Genome scale prediction of substrate specificity for acyl adenylate superfamily of enzymes based on active site residue profiles

BMC Bioinformatics

Volumn 11, Issue , 2010, Pages

  Khurana, Pankaj ^a,b   Gokhale, Rajesh S ^a   Mohanty, Debasisa ^a  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^b DEFENCE INSTITUTE OF PHYSIOLOGY AND ALLIED SCIENCES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE RESIDUES; COMPUTATIONAL PROTOCOLS; FUNCTIONAL ANNOTATION; FUNCTIONAL CLASSIFICATION; KNOWLEDGE-BASED APPROACH; SECONDARY METABOLITES; SUBSTRATE RECOGNITION; SUBSTRATE SPECIFICITY;

ENZYMES; FORECASTING; GENES; KNOWLEDGE BASED SYSTEMS; PLANTS (BOTANY); TIN;

SUBSTRATES;

ACETYL COENZYME A SYNTHETASE;

ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; METHODOLOGY; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION;

ACETATE-COA LIGASE; ALGORITHMS; AMINO ACID SEQUENCE; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 77949497027     PISSN: None     EISSN: 14712105     Source Type: Journal    
DOI: 10.1186/1471-2105-11-57     Document Type: Article

References (65)

1. Stuible HP, Kombrink E. Identification of the substrate specificity-conferring amino acid residues of 4-coumarate:coenzyme A ligase allows the rational design of mutant enzymes with new catalytic properties. J Biol Chem 2001, 276(29):26893-26897. 10.1074/jbc.M100355200, 11323416.
2. Trivedi OA, Arora P, Sridharan V, Tickoo R, Mohanty D, Gokhale RS. Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 2004, 428(6981):441-445. 10.1038/nature02384, 15042094.
3. Arora P, Goyal A, Natarajan VT, Rajakumara E, Verma P, Gupta R, Yousuf M, Trivedi OA, Mohanty D, Tyagi A, et al. Mechanistic and functional insights into fatty acid activation in Mycobacterium tuberculosis. Nat Chem Biol 2009, 5(3):166-173. 10.1038/nchembio.143, 2644305, 19182784.
4. Korchak HM, Kane LH, Rossi MW, Corkey BE. Long chain acyl coenzyme A and signaling in neutrophils. An inhibitor of acyl coenzyme A synthetase, triacsin C, inhibits superoxide anion generation and degranulation by human neutrophils. J Biol Chem 1994, 269(48):30281-30287.
5. Murakami K, Ide T, Nakazawa T, Okazaki T, Mochizuki T, Kadowaki T. Fatty-acyl-CoA thioesters inhibit recruitment of steroid receptor co-activator 1 to alpha and gamma isoforms of peroxisome-proliferator-activated receptors by competing with agonists. Biochem J 2001, 353(Pt2):231-238. 10.1042/0264-6021:3530231, 1221563, 11139385.
6. Gordon JI, Duronio RJ, Rudnick DA, Adams SP, Gokel GW. Protein N-myristoylation. J Biol Chem 1991, 266(14):8647-8650.
7. Li ZN, Hongo S, Sugawara K, Sugahara K, Tsuchiya E, Matsuzaki Y, Nakamura K. The sites for fatty acylation, phosphorylation and intermolecular disulphide bond formation of influenza C virus CM2 protein. J Gen Virol 2001, 82(Pt 5):1085-1093.
8. Rubenstein JL, Fine RE, Luskey BD, Rothman JE. Purification of coated vesicles by agarose gel electrophoresis. J Cell Biol 1981, 89(2):357-361. 10.1083/jcb.89.2.357, 2111692, 6265464.
9. DiRusso CC, Metzger AK, Heimert TL. Regulation of transcription of genes required for fatty acid transport and unsaturated fatty acid biosynthesis in Escherichia coli by FadR. Mol Microbiol 1993, 7(2):311-322. 10.1111/j.1365-2958.1993.tb01122.x, 8446033.
10. DiRusso CC, Heimert TL, Metzger AK. Characterization of FadR, a global transcriptional regulator of fatty acid metabolism in Escherichia coli. Interaction with the fadB promoter is prevented by long chain fatty acyl coenzyme A. J Biol Chem 1992, 267(12):8685-8691.
