.
73. Ashizawa, K., McPhie, P., Lin, K. H., and Cheng, S. Y. (1991) An in vitro novel mechanism of regulating the activity of pyruvate kinase M2 by thyroid hormone and fructose 1, 6-bisphosphate, Biochemistry 30, 7105-11.