Structure and function of the catalytic domain of the dihydrolipoyl acetyltransferase component in Escherichia coli pyruvate dehydrogenase complex

Journal of Biological Chemistry

Volumn 289, Issue 22, 2014, Pages 15215-15230

  Wang, Junjie ^a   Nemeria, Natalia S ^a   Chandrasekhar, Krishnamoorthy ^b   Kumaran, Sowmini ^a   Arjunan, Palaniappa ^b   Reynolds, Shelley ^b   Calero, Guillermo ^b   Brukh, Roman ^a   Kakalis, Lazaros ^a   Furey, William ^b,c   Jordan, Frank ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MASS SPECTROMETRY;

ACETYL TRANSFERASE; ACETYL-COA; CATALYTIC DOMAINS; E. COLI; MULTI DOMAINS; MULTI-FACETED APPROACH; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVATES;

ESCHERICHIA COLI;

ACETYL COENZYME A; DIHYDROLIPOAMIDE ACETYLTRANSFERASE; PYRUVATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME RECONSTITUTION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE;

CARBOHYDRATE METABOLISM; ENZYME CATALYSIS; HD EXCHANGE; MASS SPECTROMETRY (MS); NUCLEAR MAGNETIC RESONANCE (NMR); PYRUVATE DEHYDROGENASE COMPLEX (PDC); X-RAY CRYSTALLOGRAPHY;

ACETYL COENZYME A; ACETYLATION; AMINO ACID SEQUENCE; CARBOHYDRATE METABOLISM; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DEUTERIUM EXCHANGE MEASUREMENT; DIHYDROLIPOYLLYSINE-RESIDUE ACETYLTRANSFERASE; ENZYME ACTIVATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; PLASMIDS; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVIC ACID;

EID: 84901698087     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.544080     Document Type: Article

References (62)

