The dynamic organization of fungal acetyl-CoA carboxylase

Nature Communications

Volumn 7, Issue , 2016, Pages

  Hunkeler, Moritz ^a   Stuttfeld, Edward ^a   Hagmann, Anna ^a   Imseng, Stefan ^a   Maier, Timm ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; MULTIENZYME COMPLEX; SACCHAROMYCES CEREVISIAE PROTEIN;

CANCER; DRUG; ENZYME ACTIVITY; EUKARYOTE; FUNGUS; PHOSPHORUS; YEAST;

ARTICLE; CHAETOMIUM; CHAETOMIUM THERMOPHILUM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ENZYME STRUCTURE; NONHUMAN; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; X RAY CRYSTALLOGRAPHY; YEAST; CHEMISTRY; CONSERVED SEQUENCE; ENZYMOLOGY; HUMAN; METABOLISM; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

EUKARYOTA;

ACETYL-COA CARBOXYLASE; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MULTIENZYME COMPLEXES; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84963956676     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11196     Document Type: Article

References (70)

1. Wakil, S. J., Titchener, E. B. & Gibson, D. M. Evidence for the participation of biotin in the enzymic synthesis of fatty acids. Biochim. Biophys. Acta 29, 225-226 (1958).
2. Wakil, S. J., Stoops, J. K. & Joshi, V. C. Fatty acid synthesis and its regulation. Annu. Rev. Biochem. 52, 537-579 (1983).
3. Abu-Elheiga, L., Matzuk, M. M., Abo-Hashema, K. A. & Wakil, S. J. Continuous fatty acid oxidation and reduced fat storage in mice lacking acetyl-CoA carboxylase 2. Science 291, 2613-2616 (2001).
4. Abu-Elheiga, L., Oh, W., Kordari, P. & Wakil, S. J. Acetyl-CoA carboxylase 2 mutant mice are protected against obesity and diabetes induced by high-fat/ high-carbohydrate diets. Proc. Natl Acad. Sci. USA 100, 10207-10212 (2003).
5. Harwood, H. J. J. Acetyl-CoA carboxylase inhibition for the treatment of metabolic syndrome. Curr. Opin. Invest. Drugs 5, 283-289 (2004).
6. Milgraum, L. Z., Witters, L. A., Pasternack, G. R. & Kuhajda, F. P. Enzymes of the fatty acid synthesis pathway are highly expressed in in situ breast carcinoma. Clin. Cancer Res. 3, 2115-2120 (1997).
7. Swinnen, J. V., Brusselmans, K. & Verhoeven, G. Increased lipogenesis in cancer cells: new players, novel targets. Curr. Opin. Clin. Nutr. Metab. Care 9, 358-365 (2006).
8. Williams, R. S., Lee, M. S., Hau, D. D. & Glover, J. N. Structural basis of phosphopeptide recognition by the BRCT domain of BRCA1. Nat. Struct. Mol. Biol. 11, 519-525 (2004).
9. Shen, Y. & Tong, L. Structural evidence for direct interactions between the BRCT domains of human BRCA1 and a phospho-peptide from human ACC1. Biochemistry 47, 5767-5773 (2008).
10. Tong, L. Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery. Cell Mol. Life Sci. 62, 1784-1803 (2005).
11. Wakil, S. J. & Abu-Elheiga, L. A. Fatty acid metabolism: target for metabolic syndrome. J. Lipid Res. 50(Suppl): S138-S143 (2009).
12. Shen, Y., Volrath, S. L., Weatherly, S. C., Elich, T. D. & Tong, L. A mechanism for the potent inhibition of eukaryotic acetyl-coenzyme A carboxylase by soraphen A, a macrocyclic polyketide natural product. Mol. Cell 16, 881-891 (2004).
13. Campbell, J. W. & Cronan, Jr. J. E. Bacterial fatty acid biosynthesis: targets for antibacterial drug discovery. Annu. Rev. Microbiol. 55, 305-332 (2001).
14. Weatherly, S. C., Volrath, S. L. & Elich, T. D. Expression and characterization of recombinant fungal acetyl-CoA carboxylase and isolation of a soraphenbinding domain. Biochem. J. 380, 105-110 (2004).
15. Alberts, A. W. & Vagelos, P. R. Acetyl CoA carboxylase. I. Requirement for two protein fractions. Proc. Natl Acad. Sci. USA 59, 561-568 (1968).
