The three-dimensional crystal structure of the PrpF protein of Shewanella oneidensis complexed with trans-aconitate: Insights into its biological function

Protein Science

Volumn 16, Issue 7, 2007, Pages 1274-1284

  Garvey, Graeme S ^a   Rocco, Christopher J ^a   Escalante Semerena, Jorge C ^a   Rayment, Ivan ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

2 methylaconitate isomerase; 2 methylcitrate dehydratase; 2 methylcitric acid cycle; Aconitase; cis trans isomerases; Non PLP dependent isomerases protein fold; Propionate catabolism; Shewanella physiology

Indexed keywords

ACONITIC ACID; DIAMINOPIMELIC ACID; EPIMERASE; ISOMERASE; PROTEIN DERIVATIVE; PROTEIN PRPF; PROTON; RACEMASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BIOLOGICAL TRAIT; BRUCELLA MELITENSIS; CATALYSIS; CIS TRANS ISOMERISM; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; HAEMOPHILUS INFLUENZAE; IN VITRO STUDY; ISOMER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; SHEWANELLA ONEIDENSIS; STEREOCHEMISTRY; THREE DIMENSIONAL IMAGING;

ACONITATE HYDRATASE; ACONITIC ACID; BACTERIAL PROTEINS; CITRATES; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HYDRO-LYASES; ISOMERISM; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SHEWANELLA;

BACTERIA (MICROORGANISMS); BRUCELLA MELITENSIS; HAEMOPHILUS INFLUENZAE; PSEUDOMONAS AERUGINOSA; SHEWANELLA; SHEWANELLA ONEIDENSIS;

EID: 34250859670     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.072801907     Document Type: Article

References (43)