1. Balakrishnan, A., Nemeria, N. S., Chakraborty, S., Kakalis, L., and Jordan, F. (2012) Determination of pre-steady-state constants on the Escherichia coli pyruvate dehydrogenase complex reveals that loop movement controls the rate-limiting step. J. Am. Chem. Soc. 134, 18644-18655
2. Jordan, F., Arjunan, P., Kale, S., Nemeria, N. S., and Furey, W. (2009) Multiple roles of mobile active center loops in the E1 component of the Escherichia coli pyruvate dehydrogenase complex. Linkage of protein dynamics to catalysis. J. Mol. Catal. B Enzym. 61, 14-22
3. Reed, L. J., and Hackert, M. L. (1990) Structure-function relationships in dihydrolipoamide acyltransferases. J. Biol. Chem. 265, 8971-8974
4. Perham, R. (1991) Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes: a paradigm in the design of a multifunctional protein. Biochemistry 30, 8501-8512
5. Perham, R. (2000) Swinging arms and swinging domains in multifunctional enzymes: catalytic machines for multistep reactions. Annu. Rev. Biochem. 69, 961-1004
6. Perham, R. N., Jones, D. D., Chauhan, H. J., and Howard, M. J. (2002) Substrate channeling in 2-oxo acid dehydrogenase multienzyme complexes. Biochem. Soc. Trans. 30, 47-51
7. Stephens, P. E., Darlison, M. G., Lewis, H. M., and Guest, J. R. (1983) The pyruvate dehydrogenase complex of Escherichia coli K12. Nucleotide sequence encoding the pyruvate dehydrogenase component. Eur. J. Biochem. 133, 155-162
8. Stephens, P. E., Darlison, M. G., Lewis, H. M., and Guest, J. R. (1983) The pyruvate dehydrogenase complex of Escherichia coli K12. Nucleotide sequence encoding the dihydrolipoamide acetyltransferase component. Eur. J. Biochem. 133, 481-489
9. Bleile, D. M., Munk, P., Oliver, R. M., and Reed, L. J. (1979) Subunit structure of dihydrolipoyl transacetylase component of pyruvate dehydrogenase complex from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 76, 4385-4389
10. Reed, L. J., Pettit, F. H., Eley, M. H., Hamilton, L., Collins, J. H., and Oliver, R. M. (1975) Reconstitution of the Escherichia coli pyruvate dehydrogenase complex. Proc. Natl. Acad. Sci. U.S.A. 72, 3068-3072
11. Green J. D., Perham, R. N., Ullrich, S. J., and Appella, E. (1992) Conformational studies of the interdomain linker peptides in the dihydrolipoyl acetyltransferase component of the pyruvate dehydrogenase multienzyme complex of Escherichia coli. J. Biol. Chem. 267, 23484-23488
12. Stephens, P. E., Lewis, H. M., Darlison, M. G., and Guest, J. R. (1983) Nucleotide sequence of the lipoamide dehydrogenase gene of Escherichia coli K12. Eur. J. Biochem. 135, 519-527
13. Stoops, J. K., Cheng, R. H., Yazdi, M. A., Maeng, C.-Y., Schroeter, J. P., Klueppelberg, U., Kolodziej, S. J., Baker, T. S., and Reed, L. J. (1997) On the unique structural organization of the Saccharomyces cerevisiae pyruvate dehydrogenase complex. J. Biol. Chem. 272, 5757-5764
14. Zhou, Z. H., Liao, W., Cheng, R. H., Lawson, J. E., McCarthy, D. B., Reed, L. J., and Stoops, J. K. (2001) Direct evidence for the size and conformational variability of the pyruvate dehydrogenase complex revealed by three-dimensional electron microscopy. J. Biol. Chem. 276, 21704-21713
15. Yu, X., Hiromasa, Y., Tsen, H., Stoops, J. K., Roche, T. E., and Zhou, Z. H. (2008) Structures of the human pyruvate dehydrogenase complex cores: a highly conserved catalytic center with flexible N-terminal domains. Structure 16, 104-114
16. Vijayakrishnan, S., Kelly, S. M., Gilbert, R. J., Callow, P., Bhella, D., Forsyth, T., Lindsay, J. G., and Byron, O. (2010) Solution structure and characterisation of the human pyruvate dehydrogenase complex core assembly. J. Mol. Biol. 399, 71-93
17. Mattevi, A., Obmolova, G., Kalk, K. H., Westphal, A. H., de Kok, A., and Hol, W. G. (1993) Refined crystal structure of the catalytic domain of dihydrolipoyl transacetylase (E2p) from Azotobacter vinelandii at 2.6 A resolution. J. Mol. Biol. 230, 1183-1199
18. Knapp, J. E., Mitchell, D. T., Yazdi, M. A., Ernst, S. R., Reed, L. J., and Hackert, M. L. (1998) Crystal structure of the truncated cubic core component of the Escherichia coli 2-oxoglutarate dehydrogenase multienzyme complex. J. Mol. Biol. 280, 655-668
19. Mattevi, A., Obmolova, G., Kalk, K. H., Teplyakov, A., and Hol, W. G. (1993) Crystallographic analysis of substrate binding and catalysis in dihydrolipoyl transacetylase (E2p). Biochemistry 32, 3887-3901
20. Leslie, A. G. W., Moody, P. C. E., and Shaw, W. V. (1988) Structure of chloramphenicol acetyltransferase at 1.75 A resolution. Proc. Natl. Acad. Sci. U.S.A. 85, 4133-4137
21. Kato, M., Wynn, R. M., Chuang, J. L., Brautigam, C. A., Custorio, M., and Chuang, D. T. (2006) A synchronized substrate-gating mechanism revealed by cubic core structure of the bovine branched chain-ketoacid dehydrogenase complex. EMBO J. 25, 5983-5994