11. Marahiel MA, Stachelhaus T, Mootz HD. Modular Peptide Synthetases Involved in Nonribosomal Peptide Synthesis. Chem Rev 1997, 97(7):2651-2674. 10.1021/cr960029e, 11851476.
12. Hahlbrock K, Scheel D. Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 1989, 40:347-369.
13. Ferreras JA, Ryu JS, Di Lello F, Tan DS, Quadri LE. Small-molecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis. Nat Chem Biol 2005, 1(1):29-32. 10.1038/nchembio706, 16407990.
14. Contag CH, Spilman SD, Contag PR, Oshiro M, Eames B, Dennery P, Stevenson DK, Benaron DA. Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem Photobiol 1997, 66(4):523-531. 10.1111/j.1751-1097.1997.tb03184.x, 9337626.
15. Kricka LJ. Chemiluminescence and bioluminescence. Anal Chem 1995, 67(12):499R-502R. 10.1021/ac00108a035, 8686870.
16. Kricka LJ. Application of bioluminescence and chemiluminescence in biomedical sciences. Methods Enzymol 2000, 305:333-345. full_text, 10812611.
17. Fulda M, Heinz E, Wolter FP. The fadD gene of Escherichia coli K12 is located close to rnd at 39.6 min of the chromosomal map and is a new member of the AMP-binding protein family. Mol Gen Genet 1994, 242(3):241-249. 10.1007/BF00280412, 8107670.
18. Conti E, Stachelhaus T, Marahiel MA, Brick P. Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S. Embo J 1997, 16(14):4174-4183. 10.1093/emboj/16.14.4174, 1170043, 9250661.
19. May JJ, Kessler N, Marahiel MA, Stubbs MT. Crystal structure of DhbE, an archetype for aryl acid activating domains of modular nonribosomal peptide synthetases. Proc Natl Acad Sci USA 2002, 99(19):12120-12125. 10.1073/pnas.182156699, 129408, 12221282.
20. Conti E, Franks NP, Brick P. Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 1996, 4(3):287-298. 10.1016/S0969-2126(96)00033-0, 8805533.
21. Franks NP, Jenkins A, Conti E, Lieb WR, Brick P. Structural basis for the inhibition of firefly luciferase by a general anesthetic. Biophys J 1998, 75(5):2205-2211. 10.1016/S0006-3495(98)77664-7, 1299894, 9788915.
22. Gulick AM, Starai VJ, Horswill AR, Homick KM, Escalante-Semerena JC. The 1.75 A crystal structure of acetyl-CoA synthetase bound to adenosine-5'-propylphosphate and coenzyme A. Biochemistry 2003, 42(10):2866-2873. 10.1021/bi0271603, 12627952.
23. Jogl G, Tong L. Crystal structure of yeast acetyl-coenzyme A synthetase in complex with AMP. Biochemistry 2004, 43(6):1425-1431. 10.1021/bi035911a, 14769018.
24. Hisanaga Y, Ago H, Nakagawa N, Hamada K, Ida K, Yamamoto M, Hori T, Arii Y, Sugahara M, Kuramitsu S. Structural basis of the substrate-specific two-step catalysis of long chain fatty acyl-CoA synthetase dimer. J Biol Chem 2004, 279(30):31717-31726. 10.1074/jbc.M400100200, 15145952.
25. Gulick AM, Lu X, Dunaway-Mariano D. Crystal structure of 4-chlorobenzoate:CoA ligase/synthetase in the unliganded and aryl substrate-bound states. Biochemistry 2004, 43(27):8670-8679. 10.1021/bi049384m, 15236575.
26. Reger AS, Wu R, Dunaway-Mariano D, Gulick AM. Structural characterization of a 140 degrees domain movement in the two-step reaction catalyzed by 4-chlorobenzoate:CoA ligase. Biochemistry 2008, 47(31):8016-8025. 10.1021/bi800696y, 2666193, 18620418.
27. Nakatsu T, Ichiyama S, Hiratake J, Saldanha A, Kobashi N, Sakata K, Kato H. Structural basis for the spectral difference in luciferase bioluminescence. Nature 2006, 440(7082):372-376. 10.1038/nature04542, 16541080.
