The chain-flipping mechanism of ACP (acyl carrier protein)-dependent enzymes appears universal

Biochemical Journal

Volumn 460, Issue 2, 2014, Pages 157-163

  Cronan, John E ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acyl carrier protein (ACP); Chain flipping; Phosphopantetheine thiol; Saturated fatty acid synthesis

Indexed keywords

ACYL CARRIER PROTEIN; ACYLTRANSFERASE; LPXD ENZYME; PANTETHEINE PHOSPHATE; SATURATED FATTY ACID; UNCLASSIFIED DRUG;

ALPHA HELIX; COMPLEX FORMATION; CRYSTAL STRUCTURE; ESCHERICHIA COLI; FATTY ACID SYNTHESIS; HYDROPHOBICITY; MOLECULAR MECHANICS; PRIORITY JOURNAL; REVIEW; SECONDARY METABOLISM; SUBURETHRAL SLING;

ACYL CARRIER PROTEIN; ACYLTRANSFERASES; CRYSTALLIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FATTY ACID SYNTHASE, TYPE II; HYDRO-LYASES; MODELS, MOLECULAR; PANTETHEINE; PROTEIN STRUCTURE, SECONDARY;

EID: 84900475826     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140239     Document Type: Review

References (56)

1. Cronan, Jr, J. E. (2004) The structure of mammalian fatty acid synthase turned back to front. Chem. Biol. 11, 1601-1602 CrossRef PubMed
2. Cronan, J. E. (2006) Remarkable structural variation within fatty acid megasynthases. Nat. Chem. Biol. 2, 232-234 CrossRef PubMed
3. Chan, D. I. and Vogel, H. J. (2010) Current understanding of fatty acid biosynthesis and the acyl carrier protein. Biochem. J. 430, 1-19 CrossRef PubMed
4. Byers, D. M. and Gong, H. (2007) Acyl carrier protein: structure-function relationships in a conserved multifunctional protein family. Biochem. Cell Biol. 85, 649-662 CrossRef PubMed
5. Nguyen, C., Haushalter, R. W., Lee, D. J., Markwick, P. R., Bruegger, J., Caldara-Festin, G., Finzel, K., Jackson, D. R., Ishikawa, F., O'Dowd, B. et al. (2014) Trapping the dynamic acyl carrier protein in fatty acid biosynthesis. Nature 505, 427-431 CrossRef PubMed
6. Leibundgut, M., Jenni, S., Frick, C. and Ban, N. (2007) Structural basis for substrate delivery by acyl carrier protein in the yeast fatty acid synthase. Science 316, 288-290 CrossRef PubMed
7. Matje, D. M., Zhou, H., Smith, D. A., Neely, R. K., Dryden, D. T., Jones, A. C., Dahlquist, F. W. and Reich, N. O. (2013) Enzyme-promoted base flipping controls DNA methylation fidelity. Biochemistry 52, 1677-1685 CrossRef PubMed
8. Roberts, R. J. and Cheng, X. (1998) Base flipping. Annu. Rev. Biochem. 67, 181-198 CrossRef PubMed
9. Agarwal, V., Lin, S., Lukk, T., Nair, S. K. and Cronan, J. E. (2012) Structure of the enzyme-acyl carrier protein (ACP) substrate gatekeeper complex required for biotin synthesis. Proc. Natl. Acad. Sci. U.S.A. 109, 17406-17411 CrossRef PubMed
10. Cryle, M. J. and Schlichting, I. (2008) Structural insights from a P450 carrier protein complex reveal how specificity is achieved in the P450(BioI) ACP complex. Proc. Natl. Acad. Sci. U.S.A. 105, 15696-15701 CrossRef PubMed
11. Masoudi, A., Raetz, C. R., Zhou, P. and Pemble, IV, C. W. (2014) Chasing acyl carrier protein through a catalytic cycle of lipid A production. Nature 505, 422-426 CrossRef PubMed