22. Knapp, J. E., Carroll, D., Lawson, J. E., Ernst, S. R., Reed, L. J., and Hackert, M. L. (2000) Expression, purification, and structural analysis of the trimeric form of the catalytic domain of the Escherichia coli dihydrolipoamide succinyltransferase. Protein Sci. 9, 37-48
23. Hendle, J., Mattevi, A., Westphal, A. H., Spee, J., de Kok, A., Teplyakov, A., and Hol, W. G. (1995) Crystallographic and enzymatic investigations on the role of Ser558, His610, and Asn614 in the catalytic mechanism of Azotobacter vinelandii dihydrolipoamide acetyltransferase (E2p). Biochemistry 34, 4287-4298
24. Marrott, N. L., Marshall, J. J., Svergun, D. I., Crennell, S. J., Hough, D. W., Danson, M. J., and van den Elsen, J. M. (2012) The catalytic core of an archaeal 2-oxoacid dehydrogenase multienzyme complex is a 42-mer protein assembly. FEBS J. 279, 713-723
25. Izard, T., Aevarsson, A., Allen, M. D., Westphal, A. H., Perham, R. N., de Kok, A., and Hol, W. G. (1999) Principles of quasi-equivalence and Euclidean geometry govern the assembly of cubic and dodecahedral cores of pyruvate dehydrogenase complexes. Proc. Natl. Acad. Sci. U.S.A. 96, 1240-1245
26. Arjunan, P., Nemeria, N., Brunskill, A., Chandrasekhar, K., Sax, M., Yan, Y., Jordan, F., Guest, J. R., and Furey, W. (2002) Structure of the pyruvate dehydrogenase multienzyme complex E1 component from Escherichia coli at 1.85 A resolution. Biochemistry 41, 5213-5221
27. Chandrasekhar, K., Wang, J., Arjunan, P., Sax, M., Park, Y.-H., Nemeria, N. S., Kumaran, S., Song, J., Jordan, F., and Furey, W. (2013) Insight to the interaction of the dihydrolipoamide acetyltransferase (E2) core with the peripheral components in the Escherichia coli pyruvate dehydrogenase complex via multifaceted structural approaches. J. Biol. Chem. 288, 15402-15417
28. Song, J., Park, Y. H., Nemeria, N. S., Kale, S., Kakalis, L., and Jordan, F. (2010) Nuclear magnetic resonance evidence for the role of the flexible regions of the E1 component of the pyruvate dehydrogenase complex from gram-negative bacteria. J. Biol. Chem. 285, 4680-4694
29. Ali, S. T., and Guest, J. R. (1990) Isolation and characterization of lipoylated and unlipoylated domains of the E2p subunit of the pyruvate dehydrogenase complex of Escherichia coli. Biochem. J. 271, 139-145
30. Jones, D. D., Horne, H. J., Reche, P. A., and Perham, R. N. (2000) Structural determinants of post-translational modification and catalytic specificity for the lipoyl domains of the pyruvate dehydrogenase multienzyme complex of Escherichia coli. J. Mol. Biol. 295, 289-306
31. Nemeria, N., Volkov, A., Brown, A., Yi, J., Zipper, L., Guest, J. R., and Jordan, F. (1998) Systematic study of the six cysteines of the E1 subunit of the pyruvate dehydrogenase multienzyme complex from Escherichia coli: none is essential for activity. Biochemistry 37, 911-922
32. Hamuro, Y., Coales, S. J., Molnar, K. S., Tuske, S. J., and Morrow, J. A. (2008) Specificity of immobilized porcine pepsin in H/D exchange compatible conditions. Rapid Commun. Mass Spectrom. 22, 1041-1046
33. Weis, D. D., Engen, J. R., and Kass, I. J. (2006) Semi-automated data processing of hydrogen exchange mass spectra using HX-Express. J. Am. Soc. Mass Spectrom. 17, 1700-1703
34. Kavan, D., and Man, P. (2011) MSTools: Web based application for visualization and presentation of HXMS data. Int. J. Mass Spectrom. 302, 53-58
35. Nambi, S., Badireddy, S., Visweswariah, S. S., and Anand, G. S. (2012) Cyclic AMP-induced conformational changes in micobacterial protein acetyltransferases. J. Biol. Chem. 287, 18115-18129
36. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
37. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMR Pipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
38. Keller, R. L. (2004) The Computer Aided Resonance Assignment, CANTINA Verlag, Goldau, Switzerland
39. Yamazaki, T., Lee, W., Arrowsmith, C. H., Muhandiram, D. R., and Kay, L. E. (1994)Asuite of triple resonanceNMRexperiments for the backbone assignment of 15N-, 13C-,2H-labeled proteins with high sensitivity. J. Am. Chem. Soc. 116, 11655-11666
40. Live, D. H., Davis, D. G., Agosta, W. C., and Cowburn, D. (1984) Observation of 1000-fold enhancement of 15N NMR via proton-detected multiquantum coherences: studies of large peptides. J. Am. Chem. Soc. 106, 6104-6105
41. Russell, G. C., and Guest, J. R. (1991) Sequence similarities within the family of dihydrolipoamide acetyltransferases and discovery of a previously unidentified fungal enzyme. Biochim. Biophys. Acta 1076, 225-232
