Structural and mechanistic insights into the bifunctional enzyme isocitrate dehydrogenase kinase/phosphatase AceK

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1602, 2012, Pages 2656-2668

  Zheng, Jimin ^a   Yates, Susan P ^b   Jia, Zongchao ^a,b  

^a BEIJING NORMAL UNIVERSITY   (China)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

AceK; Isocitrate dehydrogenase; Kinase; Phosphatase; Phosphorylation

Indexed keywords

BIOCHEMISTRY; BIOMECHANICS; CATALYSIS; ENZYME ACTIVITY; EUKARYOTE; EVOLUTIONARY BIOLOGY; MOLECULAR ANALYSIS; PHOSPHATE;

EID: 84865089252     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0426     Document Type: Review

References (50)

1. Cozzone, A. J. 1998 Regulation of acetate metabolism by protein phosphorylation in enteric bacteria. Annu. Rev. Microbiol. 52, 127-164. (doi:10.1146/annurev.micro.52. 1.127)
2. LaPorte, D. C. & Koshland Jr, D. E. 1982 A protein with kinase and phosphatase activities involved in regulation of tricarboxylic acid cycle. Nature 300, 458-460. (doi:10.1038/300458a0)
3. Zheng, J. & Jia, Z. 2010 Structure of the bifunctional isocitrate dehydrogenase kinase/phosphatase. Nature 465, 961-965. (doi:10.1038/nature09088)
4. Wang, Z., Liu, J., Sudom, A., Ayres, M., Li, S., Wesche, H., Powers, J. P. & Walker, N. P. 2006 Crystal structures of IRAK-4 kinase in complex with inhibitors: a serine/ threonine kinase with tyrosine as a gatekeeper. Structure. 14, 1835-1844. (doi:10.1016/j.str.2006.11.001)
5. Chen, H. et al. 2008 A crystallographic snapshot of tyrosine trans-phosphorylation in action. Proc. Natl Acad. Sci. USA 105, 19660-19665. (doi:10.1073/pnas.0807752105)
6. Knowles, P. P., Murray-Rust, J., Kjaer, S., Scott, R. P., Hanrahan, S., Santoro, M., Ibanez, C. F. & McDonald, N. Q. 2006 Structure and chemical inhibition of the RET tyrosine kinase domain. J. Biol. Chem. 281, 33 577-33 587. (doi:10.1074/jbc.M605604200)
7. Scheeff, E. D. & Bourne, P. E. 2005 Structural evolution of the protein kinase-like superfamily. PLoS Comput. Biol. 1, e49. (doi:10.1371/journal.pcbi.0010049)
8. Taylor, S. S., Knighton, D. R., Zheng, J., Ten Eyck, L. F. & Sowadski, J. M. 1992 Structural framework for the protein kinase family. Annu. Rev. Cell Biol. 8, 429-462. (doi:10. 1146/annurev.cb.08.110192.002241)
9. Bossemeyer, D. 1994 The glycine-rich sequence of protein kinases: a multifunctional element. Trends Biochem. Sci. 19, 201-205. (doi:10.1016/0968-0004(94)90022-1)
10. Taylor, S. S., Knighton, D. R., Zheng, J., Sowadski, J. M., Gibbs, C. S. & Zoller, M. J. 1993 A template for the protein kinase family. Trends Biochem. Sci. 18, 84-89. (doi:10.1016/0968-0004(93)80001-R)
11. Oudot, C., Cortay, J. C., Blanchet, C., LaPorte, D. C., Di, P. A., Cozzone, A. J. & Jault, J. M. 2001 The 'catalytic' triad of isocitrate dehydrogenase kinase/phosphatase from E. coli and its relationship with that found in eukaryotic protein kinases. Biochemistry 40, 3047-3055. (doi:10. 1021/bi001713x)
12. Brenner, S. 1987 Phosphotransferase sequence homology. Nature 329, 21. (doi:10.1038/329021a0)
13. Eswaran, J., Patnaik, D., Filippakopoulos, P., Wang, F., Stein, R. L., Murray, J. W., Higgins, J. M. & Knapp, S. 2009 Structure and functional characterization of the atypical human kinase haspin. Proc. Natl Acad. Sci. USA 106, 20 198-20 203. (doi:10.1073/pnas.0901989106)
14. Eswaran, J. & Knapp, S. 2010 Insights into protein kinase regulation and inhibition by large scale structural comparison. Biochim. Biophys. Acta 1804, 429-432. (doi:10.1016/j.bbapap.2009.10.013)
15. Kornev, A. P. & Taylor, S. S. 2010 Defining the conserved internal architecture of a protein kinase. Biochim. Biophys. Acta 1804, 440-444. (doi:10.1016/j. bbapap.2009.10.017)
