Crystal structures of malonyl-coenzyme a decarboxylase provide insights into its catalytic mechanism and disease-causing mutations

Structure

Volumn 21, Issue 7, 2013, Pages 1182-1192

  Froese, D Sean ^a   Forouhar, Farhad ^b   Tran, Timothy H ^b   Vollmar, Melanie ^a   Kim, Yi Seul ^b   Lew, Scott ^b   Neely, Helen ^b   Seetharaman, Jayaraman ^b   Shen, Yang ^b   Xiao, Rong ^c,d   Acton, Thomas B ^c,d   Everett, John K ^c,d   Cannone, Giuseppe ^e   Puranik, Sriharsha ^a   Savitsky, Pavel ^a   Krojer, Tobias ^a   Pilka, Ewa S ^a   Kiyani, Wasim ^a   Lee, Wen Hwa ^a   Marsden, Brian D ^a   Von Delft, Frank ^a   Allerston, Charles K ^a   Spagnolo, Laura ^e   Gileadi, Opher ^a   Montelione, Gaetano T ^c,d   Oppermann, Udo ^a   Yue, Wyatt W ^a   Tong, Liang ^b   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; MALONYL COENZYME A DECARBOXYLASE; MONOMER;

AGROBACTERIUM VITIS; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CRYSTALLIZATION; CUPRIAVIDUS; CUPRIAVIDUS METALLIDURANS; ELECTRON MICROSCOPY; ENZYME ACTIVE SITE; HUMAN; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RHIZOBIUM; RHODOPSEUDOMONAS PALUSTRIS; STRUCTURAL HOMOLOGY; ULTRACENTRIFUGATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CARBOXY-LYASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DEFICIENCY DISEASES; ENZYME STABILITY; HUMANS; HYDROGEN BONDING; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; STRUCTURAL HOMOLOGY, PROTEIN;

AGROBACTERIUM VITIS; CUPRIAVIDUS METALLIDURANS; RHODOPSEUDOMONAS PALUSTRIS;

EID: 84879844708     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.05.001     Document Type: Article

References (70)

