Chasing acyl carrier protein through a catalytic cycle of lipid A production

Nature

Volumn 505, Issue 7483, 2014, Pages 422-426

  Masoudi, Ali ^a   Raetz, Christian R H ^a   Zhou, Pei ^a   Pemble IV, Charles W ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CARRIER PROTEIN; LIPID A; LIPOPOLYSACCHARIDE; PANTETHEINE PHOSPHATE;

CATALYSIS; CELL ORGANELLE; COLIFORM BACTERIUM; HYDROCARBON; IMMUNE SYSTEM; LIPID; METABOLISM; MOBILITY; POLYSACCHARIDE; PROTEIN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; IMMUNE SYSTEM; LIPOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REACTION ANALYSIS; STATIC ELECTRICITY;

ACYL CARRIER PROTEIN; ACYLTRANSFERASES; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; HYDROLYSIS; LIPID A; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION;

ESCHERICHIA COLI; MAMMALIA; NEGIBACTERIA;

EID: 84892604605     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12679     Document Type: Article

References (42)

1. Butland, G. et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433, 531-537 (2005)
2. Byers, D. M. & Gong, H. Acyl carrier protein: structure-function relationships in a conservedmultifunctional protein family. Biochem. Cell Biol. 85, 649-662 (2007)
3. White, S. W., Zheng, J., Zhang, Y. M. & Rock. The structural biology of type II fatty acid biosynthesis. Annu. Rev. Biochem. 74, 791-831 (2005)
4. Galloway, S. M. & Raetz, C. R. H. A mutant of Escherichia coli defective in the first step of endotoxin biosynthesis. J. Biol. Chem. 265, 6394-6402 (1990)
5. Belunis, C. J., Clementz, T., Carty, S. M. & Raetz, C. R. H. Inhibition of lipopolysaccharide biosynthesis and cell growth following inactivation of the kdtA gene in Escherichia coli. J. Biol. Chem. 270, 27646-27652 (1995)
6. Poltorak, A. et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088 (1998)
7. Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783-801 (2006)
8. Onishi, H. R. et al.Antibacterial agents that inhibit lipidAbiosynthesis. Science274, 980-982 (1996)
9. Williams, A. H., Immormino, R. M., Gewirth, D. T. & Raetz, C. R. H. Structure of UDPN- acetylglucosamine acyltransferase with a bound antibacterial pentadecapeptide. Proc. Natl Acad. Sci. USA 103, 10877-10882 (2006)
10. Jenkins, R. J. & Dotson, G. D. Dual targeting antibacterial peptide inhibitor of early lipid A biosynthesis. ACS Chem. Biol. 7, 1170-1177 (2012)
11. Raetz, C. R. H., Reynolds, C. M., Trent, M. S. & Bishop, R. E. Lipid A modification systems in Gram-negative bacteria. Annu. Rev. Biochem. 76, 295-329 (2007)
12. Bartling, C. M. & Raetz, C. R. H. Steady-state kinetics and mechanismof LpxD, the N-acyltransferase of lipid A biosynthesis. Biochemistry 47, 5290-5302 (2008)
13. Leibundgut,M., Jenni,S., Frick, C. & Ban, N.Structural basis for substrate delivery by acyl carrier protein in the yeast fatty acid synthase. Science 316, 288-290 (2007)
14. Nooren, I. M.&Thornton, J. M. Diversity of protein-protein interactions.EMBOJ. 22, 3486-3492 (2003)
15. Chan, D. I. & Vogel, H. J. Current understanding of fatty acid biosynthesis and the acyl carrier protein. Biochem. J. 430, 1-19 (2010)
16. Ploskon, E. et al. Recognition of intermediate functionality by acyl carrier protein over a complete cycle of fatty acid biosynthesis. Chem. Biol. 17, 776-785 (2010)
17. Roujeinikova, A. et al. 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 (2007)
18. Buetow, L.,Smith, T. K., Dawson, A., Fyffe, S.&Hunter, W. N. Structure and reactivity of LpxD, theN-acyltransferase of lipidA biosynthesis. Proc.Natl Acad. Sci.USA 104, 4321-4326 (2007)