16. Kornev, A. P., Haste, N. M., Taylor, S. S. & Eyck, L. F. 2006 Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism. Proc. Natl Acad. Sci. USA 103, 17 783-17 788. (doi:10.1073/pnas.0607656103)
17. Kornev, A. P., Taylor, S. S. & Ten Eyck, L. F. 2008 A helix scaffold for the assembly of active protein kinases. Proc. Natl Acad. Sci. USA 105, 14 377-14 382. (doi:10.1073/pnas.0807988105)
18. Burk, D. L., Hon, W. C., Leung, A. K. & Berghuis, A. M. 2001 Structural analyses of nucleotide binding to an aminoglycoside phosphotransferase. Biochemistry 40, 8756-8764. (doi:10.1021/bi010504p)
19. Azam, M., Seeliger, M. A., Gray, N. S., Kuriyan, J. & Daley, G. Q. 2008 Activation of tyrosine kinases by mutation of the gatekeeper threonine. Nat. Struct. Mol. Biol. 15, 1109-1118. (doi:10.1038/nsmb.1486)
20. Huse, M. & Kuriyan, J. 2002 The conformational plasticity of protein kinases. Cell 109, 275-282. (doi:10. 1016/S0092-8674(02)00741-9)
21. Nolen, B., Taylor, S. & Ghosh, G. 2004 Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 15, 661-675. (doi:10. 1016/j.molcel.2004.08.024)
22. Rabiller, M., Getlik, M., Kluter, S., Richters, A., Tuckmantel, S., Simard, J. R. & Rauh, D. 2010 Proteus in the world of proteins: conformational changes in protein kinases. Arch. Pharm. (Weinheim) 343, 193-206. (doi:10.1002/ardp.201000028)
23. Deshmukh, K., Anamika, K. & Srinivasan, N. 2010 Evolution of domain combinations in protein kinases and its implications for functional diversity. Prog. Biophys. Mol. Biol. 102, 1-15. (doi:10.1016/j.pbiomol bio.2009.12.009)
24. Kim, C., Xuong, N. H. & Taylor, S. S. 2005 Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA. Science 307, 690-696. (doi:10.1126/science.1104607)
25. Osborne, B. W. et al. 2011 Crystal structure of cGMPdependent protein kinase reveals novel site of interchain communication. Structure 19, 1317-1327. (doi:10. 1016/j.str.2011.06.012)
26. Carling, D. 2005 AMP-activated protein kinase: balancing the scales. Biochimie 87, 87-91. (doi:10.1016/j. biochi.2004.10.017)
27. Lahiri, S. D., Zhang, G., Dunaway-Mariano, D. & Allen, K. N. 2003 The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science 299, 2067-2071. (doi:10.1126/science.1082710)
28. Hausmann, S., Erdjument-Bromage, H. & Shuman, S. 2004 Schizosaccharomyces pombe carboxyl-terminal domain (CTD) phosphatase Fcp1: distributive mechanism, minimal CTD substrate, and active site mapping. J. Biol. Chem. 279, 10 892-10 900. (doi:10.1074/jbc. M312513200)
29. Collet, J. F., Stroobant, V., Pirard, M., Delpierre, G. & Van, S. E. 1998 A new class of phosphotransferases phosphorylated on an aspartate residue in an aminoterminal DXDX(T/V) motif. J. Biol. Chem. 273, 14 107-14 112.
30. Collet, J. F., Stroobant, V. & Van, S. E. 2002 Evidence for phosphotransferases phosphorylated on aspartate residue in N-terminal DXDX(T/V) motif. Methods Enzymol. 354, 177-188. (doi:10.1016/S0076-6879(02)54014-3)
31. Nguyen, H. H., Wang, L., Huang, H., Peisach, E., Dunaway-Mariano, D. & Allen, K. N. 2010 Structural determinants of substrate recognition in the HAD superfamily member D-glycero-D-manno-heptose-1,7-bisphosphate phosphatase (GmhB). Biochemistry 49, 1082-1092. (doi:10.1021/bi902019q)
32. Ikeda, T. P., Houtz, E. & LaPorte, D. C. 1992 Isocitrate dehydrogenase kinase/phosphatase: identification of mutations which selectively inhibit phosphatase activity. J. Bacteriol. 174, 1414-1416.
33. Miller, S. P., Karschnia, E. J., Ikeda, T. P. & LaPorte, D. C. 1996 Isocitrate dehydrogenase kinase/phosphatase. Kinetic characteristics of the wild-type and two mutant proteins. J. Biol. Chem. 271, 19 124-19 128. (doi:10. 1074/jbc.271.32.19124)