1. J.P. Abrahams, and A.G.W. Leslie Methods used in the structure determination of bovine mitochondrial F1 ATPase Acta Crystallogr. D Biol. Crystallogr. 52 1996 30 42
2. T.B. Acton, K.C. Gunsalus, R. Xiao, L.C. Ma, J. Aramini, M.C. Baran, Y.W. Chiang, T. Climent, B. Cooper, and N.G. Denissova Robotic cloning and protein production platform of the Northeast Structural Genomics Consortium Methods Enzymol. 394 2005 210 243
3. J. An, D.M. Muoio, M. Shiota, Y. Fujimoto, G.W. Cline, G.I. Shulman, T.R. Koves, R. Stevens, D. Millington, and C.B. Newgard Hepatic expression of malonyl-CoA decarboxylase reverses muscle, liver and whole-animal insulin resistance Nat. Med. 10 2004 268 274
4. D. Aparicio, R. Pérez-Luque, X. Carpena, M. Díaz, J.C. Ferrer, P.C. Loewen, and I. Fita Structural asymmetry and disulfide bridges among subunits modulate the activity of human malonyl-CoA decarboxylase J. Biol. Chem. 288 2013 11907 11919
5. M.M. Benning, T. Haller, J.A. Gerlt, and H.M. Holden New reactions in the crotonase superfamily: structure of methylmalonyl CoA decarboxylase from Escherichia coli Biochemistry 39 2000 4630 4639
6. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.-S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
7. J.-F. Cheng, M. Chen, D. Wallace, S. Tith, M. Haramura, B. Liu, C.C. Mak, T. Arrhenius, S. Reily, and S. Brown Synthesis and structure-activity relationship of small-molecule malonyl coenzyme A decarboxylase inhibitors J. Med. Chem. 49 2006 1517 1525
8. J.-F. Cheng, Y. Huang, R. Penuliar, M. Nishimoto, L. Liu, T. Arrhenius, G. Yang, E. O'leary, M. Barbosa, and R. Barr Discovery of potent and orally available malonyl-CoA decarboxylase inhibitors as cardioprotective agents J. Med. Chem. 49 2006 4055 4058
9. J.-F. Cheng, C.C. Mak, Y. Huang, R. Penuliar, M. Nishimoto, L. Zhang, M. Chen, D. Wallace, T. Arrhenius, and D. Chu Heteroaryl substituted bis-trifluoromethyl carbinols as malonyl-CoA decarboxylase inhibitors Bioorg. Med. Chem. Lett. 16 2006 3484 3488
10. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
11. D.R. Cooper, T. Boczek, K. Grelewska, M. Pinkowska, M. Sikorska, M. Zawadzki, and Z. Derewenda Protein crystallization by surface entropy reduction: optimization of the SER strategy Acta Crystallogr. D Biol. Crystallogr. 63 2007 636 645
12. C. Courchesne-Smith, S.H. Jang, Q. Shi, J. DeWille, G. Sasaki, and P.E. Kolattukudy Cytoplasmic accumulation of a normally mitochondrial malonyl-CoA decarboxylase by the use of an alternate transcription start site Arch. Biochem. Biophys. 298 1992 576 586
13. K. Cowtan The Buccaneer software for automated model building. 1. Tracing protein chains Acta Crystallogr. D Biol. Crystallogr. 62 2006 1002 1011
14. J.E. Cronan Jr., and G.L. Waldrop Multi-subunit acetyl-CoA carboxylases Prog. Lipid Res. 41 2002 407 435
15. S. Doublié, U. Kapp, A. Aberg, K. Brown, K. Strub, and S. Cusack Crystallization and preliminary X-ray analysis of the 9 kDa protein of the mouse signal recognition particle and the selenomethionyl-SRP9 FEBS Lett. 384 1996 219 221
16. J.R.B. Dyck, T.A. Hopkins, S. Bonnet, E.D. Michelakis, M.E. Young, M. Watanabe, Y. Kawase, K.I. Jishage, and G.D. Lopaschuk Absence of malonyl coenzyme A decarboxylase in mice increases cardiac glucose oxidation and protects the heart from ischemic injury Circulation 114 2006 1721 1728
17. F. Dyda, D.C. Klein, and A.B. Hickman GCN5-related N-acetyltransferases: a structural overview Annu. Rev. Biophys. Biomol. Struct. 29 2000 81 103
18. P. Emsley, and K.D. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
19. M. Fantino Role of lipids in the control of food intake Curr. Opin. Clin. Nutr. Metab. Care 14 2011 138 144
20. C.D.L. Folmes, and G.D. Lopaschuk Role of malonyl-CoA in heart disease and the hypothalamic control of obesity Cardiovasc. Res. 73 2007 278 287
21. Z. Fu, M. Wang, R. Paschke, K.S. Rao, F.E. Frerman, and J.J. Kim Crystal structure of human glutaryl-CoA dehydrogenase with and without an alternate substrate: structural bases of dehydrogenation and decarboxylation reactions Biochemistry 43 2004 9674 9684