12. Butland, G., Peregrin-Alvarez, J. M., Li, J., Yang, W., Yang, X., Canadien, V., Starostine, A., Richards, D., Beattie, B., Krogan, N. et al. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coIi. Nature 433, 531-537 CrossRef PubMed
13. Zhao, X., Miller, J. R., Jiang, Y., Marletta, M. A. and Cronan, J. E. (2003) Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem. Biol. 10, 1293-1302 CrossRef PubMed
14. Lin, S., Hanson, R. E. and Cronan, J. E. (2010) Biotin synthesis begins by hijacking the fatty acid synthetic pathway. Nat. Chem. Biol. 6, 682-688 CrossRef PubMed
15. Lu, P., Vogel, C., Wang, R., Yao, X. and Marcotte, E. M. (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25, 117-124 CrossRef PubMed
16. Rock, C. O. and Cronan, Jr, J. E. (1981) Acyl carrier protein from Escherichia coli. Methods Enzymol. 71, 341-351 CrossRef PubMed
17. Rock, C. O. and Cronan, Jr, J. E. (1979) Re-evaluation of the solution structure of acyl carrier protein. J. Biol. Chem. 254, 9778-9785 PubMed
18. Cronan, Jr, J. E. and Klages, A. L. (1981) Chemical synthesis of acyl thioesters of acyl carrier protein with native structure. Proc. Natl. Acad. Sci. U.S.A. 78, 5440-5444 CrossRef PubMed
19. Cronan, Jr, J. E. (1982) Molecular properties of short chain acyl thioesters of acyl carrier protein. J. Biol. Chem. 257, 5013-5017 PubMed
20. Rock, C. O., Cronan, Jr, J. E. and Armitage, I. M. (1981) Molecular properties of acyl carrier protein derivatives. J. Biol. Chem. 256, 2669-2674 PubMed
21. Holak, T. A., Kearsley, S. K., Kim, Y. and Prestegard, J. H. (1988) Three-dimensional structure of acyl carrier protein determined by NMR pseudoenergy and distance geometry calculations. Biochemistry 27, 6135-6142 CrossRef PubMed
22. Kim, Y. and Prestegard, J. H. (1989) A dynamic model for the structure of acyl carrier protein in solution. Biochemistry 28, 8792-8797 CrossRef PubMed
23. Kim, Y. and Prestegard, J. H. (1990) Refinement of the NMR structures for acyl carrier protein with scalar coupling data. Proteins 8, 377-385 CrossRef PubMed
24. Roujeinikova, A., Baldock, C., Simon, W. J., Gilroy, J., Baker, P. J., Stuitje, A. R., Rice, D. W., Slabas, A. R. and Rafferty, J. B. (2002) X-ray crystallographic studies on butyryl-ACP reveal flexibility of the structure around a putative acyl chain binding site. Structure 10, 825-835 CrossRef PubMed
25. Roujeinikova, A., Simon, W. J., Gilroy, J., Rice, D. W., Rafferty, J. B. and Slabas, A. R. (2007) Structural studies of fatty acyl-(acyl carrier protein) thioesters reveal a hydrophobic binding cavity that can expand to fit longer substrates. J. Mol. Biol. 365, 135-145 CrossRef PubMed
26. Parris, K. D., Lin, L., Tam, A., Mathew, R., Hixon, J., Stahl, M., Fritz, C. C., Seehra, J. and Somers, W. S. (2000) Crystal structures of substrate binding to Bacillus subtilis holo-(acyl carrier protein) synthase reveal a novel trimeric arrangement of molecules resulting in three active sites. Structure 8, 883-895 CrossRef PubMed
27. Qiu, X. and Janson, C. A. (2004) Structure of apo acyl carrier protein and a proposal to engineer protein crystallization through metal ions. Acta Crystallogr. D Biol. Crystallogr. 60, 1545-1554 CrossRef