34. LaPorte, D. C., Walsh, K. & Koshland Jr, D. E. 1984 The branch point effect. Ultrasensitivity and subsensitivity to metabolic control. J. Biol. Chem. 259, 14 068-14 075.
35. Cozzone, A. J. & El-Mansi, M. 2005 Control of isocitrate dehydrogenase catalytic activity by protein phosphorylation in Escherichia coli. J. Mol. Microbiol. Biotechnol. 9, 132-146. (doi:10.1159/000089642)
36. Lorca, G. L., Ezersky, A., Lunin, V. V., Walker, J. R., Altamentova, S., Evdokimova, E., Vedadi, M., Bochkarev, A. & Savchenko, A. 2007 Glyoxylate and pyruvate are antagonistic effectors of the Escherichia coli IclR transcriptional regulator. J. Biol. Chem. 282, 16 476-16 491. (doi:10.1074/jbc.M610838200)
37. el-Mansi, E. M., Nimmo, H. G. & Holms, W. H. 1986 Pyruvate metabolism and the phosphorylation state of isocitrate dehydrogenase in Escherichia coli. J. Gen. Microbiol. 132, 797-806.
38. Cortay, J. C., Negre, D., Galinier, A., Duclos, B., Perriere, G. & Cozzone, A. J. 1991 Regulation of the acetate operon in Escherichia coli: purification and functional characterization of the IclR repressor. EMBO J. 10, 675-679.
39. Miller, S. P., Chen, R., Karschnia, E. J., Romfo, C., Dean, A. & LaPorte, D. C. 2000 Locations of the regulatory sites for isocitrate dehydrogenase kinase/ phosphatase. J. Biol. Chem. 275, 833-839. (doi:10. 1074/jbc.275.2.833)
40. Amodeo, G. A., Rudolph, M. J. & Tong, L. 2007 Crystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1. Nature 449, 492-495. (doi:10.1038/nature06127)
41. Xiao, B. et al. 2007 Structural basis for AMP binding to mammalian AMP-activated protein kinase. Nature 449, 496-500. (doi:10.1038/nature06161)
42. Iancu, C.V., Mukund, S., Fromm, H. J. &Honzatko, R.B. 2005 R-state AMP complex reveals initial steps of the quaternary transition of fructose-1,6-bisphosphatase. J. Biol. Chem. 280, 19 737-19 745. (doi:10.1074/jbc. M501011200)
43. Choe, J. Y., Fromm, H. J. & Honzatko, R. B. 2000 Crystal structures of fructose 1,6-bisphosphatase: mechanism of catalysis and allosteric inhibition revealed in product complexes. Biochemistry 39, 8565-8574. (doi:10.1021/bi000574g)
44. Johnson, L. N., Snape, P., Martin, J. L., Acharya, K. R., Barford, D. & Oikonomakos, N. G. 1993 Crystallographic binding studies on the allosteric inhibitor glucose-6-phosphate to T state glycogen phosphorylase b. J. Mol. Biol. 232, 253-267. (doi:10.1006/jmbi.1993.1380)
45. Rath, V. L. et al. 2000 Activation of human liver glycogen phosphorylase by alteration of the secondary structure and packing of the catalytic core. Mol. Cell 6, 139-148. (doi:10.1016/S1097-2765(05)00006-7)
46. Barford, D., Hu, S. H. & Johnson, L. N. 1991 Structural mechanism for glycogen phosphorylase control by phosphorylation and AMP. J. Mol. Biol. 218, 233-260. (doi:10.1016/0022-2836(91)90887-C)
47. Wang, Q. et al. 2010 Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327, 1004-1007. (doi:10.1126/science.1179687)
48. McKee, J. S., Hlodan, R. & Nimmo, H. G. 1989 Studies of the phosphorylation of Escherichia coli isocitrate dehydrogenase. Recognition of the enzyme by isocitrate dehydrogenase kinase/phosphatase and effects of phosphorylation on its structure and properties. Biochimie 71, 1059-1064. (doi:10.1016/0300-9084(89)90111-9)
49. Manning, G., Plowman, G. D., Hunter, T. & Sudarsanam, S. 2002 Evolution of protein kinase signaling from yeast to man. Trends Biochem. Sci. 27, 514-520. (doi:10.1016/S0968-0004(02)02179-5)
50. Yates, S. P., Edwards, T. E., Bryan, C. M., Stein, A. J., Van Voorhis, W. C., Myler, P. J., Stewart, L. J., Zheng, J. & Jia, Z. 2011 Structural basis of the substrate specificity of bifunctional isocitrate dehydrogenase kinase/ phosphatase. Biochemistry 50, 8103-8106. (doi:10. 1021/bi200809p)