16. Alberts, A. W., Nervi, A. M. & Vagelos, P. R. Acetyl CoA carboxylase, II. Deomonstration of biotin-protein and biotin carboxylase subunits. Proc. Natl Acad. Sci. USA 63, 1319-1326 (1969).
17. Cronan, Jr. J. E. & Waldrop, G. L. Multi-subunit acetyl-CoA carboxylases. Prog. Lipid Res. 41, 407-435 (2002).
18. Bianchi, A. et al. Identification of an isozymic form of acetyl-CoA carboxylase. J. Biol. Chem. 265, 1502-1509 (1990).
19. Abu-Elheiga, L. et al. The subcellular localization of acetyl-CoA carboxylase 2. Proc. Natl Acad. Sci. USA 97, 1444-1449 (2000).
20. Brownsey, R. W., Boone, A. N., Elliott, J. E., Kulpa, J. E. & Lee, W. M. Regulation of acetyl-CoA carboxylase. Biochem. Soc. Trans. 34, 223-227 (2006).
21. Munday, M. R. Regulation of mammalian acetyl-CoA carboxylase. Biochem. Soc. Trans. 30, 1059-1064 (2002).
22. Shi, S., Chen, Y., Siewers, V. & Nielsen, J. Improving production of malonyl coenzyme A-derived metabolites by abolishing Snf1-dependent regulation of Acc1. MBio 5, e01130-01114 (2014).
23. Huang, C. S. et al. Crystal structure of the alpha(6)beta(6) holoenzyme of propionyl-coenzyme A carboxylase. Nature 466, 1001-1005 (2010).
24. Huang, C. S., Ge, P., Zhou, Z. H. & Tong, L. An unanticipated architecture of the 750-kDa alpha6beta6 holoenzyme of 3-methylcrotonyl-CoA carboxylase. Nature 481, 219-223 (2012).
25. Waldrop, G. L., Rayment, I. & Holden, H. M. Three-dimensional structure of the biotin carboxylase subunit of acetyl-CoA carboxylase. Biochemistry 33, 10249-10256 (1994).
26. Athappilly, F. K. & Hendrickson, W. A. Structure of the biotinyl domain of acetyl-coenzyme A carboxylase determined by MAD phasing. Structure 3, 1407-1419 (1995).
27. Zhang, H., Yang, Z., Shen, Y. & Tong, L. Crystal structure of the carboxyltransferase domain of acetyl-coenzyme A carboxylase. Science 299, 2064-2067 (2003).
28. Bilder, P. et al. The structure of the carboxyltransferase component of acetyl-coA carboxylase reveals a zinc-binding motif unique to the bacterial enzyme. Biochemistry 45, 1712-1722 (2006).
29. Tong, L. Structure and function of biotin-dependent carboxylases. Cell Mol. Life Sci. 70, 863-891 (2013).
30. St Maurice, M. et al. Domain architecture of pyruvate carboxylase, a biotin-dependent multifunctional enzyme. Science 317, 1076-1079 (2007).
31. Tran, T. H. et al. Structure and function of a single-chain, multi-domain long-chain acyl-CoA carboxylase. Nature 518, 120-124 (2015).
32. Kim, C. W. et al. Induced polymerization of mammalian acetyl-CoA carboxylase by MIG12 provides a tertiary level of regulation of fatty acid synthesis. Proc. Natl Acad. Sci. USA 107, 9626-9631 (2010).
33. Ray, H., Moreau, K., Dizin, E., Callebaut, I. & Venezia, N. D. ACCA phosphopeptide recognition by the BRCT repeats of BRCA1. J. Mol. Biol. 359, 973-982 (2006).
34. Davies, S. P., Sim, A. T. & Hardie, D. G. Location and function of three sites phosphorylated on rat acetyl-CoA carboxylase by the AMP-activated protein kinase. Eur. J. Biochem. 187, 183-190 (1990).
35. Ha, J., Daniel, S., Broyles, S. S. & Kim, K. H. Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 269, 22162-22168 (1994).
36. Cho, Y. S. et al. Molecular mechanism for the regulation of human ACC2 through phosphorylation by AMPK. Biochem. Biophys. Res. Commun. 391, 187-192 (2010).
37. Ficarro, S. B. et al. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat. Biotechnol. 20, 301-305 (2002).
38. Woods, A. et al. Yeast SNF1 is functionally related to mammalian AMPactivated protein kinase and regulates acetyl-CoA carboxylase in vivo. J. Biol. Chem. 269, 19509-19515 (1994).
39. Holt, L. J. et al. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325, 1682-1686 (2009).