28. Gally, H. U., Spencer, A. K., Armitage, I. M., Prestegard, J. H. and Cronan, Jr, J. E. (1978) Acyl carrier protein from Escherichia coli:characterization by proton and fluorine-19 nuclear magnetic resonance and evidence for restricted mobility of the fatty acid chain in tetradecanoyl-acyl- carrier protein. Biochemistry 17, 5377-5382 CrossRef PubMed
29. Kosa, N. M., Haushalter, R. W., Smith, A. R. and Burkart, M. D. (2012) Reversible labeling of native and fusion-protein motifs. Nat. Methods 9, 981-984 CrossRef PubMed
30. Ploskon, E., Arthur, C. J., Kanari, A. L., Wattana-amorn, P., Williams, C., Crosby, J., Simpson, T. J., Willis, C. L. and Crump, M. P. (2010) Recognition of intermediate functionality by acyl carrier protein over a complete cycle of fatty acid biosynthesis. Chem. Biol. 17, 776-785 CrossRef PubMed
31. Chan, D. I., Tieleman, D. P. and Vogel, H. J. (2010) Molecular dynamics simulations of β-ketoacyl-, β-hydroxyacyl-, and trans-2-enoyl-acyl carrier proteins of Escherichia coli. Biochemistry 49, 2860-2868 CrossRef PubMed
32. Upadhyay, S. K., Misra, A., Srivastava, R., Surolia, N., Surolia, A. and Sundd, M. (2009) Structural insights into the acyl intermediates of the Plasmodium falciparumfatty acid synthesis pathway: the mechanism of expansion of the acyl carrier protein core. J. Biol. Chem. 284, 22390-22400 CrossRef PubMed
33. Zornetzer, G. A., Tanem, J., Fox, B. G. and Markley, J. L. (2010) The length of the bound fatty acid influences the dynamics of the acyl carrier protein and the stability of the thioester bond. Biochemistry 49, 470-477 CrossRef PubMed
34. Rafi, S., Novichenok, P., Kolappan, S., Zhang, X., Stratton, C. F., Rawat, R., Kisker, C., Simmerling, C. and Tonge, P. J. (2006) Structure of acyl carrier protein bound to FabI, the FASII enoyl reductase from Escherichia coli. J. Biol. Chem. 281, 39285-39293 CrossRef PubMed
35. Bloch, K. (1971) β-Hydroxydecanoyl thioester dehydrase. In The Enzymes (Boyer, P. D., ed.), pp. 441-464, Academic Press, New York CrossRef
36. Feng, Y. and Cronan, J. E. (2009) Escherichia coliunsaturated fatty acid synthesis: complex transcription of the fabA gene and in vivo identification of the essential reaction catalyzed by FabB. J. Biol. Chem. 284, 29526-29535 CrossRef PubMed
37. Bloch, K. (1986) The beginnings of enzyme suicide. J. Protein. Chem. 5, 69-73 CrossRef
38. Brock, D. J., Kass, L. R. and Bloch, K. (1967) β-Hydroxydecanoyl thioester dehydrase. II. Mode of action. J. Biol. Chem. 242, 4432-4440
39. Helmkamp, Jr, G. M. and Bloch, K. (1969) β-Hydroxydecanoyl thioester dehydrase. Studies on molecular structure and active site. J. Biol. Chem. 244, 6014-6022 PubMed
40. Schwab, J. M., Ho, C. K., Li, W. B., Townsend, C. A. and Salituro, G. M. (1986) β-Hydroxydecanoyl thioester dehydrase: complete characterization of the fate of the suicide substrate 3-decynoyl-NAC. J. Am. Chem. Soc. 108, 5309-5316 CrossRef
41. Helmkamp, Jr, G. M., Rando, R. R., Brock, D. J. and Bloch, K. (1968) β-Hydroxydecanoyl thioester dehydrase. Specificity of substrates and acetylenic inhibitors. J. Biol. Chem. 243, 3229-3231 PubMed
42. Rando, R. R. and Bloch, K. (1968) Mechanism of action of β-hydroxydecanoyl thioester dehydrase. J. Biol. Chem. 243, 5627-5634 PubMed