19. Bartling, C. M. & Raetz, C. R. H. Crystal structure and acyl chain selectivity of Escherichia coli LpxD, the N-acyltransferase of lipid A biosynthesis. Biochemistry 48, 8672-8683 (2009)
20. Raetz, C. R. H.&Roderick, S. L.Aleft-handedparallel b helix in the structure ofUDPN- acetylglucosamine acyltransferase. Science 270, 997-1000 (1995)
21. Frederick, A. F., Kay, L. E. & Prestegard, J. H. Location of divalent ion sites in acyl carrier protein using relaxation perturbed 2DNMR. FEBS Lett. 238, 43-48 (1988)
22. Cryle, M. J.&Schlichting, I. Structural insights froma P450carrier protein complex reveal how specificity is achieved in the P450(BioI) ACP complex. Proc. Natl Acad. Sci. USA 105, 15696-15701 (2008)
23. Parris, K. D. et al. 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 (2000)
24. Kraut, D. A., Carroll, K. S. & Herschlag, D. Challenges in enzyme mechanism and energetics. Annu. Rev. Biochem. 72, 517-571 (2003)
25. Kelly, T. M., Stachula, S. A.,Raetz, C. R.&Anderson, M.S. ThefirA gene of Escherichia coli encodes UDP-3-O-(R-3-hydroxymyristoyl)-glucosamine N-acyltransferase. The third step ofendotoxinbiosynthesis. J. Biol.Chem.268,19866-19874(1993)
26. Agarwal, V., Lin, S., Lukk, T., Nair, S. K. & Cronan, J. E. Structure of the enzyme-acyl carrier protein (ACP) substrate gatekeeper complex required for biotin synthesis. Proc. Natl Acad. Sci. USA 109, 17406-17411 (2012)
27. Babu, M. et al. Structure of a SLC26 anion transporter STAS domain in complex with acyl carrier protein: implications for E. coli YchM in fatty acid metabolism. Structure 18, 1450-1462 (2010)
28. Holak, T. A., Nilges, M., Prestegard, J. H., Gronenborn, A. M. & Clore, G. M. Threedimensional structure of acyl carrier protein in solution determined by nuclear magnetic resonance andthe combined use of dynamical simulated annealing and distance geometry. Eur. J. Biochem. 175, 9-15 (1988)
29. Roujeinikova, A. et al. X-ray crystallographic studies on butyryl-ACP reveal flexibility of the structure around a putative acyl chain binding site. Structure 10, 825-835 (2002)
30. Jiang, Y.,Chan, C. H.&Cronan, J. E. The soluble acyl-acyl carrier protein synthetase of Vibrio harveyi B392 is a member of the medium chain acyl-CoA synthetase family. Biochemistry 45, 10008-10019 (2006)
31. Rock, C. O., Cronan, J. E. Jr & Armitage, I. M. Molecular properties of acyl carrier protein derivatives. J. Biol. Chem. 256, 2669-2674 (1981)
32. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997)
33. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010)
34. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007)
35. Qiu, X. & Janson, C. A. Structure of apo acyl carrier protein and a proposal to engineer protein crystallization through metal ions. Acta Crystallogr. D 60, 1545-1554 (2004)
36. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004)
37. Schuttelkopf, A. W. & van Aalten, D. M. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D 60, 1355-1363 (2004)
38. Brunger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998)
39. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235-242 (2011)
40. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010)
41. DeLano, W. L. The PyMOL Molecular Graphics Systemv. 1.3r1 (Schrödinger, LLC, New York, New York, 2012)
42. Stokes, G. B. & Stumpf, P. K. Fat metabolism in higher plants. The nonenzymatic acylation of dithiothreitol by acyl coenzyme A. Arch. Biochem. Biophys. 162, 638-648 (1974).