40. Diacovich, L. et al. Kinetic and structural analysis of a new group of Acyl-CoA carboxylases found in Streptomyces coelicolor A3(2). J. Biol. Chem. 277, 31228-31236 (2002).
41. Wei, J. & Tong, L. Crystal structure of the 500-kDa yeast acetyl-CoA carboxylase holoenzyme dimer. Nature 526, 723-727 (2015).
42. Bernado, P. Effect of interdomain dynamics on the structure determination of modular proteins by small-angle scattering. Eur. Biophys. J. 39, 769-780 (2010).
43. Smith, J. L., Skiniotis, G. & Sherman, D. H. Architecture of the polyketide synthase module: surprises from electron cryo-microscopy. Curr. Opin. Struct. Biol. 31, 9-19 (2015).
44. Maier, T., Leibundgut, M. & Ban, N. The crystal structure of a mammalian fatty acid synthase. Science 321, 1315-1322 (2008).
45. Brignole, E. J. & Smith, S. Asturias FJ. Conformational flexibility of metazoan fatty acid synthase enables catalysis. Nat. Struct. Mol. Biol. 16, 190-197 (2009).
46. Strieker, M., Tanovic, A. & Marahiel, M. A. Nonribosomal peptide synthetases: structures and dynamics. Curr. Opin. Struct. Biol. 20, 234-240 (2010).
47. Patel, M. S., Nemeria, N. S., Furey, W. & Jordan, F. The pyruvate dehydrogenase complexes: structure-based function and regulation. J. Biol. Chem. 289, 16615-16623 (2014).
48. Fitzgerald, D. J. et al. Protein complex expression by using multigene baculoviral vectors. Nat. Methods 3, 1021-1032 (2006).
49. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
50. Zhang, K. Y., Cowtan, K. & Main, P. Combining constraints for electrondensity modification. Methods Enzymol. 277, 53-64 (1997).
51. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
52. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
53. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
54. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
55. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D 60, 2256-2268 (2004).
56. Pape, T. & Schneider, T. R. HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844 (2004).
57. Olsen, J. V. et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3 (2010).
58. Bian, Y. et al. An enzyme assisted RP-RPLC approach for in-depth analysis of human liver phosphoproteome. J. Proteomics 96, 253-262 (2014).
59. Cantin, G. T. et al. Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteomic analysis. J. Proteome Res. 7, 1346-1351 (2008).
60. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
61. Biasini, M. et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252-W258 (2014).
62. Pei, J. & Grishin, N. V. AL2CO: calculation of positional conservation in a protein sequence alignment. Bioinformatics 17, 700-712 (2001).
63. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
64. Petoukhov, M. V. et al. New developments in the program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350 (2012).
65. Skou, S., Gillilan, R. E. & Ando, N. Synchrotron-based small-angle X-ray scattering of proteins in solution. Nat. Protoc. 9, 1727-1739 (2014).
66. Jacques, D. A. & Trewhella, J. Small-angle scattering for structural biology- Expanding the frontier while avoiding the pitfalls. Protein Sci. 19, 642-657 (2010).
67. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. & Svergun, D. I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282 (2003).
68. Fischer, H., Neto, M. D., Napolitano, H. B., Polikarpov, I. & Craievich, A. F. Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale. J. Appl. Crystallogr. 43, 101-109 (2010).
69. Scheres, S. H. A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 415, 406-418 (2012).
70. Marabini, R. et al. Xmipp: an image processing package for electron microscopy. J. Struct. Biol. 116, 237-240 (1996).