43. Morisaki, M. and Bloch, K. (1972) On the mode of interaction of β-hydroxydecanoyl thioester dehydrase with allenic acid derivatives. Biochemistry 11, 309-314 CrossRef PubMed
44. Meier, J. L., Haushalter, R. W. and Burkart, M. D. (2010) A mechanism based protein crosslinker for acyl carrier protein dehydratases. Bioorg. Med. Chem. Lett. 20, 4936-4939 CrossRef PubMed
45. Ishikawa, F., Haushalter, R. W. and Burkart, M. D. (2012) Dehydratase-specific probes for fatty acid and polyketide synthases. J. Am. Chem. Soc. 134, 769-772 CrossRef PubMed
46. Ishikawa, F., Haushalter, R. W., Lee, D. J., Finzel, K. and Burkart, M. D. (2013) Sulfonyl 3-alkynyl pantetheinamides as mechanism-based cross-linkers of acyl carrier protein dehydratase. J. Am. Chem. Soc. 135, 8846-8849 CrossRef PubMed
47. Worthington, A. S. and Burkart, M. D. (2006) One-pot chemo-enzymatic synthesis of reporter-modified proteins. Org. Biomol. Chem. 4, 44-46 CrossRef PubMed
48. Leesong, M., Henderson, B. S., Gillig, J. R., Schwab, J. M. and Smith, J. L. (1996) Structure of a dehydratase-isomerase from the bacterial pathway for biosynthesis of unsaturated fatty acids: two catalytic activities in one active site. Structure 4, 253-264 CrossRef PubMed
49. Moynie, L., Leckie, S. M., McMahon, S. A., Duthie, F. G., Koehnke, A., Taylor, J. W., Alphey, M. S., Brenk, R., Smith, A. D. and Naismith, J. H. (2013) Structural insights into the mechanism and inhibition of the β-hydroxydecanoyl-acyl carrier protein dehydratase from Pseudomonas aeruginosa. J. Mol. Biol. 425, 365-377 CrossRef PubMed
50. Bartling, C. M. and Raetz, C. R. (2008) Steady-state kinetics and mechanism of LpxD, the N-acyltransferase of lipid A biosynthesis. Biochemistry 47, 5290-5302 CrossRef PubMed
51. Bartling, C. M. and Raetz, C. R. (2009) Crystal structure and acyl chain selectivity of Escherichia coli LpxD, the N-acyltransferase of lipid A biosynthesis. Biochemistry 48, 8672-8683 CrossRef PubMed
52. Andrec, M., Hill, R. B. and Prestegard, J. H. (1995) Amide exchange rates in Escherichia coli acyl carrier protein: correlation with protein structure and dynamics. Protein Sci. 4, 983-993 CrossRef PubMed
53. Ploskon, E., Arthur, C. J., Evans, S. E., Williams, C., Crosby, J., Simpson, T. J. and Crump, M. P. (2008) A mammalian type I fatty acid synthase acyl carrier protein domain does not sequester acyl chains. J. Biol. Chem. 283, 518-528 CrossRef PubMed
54. Cronan, J. E. and Thomas, J. (2009) Bacterial fatty acid synthesis and its relationships with polyketide synthetic pathways. Methods Enzymol. 459, 395-433 CrossRef PubMed
55. Evans, S. E., Williams, C., Arthur, C. J., Ploskon, E., Wattana-amorn, P., Cox, R. J., Crosby, J., Willis, C. L., Simpson, T. J. and Crump, M. P. (2009) Probing the Interactions of early polyketide intermediates with the Actinorhodin ACP from S. coelicolor A3(2). J. Mol. Biol. 389, 511-528 CrossRef PubMed
56. Yang, Z., Lasker, K., Schneidman-Duhovny, D., Webb, B., Huang, C. C., Pettersen, E. F., Goddard, T. D., Meng, E. C., Sali, A. and Ferrin, T. E. (2012) UCSF Chimera, MODELLER, and IMP: an integrated modeling system. J. Struct. Biol. 179, 269-278 CrossRef PubMed