22. J. Gao, L. Waber, M.J. Bennett, K.M. Gibson, and J.C. Cohen Cloning and mutational analysis of human malonyl-coenzyme A decarboxylase J. Lipid Res. 40 1999 178 182
23. T.D. Goddard, C.C. Huang, and T.E. Ferrin Visualizing density maps with UCSF Chimera J. Struct. Biol. 157 2007 281 287
24. L. Goldschmidt, D.R. Cooper, Z.S. Derewenda, and D. Eisenberg Toward rational protein crystallization: A Web server for the design of crystallizable protein variants Protein Sci. 16 2007 1569 1576
25. L. Gu, T.W. Geders, B. Wang, W.H. Gerwick, K. Håkansson, J.L. Smith, and D.H. Sherman GNAT-like strategy for polyketide chain initiation Science 318 2007 970 974
26. H. Guillou, D. Zadravec, P.G.P. Martin, and A. Jacobsson The key roles of elongases and desaturases in mammalian fatty acid metabolism: Insights from transgenic mice Prog. Lipid Res. 49 2010 186 199
27. L. Holm, S. Kääriäinen, P. Rosenström, and A. Schenkel Searching protein structure databases with DaliLite v.3 Bioinformatics 24 2008 2780 2781
28. 13C-enriched fusion proteins in Escherichia coli J. Biomol. NMR 7 1996 131 141
29. E. Joly, M. Bendayan, R. Roduit, A.K. Saha, N.B. Ruderman, and M. Prentki Malonyl-CoA decarboxylase is present in the cytosolic, mitochondrial and peroxisomal compartments of rat hepatocytes FEBS Lett. 579 2005 6581 6586
30. J.S. Jung, D.J. Baek, G.Y. Lee, Y.S. Kim, and B.H. Oh Crystallization and preliminary X-ray crystallographic analysis of malonyl-CoA decarboxylase from Rhizobium leguminosarum bv. trifolii Acta Crystallogr. D Biol. Crystallogr. 59 2003 166 167
31. W. Kabsch Integration, scaling, space-group assignment and post-refinement Acta Crystallogr. D Biol. Crystallogr. 66 2010 133 144
32. Y.S. Kim, and P.E. Kolattukudy Purification and properties of malonyl-CoA decarboxylase from rat liver mitochondria and its immunological comparison with the enzymes from rat brain, heart, and mammary gland Arch. Biochem. Biophys. 190 1978 234 246
33. P.E. Kolattukudy, A.J. Poulose, and Y.S. Kim Malonyl-CoA decarboxylase from avian, mammalian, and microbial sources Methods Enzymol. 71 Pt C 1981 150 163
34. F.P. Kuhajda Fatty acid synthase and cancer: new application of an old pathway Cancer Res. 66 2006 5977 5980
35. M.D. Lane, M. Wolfgang, S.H. Cha, and Y. Dai Regulation of food intake and energy expenditure by hypothalamic malonyl-CoA Int. J. Obes. (Lond.) 32 Suppl 4 2008 S49 S54
36. T.M. Laue, B.D. Shah, T.M. Ridgeway, and S.L. Pelletier Computer-aided interpretation of analytical sedimentation data for proteins S.E. Harding, A.J. Rowe, J.C. Horton, Analytical ultracentrifugation in biochemistry and polymer science 1992 The Royal Society of Chemistry Cambridge 90 125
37. G.Y. Lee, Y.Y. Bahk, and Y.S. Kim Rat malonyl-CoA decarboxylase; cloning, expression in E. coli and its biochemical characterization J. Biochem. Mol. Biol. 35 2002 213 219
38. J. Liu, G.T. Montelione, and B. Rost Novel leverage of structural genomics Nat. Biotechnol. 25 2007 849 851
39. M.C. Lo, M. Wang, K.W. Kim, J. Busby, H. Yamane, J. Zondlo, C. Yuan, S.W. Young, and S.H. Xiao A highly sensitive high-throughput luminescence assay for malonyl-CoA decarboxylase Anal. Biochem. 376 2008 122 130
40. G.D. Lopaschuk, J.R. Ussher, and J.S. Jaswal Targeting intermediary metabolism in the hypothalamus as a mechanism to regulate appetite Pharmacol. Rev. 62 2010 237 264
41. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97
42. S. Malvagia, L. Papi, A. Morrone, M.A. Donati, F. Ciani, E. Pasquini, G. la Marca, H.R. Scholte, M. Genuardi, and E. Zammarchi Fatal malonyl CoA decarboxylase deficiency due to maternal uniparental isodisomy of the telomeric end of chromosome 16 Ann. Hum. Genet. 71 2007 705 712
43. J.D. McGarry, and N.F. Brown The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis Eur. J. Biochem. 244 1997 1 14
44. D.E. McRee XtalView/Xfit - A versatile program for manipulating atomic coordinates and electron density J. Struct. Biol. 125 1999 156 165
45. H.W. Nam, G.Y. Lee, and Y.S. Kim Mass spectrometric identification of K210 essential for rat malonyl-CoA decarboxylase catalysis J. Proteome Res. 5 2006 1398 1406