1. Alhapel, A., Darley, D.J., Wagener, N., Eckel, E., Elsner, N., and Pierik, A.J. 2006. Molecular and functional analysis of nicotinate catabolism in Eubacterium barkeri. Proc. Natl. Acad. Sci. 103: 12341-12346.
2. Atlas, R. 1995. Handbook of media for environmental microbiology. CRC Press, Boca Raton, FL.
3. 12-dependent 2-methyleneglutarate mutase from Clostridium barkeri in Escherichia coli. Eur. J. Biochem. 221: 101-109.
4. Bertani, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62: 293-300.
5. Bertani, G. 2004. Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J. Bacteriol. 186: 595-600.
6. Blankenfeldt, W., Kuzin, A.P., Skarina, T., Korniyenko, Y., Tong, L., Bayer, P., Janning, P., Thomashow, L.S., and Mavrodi, D.V. 2004. Structure and function of the phenazine biosynthetic protein PhzF from Pseudomonas fluorescens. Proc. Natl. Acad. Sci. 101: 16431-16436.
7. Bramer, C.O. and Steinbuchel, A. 2001. The methylcitric acid pathway in Ralstonia eutropha: New genes identified involved in propionate metabolism. Microbiology 147: 2203-2214.
8. Bramer, C.O., Silva, L.F., Gomez, J.G., Priefert, H., and Steinbuchel, A. 2002. Identification of the 2-methylcitrate pathway involved in the catabolism of propionate in the polyhydroxyalkanoate-producing strain Burkholderia sacchari IPT101(T) and analysis of a mutant accumulating a copolyester with higher 3-hydroxyvalerate content. Appl. Environ. Microbiol. 68: 271-279.
9. Buckel, W. 1999. Anaerobic energy metabolism. In Biology of the procaryotes (eds. J.W. Lengler, G. Drews, and H.G. Chlegel), pp. 278-326. Thieme, Stuttgart, Germany.
10. Cirilli, M., Zheng, R., Scapin, G., and Blanchard, J.S. 1998. Structural symmetry: The three-dimensional structure of Haemophilus influenzae diaminopimelate epimerase. Biochemistry 37: 16452-16458.
11. Claes, W.A., Puhler, A., and Kalinowski, J. 2002. Identification of two prpDBC gene clusters in Corynebacterium glutamicum and their involvement in propionate degradation via the 2-methylcitrate cycle. J. Bacteriol. 184: 2728-2739.
12. Cohen, G.H. 1997. ALIGN: A program to superimpose protein coordinates, accounting for insertions and deletions. J. Appl. Crystallogr. 30: 1160-1161.
13. Cummings, J.H. 1995. Short chain fatty acids. In Human colonic bacteria: Role in nutrition, physiology and pathology (ed. G. Gibson and G. Macfarlane), pp. 101-105. CRC Press, London.
14. Cummings, J.H., Pomare, E.W., Branch, W.J., Naylor, C.P., and Macfarlane, G.T. 1987. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28: 1221-1227.
15. DeLano, W.L. 2002. The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA.
16. Emsley, P. and Cowtan, K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132.
17. Grassick, A., Sulzenbacher, G., Roig-Zamboni, V., Campanacci, V., Cambillau, C., and Bourne, Y. 2004. Crystal structure of E. coli yddE protein reveals a striking homology with diaminopimelate epimerase. Proteins 55: 764-767.
18. Grimek, T.L. and Escalante-Semerena, J.C. 2004. The acnD genes of Shewenella oneidensis and Vibrio cholerae encode a new Fe/S-dependent 2-methylcitrate dehydratase enzyme that requires prpF function in vivo. J. Bacteriol. 186: 454-462.
19. Horswill, A.R. and Escalante-Semerena, J.C. 1997. Propionate catabolism in Salmonella typhimurium LT2: Two divergently transcribed units comprise the prp locus at 8.5 centisomes, prpR encodes a member of the sigma-54 family of activators, and the prpBCDE genes constitute an operon. J. Bacteriol. 179: 928-940.
20. Horswill, A.R. and Escalante-Semerena, J.C. 2001. In vitro conversion of propionate to pyruvate by Salmonella enterica enzymes: 2-Methylcitrate dehydratase (PrpD) and aconitase enzymes catalyze the conversion of 2-methylcitrate to 2-methylisocitrate. Biochemistry 40: 4703-4713.
21. Horswill, A.R., Dudding, A.R., and Escalante-Semerena, J.C. 2001. Studies of propionate toxicity in Salmonella enterica identify 2-methylcitrate as a potent inhibitor of cell growth. J. Biol. Chem. 276: 19094-19101.
22. Kissinger, C.R., Gehlhaar, D.K., and Fogel, D.B. 1999. Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. D Biol. Crystallogr. 55: 484-491.
23. Klinman, J.P. and Rose, I.A. 1971a. Mechanism of the aconitate isomerase reaction. Biochemistry 10: 2259-2266.
24. Klinman, J.P. and Rose, I.A. 1971b. Purification and kinetic properties of aconitate isomerase from Pseudomonas putida. Biochemistry 10: 2253-2259.
25. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
26. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
27. Lassmann, T. and Sonnhammer, E.L. 2005. Kalign - An accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics doi: 10.1186/1471-2105-6-298.
28. Ma, Z., Gong, S., Richard, H., Tucker, D.L., Conway, T., and Foster, J.W. 2003. GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol. Microbiol. 49: 1309-1320.
29. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53: 240-255.
30. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
31. Pillai, B., Cherney, M.M., Diaper, C.M., Sutherland, A., Blanchard, J.S., Vederas, J.C., and James, M.N. 2006. Structural insights into stereochemical inversion by diaminopimelate epimerase: An antibacterial drug target. Proc. Natl. Acad. Sci. 103: 8668-8673.
32. Richard, J.P., Williams, G., O'Donoghue, A.C., and Amyes, T.L. 2002. Formation and stability of enolates of acetamide and acetate anion: An Eigen plot for proton transfer at alpha-carbonyl carbon. J. Am. Chem. Soc. 124: 2957-2968.
33. Roe, A.J., McLaggan, D., Davidson, I., O'Byrne, C., and Booth, I.R. 1998. Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. J. Bacteriol. 180: 767-772.
34. Roe, A.J., O'Byrne, C., McLaggan, D., and Booth, I.R. 2002. Inhibition of Escherichia coli growth by acetic acid: A problem with methionine biosynthesis and homocysteine toxicity. Microbiol. 148: 2215-2222.
35. Russell, R.J., Gerike, U., Danson, M.J., Hough, D.W., and Taylor, G.L. 1998. Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6: 351-361.
36. Sasse, J. 1991. Detection of proteins. In Current protocols in molecular biology. (eds. F.A. Ausubel et al.,) pp. 10.16.11-10.16.18. Wiley Interscience, New York.
37. Shih, Y.P., Wu, H.C., Hu, S.M., Wang, T.F., and Wang, A.H. 2005. Self-cleavage of fusion protein in vivo using TEV protease to yield native protein. Protein Sci. 14: 936-941.
38. Tabuchi, T. and Hara, S. 1974. Production of 2-methylisocitric acid from N-paraffins by mutants of candida-lipolytica. Agric. Biol. Chem. 38: 1105-1106.
39. Terwilliger, T.C. 2000. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56: 965-972.
40. Terwilliger, T.C. and Berendzen, J. 1999. Automated MAD and MIR structure solution. Acta Crystallogr. D55: 849-861.
41. Textor, S., Wendisch, V.F., DeGraaf, A., Muller, U., Linder, M.I., Linder, D., and Buckel, W. 1997. Propionate oxidation in Escherichia coli: Evidence for operation of a methylcitrate cycle in bacteria. Arch. Microbiol. 168: 428-436.
42. Wallace, A.C., Laskowski, R.A., and Thornton, J.M. 1995. LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8: 127-134.
43. Wolfe, A.J. 2005. The acetate switch. Microbiol. Mol. Biol. Rev. 69: 12-50.