Structure and function of a single-chain, multi-domain long-chain acyl-CoA carboxylase

Nature

Volumn 518, Issue 7537, 2015, Pages 120-124

  Tran, Timothy H ^a   Hsiao, Yu Shan ^b,d   Jo, Jeanyoung ^a   Chou, Chi Yuan ^a,e   Dietrich, Lars E P ^a   Walz, Thomas ^b,c   Tong, Liang ^a  

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

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^e NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; BACTERIAL ENZYME; BIOTIN; HOLOENZYME; NITROGEN; SINGLE CHAIN ENZYME; UNCLASSIFIED DRUG; ACYL COENZYME A; ACYL-COA CARBOXYLASE; CARBON; LIGASE; PROTEIN SUBUNIT;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; MOLECULAR WEIGHT; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

ACYL COENZYME A; BIOCATALYSIS; BIOTIN; CARBON; CARBON-CARBON LIGASES; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; HOLOENZYMES; MODELS, MOLECULAR; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; NITROGEN; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PSEUDOMONAS AERUGINOSA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84925490764     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13912     Document Type: Article

References (45)

1. Tong, L. Structure and function of biotin-dependent carboxylases. Cell. Mol. Life Sci. 70, 863-891 (2013).
2. 2 metabolism: what structures reveal about their reactionmechanisms. Protein Sci. 21, 1597-1619 (2012).
3. Gago, G., Diacovich, L., Arabolaza, A., Tsai, S.-C. & Gramajo, H. Fatty acid biosynthesis in actinomycetes. FEMS Microbiol. Rev. 35, 475-497 (2011).
4. Jitrapakdee, S. et al. Structure, mechanismand regulationof pyruvate carboxylase. Biochem. J. 413, 369-387 (2008).
5. Tong, L. Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery. Cell. Mol. Life Sci. 62, 1784-1803 (2005).
6. Cronan, J. E. Jr & Waldrop, G. L. Multi-subunit acetyl-CoA carboxylases. Prog. Lipid Res. 41, 407-435 (2002).
7. Polyak, S. W., Abell, A. D., Wilce, M. C. J., Zhang, L.&Booker, G. W. Structure, function and selective inhibition of bacterial acetyl-CoA carboxylase. Appl. Microbiol. Biotechnol. 93, 983-992 (2012).
8. Abramson, H. N. The lipogenesis pathway as a cancer target. J. Med. Chem. 54, 5615-5638 (2011).
9. Wakil, S. J. & Abu-Elheiga, L. A. Fatty acid metabolism: target for metabolic syndrome. J. Lipid Res. 50, S138-S143 (2009).
10. Huang, C. S. et al. Crystal structure of the a6b6 holoenzyme of propionyl-coenzyme A carboxylase. Nature 466, 1001-1005 (2010).
11. Huang, C. S., Ge, P., Zhou, Z. H. & Tong, L. An unanticipated architecture of the 750-kDa a6b6 holoezyme of 3-methylcrotonyl-CoA carboxylase. Nature 481, 219-223 (2012).
12. St. Maurice, M. et al. Domain architecture of pyruvate carboxylase, a biotin-dependent multifunctional enzyme. Science 317, 1076-1079 (2007).
13. Xiang, S. & Tong, L. Crystal structures of human and Staphylococcus aureus pyruvate carboxylase and molecular insights into the carboxyltransfer reaction. Nature Struct. Mol. Biol. 15, 295-302 (2008).
14. Fan, C., Chou, C.-Y., Tong, L.&Xiang, S. Crystal structure of urea carboxylase provides insights into the carboxyltransfer reaction. J. Biol. Chem. 287, 9389-9398 (2012).
15. Li, L. et al. The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. Proc. Natl Acad. Sci. USA 102, 12344-12349 (2005).
16. Stover, C. K. et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964 (2000).
17. Lai, H., Kraszewski, J. L., Purwantini, E. & Mukhopadhyay, B. Identification of pyruvate carboxylase genes in Pseudomonas aeruginosa PAO1 and development of a P.aeruginosa-based overexpression system for a4-and a4b4-type pyruvate carboxylases. Appl. Environ. Microbiol. 72, 7785-7792 (2006).