46. A.F. Neuwald, and D. Landsman GCN5-related histone N-acetyltransferases belong to a diverse superfamily that includes the yeast SPT10 protein Trends Biochem. Sci. 22 1997 154 155
47. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
48. R.R. Ramsay, R.D. Gandour, and F.R. van der Leij Molecular enzymology of carnitine transfer and transport Biochim. Biophys. Acta 1546 2001 21 43
49. K.A. Sacksteder, J.C. Morrell, R.J.A. Wanders, R. Matalon, and S.J. Gould MCD encodes peroxisomal and cytoplasmic forms of malonyl-CoA decarboxylase and is mutated in malonyl-CoA decarboxylase deficiency J. Biol. Chem. 274 1999 24461 24468
50. D. Saggerson Malonyl-CoA, a key signaling molecule in mammalian cells Annu. Rev. Nutr. 28 2008 253 272
51. G.S. Salomons, C. Jakobs, L.L. Pope, A. Errami, M. Potter, M. Nowaczyk, S. Olpin, N. Manning, J.A.J. Raiman, and T. Slade Clinical, enzymatic and molecular characterization of nine new patients with malonyl-coenzyme A decarboxylase deficiency J. Inherit. Metab. Dis. 30 2007 23 28
52. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78 2000 1606 1619
53. G.M. Sheldrick A short history of SHELX Acta Crystallogr. A 64 2008 112 122
54. H. Tang, Y. Yan, Z. Feng, R.K. de Jesus, L. Yang, D.A. Levorse, K.A. Owens, T.E. Akiyama, R. Bergeron, and G.A. Castriota Design and synthesis of a new class of malonyl-CoA decarboxylase inhibitors with anti-obesity and anti-diabetic activities Bioorg. Med. Chem. Lett. 20 2010 6088 6092
55. T.C. Terwilliger SOLVE and RESOLVE: automated structure solution and density modification Methods Enzymol. 374 2003 22 37
56. L. Tong Structure and function of biotin-dependent carboxylases Cell. Mol. Life Sci. 70 2013 863 891
57. J.R. Ussher, and G.D. Lopaschuk Targeting malonyl CoA inhibition of mitochondrial fatty acid uptake as an approach to treat cardiac ischemia/reperfusion Basic Res. Cardiol. 104 2009 203 210
58. A.A. Vagin, and A. Teplyakov An approach to multi-copy search in molecular replacement Acta Crystallogr. D Biol. Crystallogr. 56 2000 1622 1624
59. M. van Heel, G. Harauz, E.V. Orlova, R. Schmidt, and M. Schatz A new generation of the IMAGIC image processing system J. Struct. Biol. 116 1996 17 24
60. M.W. Vetting, L.P. S de Carvalho, M. Yu, S.S. Hegde, S. Magnet, S.L. Roderick, and J.S. Blanchard Structure and functions of the GNAT superfamily of acetyltransferases Arch. Biochem. Biophys. 433 2005 212 226
61. M.W. Vetting, J.C. Errey, and J.S. Blanchard Rv0802c from Mycobacterium tuberculosis: the first structure of a succinyltransferase with the GNAT fold Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64 2008 978 985
62. C. Vonrhein, E. Blanc, P. Roversi, and G. Bricogne Automated structure solution with autoSHARP Methods Mol. Biol. 364 2007 215 230
63. S.J. Wakil, J.K. Stoops, and V.C. Joshi Fatty acid synthesis and its regulation Annu. Rev. Biochem. 52 1983 537 579
64. D.M. Wallace, M. Haramura, J.-F. Cheng, T. Arrhenius, and A.M. Nadzan Novel trifluoroacetophenone derivatives as malonyl-CoA decarboxylase inhibitors Bioorg. Med. Chem. Lett. 17 2007 1127 1130
65. P.J. Wightman, R. Santer, A. Ribes, F. Dougherty, N. McGill, D.R. Thorburn, and D.R. FitzPatrick MLYCD mutation analysis: evidence for protein mistargeting as a cause of MLYCD deficiency Hum. Mutat. 22 2003 288 300
66. M.J. Wolfgang, and M.D. Lane Hypothalamic malonyl-coenzyme A and the control of energy balance Mol. Endocrinol. 22 2008 2012 2020
67. J. Xue, J. Peng, M. Zhou, L. Zhong, F. Yin, D. Liang, and L. Wu Novel compound heterozygous mutation of MLYCD in a Chinese patient with malonic aciduria Mol. Genet. Metab. 105 2012 79 83
68. V.A. Zammit The malonyl-CoA-long-chain acyl-CoA axis in the maintenance of mammalian cell function Biochem. J. 343 1999 505 515
69. D. Zhou, P. Yuen, D. Chu, V. Thon, S. McConnell, S. Brown, A. Tsang, M. Pena, A. Russell, and J.-F. Cheng Expression, purification, and characterization of human malonyl-CoA decarboxylase Protein Expr. Purif. 34 2004 261 269
70. W. Zhou, Y. Tu, P.J. Simpson, and F.P. Kuhajda Malonyl-CoA decarboxylase inhibition is selectively cytotoxic to human breast cancer cells Oncogene 28 2009 2979 2987