42. Russell, G. C., and Guest, J. R. (1990) Overexpression of restructured pyruvate dehydrogenase complexes and site-directed mutagenesis of a potential active-site histidine residue. Biochem. J. 269, 443-450
43. Russell, G. C., and Guest, J. R. (1991) Site-directed mutagenesis of the lipoate acetyltransferase of Escherichia coli. Proc. Biol. Sci. 243, 155-160
44. Yang, Y. S., and Frey, P. A. (1986) Dihydrolipoyl tranaacetylase of Esche- richia coli: formation of 8-S-acetyldihydrolipoamide. Biochemistry 25, 8173-8178
45. Butterworth, P. J., Tsai, C. S., Eley, M. H., Roche, T. E., and Reed, L. J. (1975) A kinetic study of dihydrolipoyl transacetylase from bovine kidney. J. Biol. Chem. 250, 1921-1925
46. Allen, M. D., and Perham, R. N. (1997) The catalytic domain of dihydrolipoyl acetyltransferase from the pyruvate dehydrogenase multienzyme complex of Bacillus stearothermophilus: expresssion, purification and reversible denaturation. FEBS Lett. 413, 339-343
47. Niu, X.-D., Stoops, J. K., and Reed, L. J. (1990) Overexpression and mutagenesis of the catalytic domain of dihydrolipoamide acetyltransferase from Saccharomyces cerevisiae. Biochemistry 29, 8614-8619
48. CaJacob, C. A., Gavino, G. R., and Frey, P. A. (1985) Pyruvate dehydrogenase complex of Escherichia coli: thiamin pyrophosphate and NADH-dependent hydrolysis of acetyl-CoA. J. Biol. Chem. 260, 14610-14615
49. Song, J., and Jordan, F. (2012) Interchain acetyl transfer in the E2 component of bacterial pyruvate dehydrogenase suggests a model with different roles for each chain in a trimer of the homooligomeric component. Biochemistry 51, 2795-2803
50. Park, Y. H., Wei, W., Zhou, L., Nemeria, N., and Jordan, F. (2004) Aminoterminal residues 1-45 of the Escherichia coli pyruvate dehydrogenase complex E1 subunit interact with the E2 subunit and are required for activity of the complex but not for reductive acetylation of the E2 subunit. Biochemistry 43, 14037-14046
51. Schulze, E., Westphal, A. H., Obmolova, G., Mattevi, A., Hol, W. G., and de Kok, A. (1991) The catalytic domain of the dihydrolipoyl transacetylase component of the pyruvate dehydrogenase complex from Azotobacter vinelandii and Escherichia coli: expression, purification, properties and preliminary x-ray analysis. Eur. J. Biochem. 201, 561-568
52. Jones, D. D., Stott, K. M., Howard, M. J., and Perham, R. N. (2000) Resticted motion of the lipoyl-lysine swinging arm in the pyruvate dehydrogenase complex of Escherichia coli. Biochemistry 39, 8448-8459
53. Jones, D. D., Stott, K. M., Reche, P. A., and Perham, R. N. (2001) Recognition of the lipoyl domain is the ultimate determinant of substrate channeling in the pyruvate dehydrogenase multienzyme complex. J. Mol. Biol. 305, 49-60
54. Jordan, F., Nemeria, N. S., Zhang, S., Yan, Y., Arjunan, P., and Furey, W. (2003) Dual catalytic apparatus of the thiamin diphosphate coenzyme: acid-base via the 1′,4′-iminopyrimidine tautomer along with its electrophilic role. J. Am. Chem. Soc. 125, 12732-12738
55. Nemeria, N., Baykal, A., Joseph, E., Zhang, S., Yan, Y., Furey, W., and Jordan, F. (2004) Tetrahedral intermediates in thiamin diphosphate-dependent decarboxylations exist as a 1′,4′-imino tautomeric form of the coenzyme, unlike the Michaelis complex or the free coenzyme. Biochemistry 43, 6565-6575
56. Nemeria, N., Chakraborty, S., Baykal, A., Korotchkina L. G., Patel, M. S., and Jordan, F. (2007) The 1′,4′-iminopyrimidine tautomer of thiamin diphosphate is poised for catalysis in asymmetric active centers on enzymes. Proc. Natl. Acad. Sci. U.S.A. 104, 78-82
57. Nemeria, N., Korotchkina L., McLeish M. J., Kenyon G. L., Patel M. S., and Jordan, F. (2007) Elucidation of the chemistry of enzyme-bound thiamin diphosphate prior to substrate binding: defining internal equilibria among tautomeric and ionization states. Biochemistry 46, 10739-10744
58. Nemeria N. S., Chakraborty, S., Balakrishnan, A., and Jordan, F. (2009) Defining states of ionization and tautomerization of the coenzyme at individual steps on thiamin diphosphate dependent enzymatic pathways, FEBS J. 276, 2432-2446
59. Hupe, D. J., and Jencks, W. P. (1977) Nonlinear structure-reactivity correlations: acyl transfer between sulfur and oxygen nucleophiles. J. Am. Chem. Soc. 99, 451-464
60. Shuker, S. B., Hajduk, P. J., Meadows, R. P., and Fesik, S. W. (1996) Discovering high affinity ligands for proteins: SAR by NMR. Science 274, 1531-1534
61. Tompa P. (2014) Multisteric regulation by structural disorder in modular signaling proteins: an extension of the concept of allostery. Chem. Rev., in press
62. Jordan, F., and Nemeria, N. (2005) Experimental observation of thiamin diphosphate-bound intermediates on enzymes and the mechanistic information derived from these observations. Bioorg. Chem. 33, 190-215