18. Grande, R. et al. The two carboxylases of Corynebacterium glutamicumessential for fatty acid and mycolic acid synthesis. J. Bacteriol. 189, 5257-5264 (2007).
19. 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).
20. Chou, C.-Y., Yu, L. P. C.& Tong, L. Crystal structure of biotin carboxylase in complex with substrates and implications for its catalytic mechanism. J. Biol. Chem. 284, 11690-11697 (2009).
21. Hohn, M. et al. SPARX, a new environment for Cryo-EMimage processing. J. Struct. Biol. 157, 47-55 (2007).
22. Knowles, J. R. The mechanismof biotin-dependent enzymes. Annu. Rev. Biochem. 58, 195-221 (1989).
23. Lin, T. W. et al. Structure-based inhibitor design of AccD5, an essential acyl-CoA carboxylase carboxyltransferase domain of Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 103, 3072-3077 (2006).
24. Forster-Fromme, K. & Jendrossek, D. Catabolism of citronellol and related acyclic terpenoids in pseudomonads. Appl. Microbiol. Biotechnol. 87, 859-869 (2010).
25. Aguilar, J. A. et al. Substrate specificity of the 3-methylcrotonyl coenzyme A (CoA) and geranyl-CoA carboxylases from Pseudomonas aeruginosa. J. Bacteriol. 190, 4888-4893 (2008).
26. Liberati, N. T. et al. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl Acad. Sci. USA 103, 2833-2838 (2006).
27. Shea, A., Wolcott, M., Daefler, S. & Rozak, D. A. Biolog phenotype microarrays. Methods Mol. Biol. 881, 331-373 (2012).
28. Takayama, K., Wang, C. & Besra, G. S. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin. Microbiol. Rev. 18, 81-101 (2005).
29. Zhang, H., Yang, Z., Shen, Y. & Tong, L. Crystal structure of the carboxyltransferase domain of acetyl-coenzyme A carboxylase. Science 299, 2064-2067 (2003).
30. Hendrickson, W. A., Horton, J. R. & LeMaster, D. M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9, 1665-1672 (1990).
31. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
32. McCoy, A. J. et al.Phaser crystallographic software. J.Appl.Cryst. 40, 658-674(2007).
33. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
34. Terwilliger, T. C. SOLVE and RESOLVE: automated structure solution and density modification. Methods Enzymol. 374, 22-37 (2003).
35. Emsley, P. & Cowtan, K. D. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
36. Brunger, A. T. et al. Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
37. Ohi, M., Li, Y., Cheng, Y. & Walz, T. Negative staining and image classification - powerful tools inmodernelectronmicroscopy. Biol.Proced.Online 6, 23-34(2004).
38. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
39. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996).
40. Yang, Z., Fang, J., Chittuluru, J., Asturias, F. J. & Penczek, P. A. Iterative stable alignment and clustering of 2D transmission electron microscope images. Structure 20, 237-247 (2012).
41. Blanchard, C. Z., Lee, Y. M., Frantom, P. A. & Waldrop, G. L. Mutations at four active site residues of biotin carboxylase abolish substrate-induced synergism by biotin. Biochemistry 38, 3393-3400 (1999).
42. Recinos, D. A. et al. Redundant phenazine operons in Pseudomonas aeruginosa exhibit environment-dependent expression and differential roles in pathogenicity. Proc. Natl Acad. Sci. USA 109, 19420-19425 (2012).
43. Shanks, R. M., Caiazza, N. C., Hinsa, S. M., Toutain, C. M. & O'Toole, G. A. Saccharomyces cerevisiae-basedmolecular tool kit for manipulation of genes from Gram-negative bacteria. Appl. Environ. Microbiol. 72, 5027-5036 (2006).
44. Dereeper, A. et al.Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469 (2008).
45. Gouet, P., Courcelle, E., Stuart, D. I. & Metoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999).