28. Tanovic A, Samel SA, Essen LO, Marahiel MA. Crystal structure of the termination module of a nonribosomal peptide synthetase. Science 2008, 321(5889):659-663. 10.1126/science.1159850, 18583577.
29. Du L, He Y, Luo Y. Crystal structure and enantiomer selection by D-alanyl carrier protein ligase DltA from Bacillus cereus. Biochemistry 2008, 47(44):11473-11480. 10.1021/bi801363b, 18847223.
30. Bains J, Boulanger MJ. Biochemical and structural characterization of the paralogous benzoate CoA ligases from Burkholderia xenovorans LB400: defining the entry point into the novel benzoate oxidation (box) pathway. J Mol Biol 2007, 373(4):965-977. 10.1016/j.jmb.2007.08.008, 17884091.
31. Challis GL, Ravel J, Townsend CA. Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem Biol 2000, 7(3):211-224. 10.1016/S1074-5521(00)00091-0, 10712928.
32. Stachelhaus T, Mootz HD, Marahiel MA. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol 1999, 6(8):493-505. 10.1016/S1074-5521(99)80082-9, 10421756.
33. von Dohren H, Dieckmann R, Pavela-Vrancic M. The nonribosomal code. Chem Biol 1999, 6(10):R273-279. 10.1016/S1074-5521(00)80014-9, 10508683.
34. Ansari MZ, Yadav G, Gokhale RS, Mohanty D. NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res 2004, (32 Web Server):W405-413. 10.1093/nar/gkh359, 441497, 15215420.
35. Stuible H, Buttner D, Ehlting J, Hahlbrock K, Kombrink E. Mutational analysis of 4-coumarate:CoA ligase identifies functionally important amino acids and verifies its close relationship to other adenylate-forming enzymes. FEBS Lett 2000, 467(1):117-122. 10.1016/S0014-5793(00)01133-9, 10664468.
36. Ehlting J, Shin JJ, Douglas CJ. Identification of 4-coumarate:coenzyme A ligase (4CL) substrate recognition domains. Plant J 2001, 27(5):455-465. 10.1046/j.1365-313X.2001.01122.x, 11576429.
37. Schneider K, Hovel K, Witzel K, Hamberger B, Schomburg D, Kombrink E, Stuible HP. The substrate specificity-determining amino acid code of 4-coumarate:CoA ligase. Proc Natl Acad Sci USA 2003, 100(14):8601-8606. 10.1073/pnas.1430550100, 166275, 12819348.
38. Lindermayr C, Fliegmann J, Ebel J. Deletion of a single amino acid residue from different 4-coumarate:CoA ligases from soybean results in the generation of new substrate specificities. J Biol Chem 2003, 278(5):2781-2786. 10.1074/jbc.M202632200, 12421821.
39. Branchini BR, Magyar RA, Murtiashaw MH, Anderson SM, Zimmer M. Site-directed mutagenesis of histidine 245 in firefly luciferase: a proposed model of the active site. Biochemistry 1998, 37(44):15311-15319. 10.1021/bi981150d, 9799491.
40. Branchini BR, Southworth TL, Murtiashaw MH, Boije H, Fleet SE. A mutagenesis study of the putative luciferin binding site residues of firefly luciferase. Biochemistry 2003, 42(35):10429-10436. 10.1021/bi030099x, 12950169.
41. Sandalova TP, Ugarova NN. Model of the active site of firefly luciferase. Biochemistry (Mosc) 1999, 64(8):962-967.
42. Oba Y, Ojika M, Inouye S. Characterization of CG6178 gene product with high sequence similarity to firefly luciferase in Drosophila melanogaster. Gene 2004, 329:137-145. 10.1016/j.gene.2003.12.026, 15033536.
43. Oba Y, Sato M, Ojika M, Inouye S. Enzymatic and genetic characterization of firefly luciferase and Drosophila CG6178 as a fatty acyl-CoA synthetase. Biosci Biotechnol Biochem 2005, 69(4):819-828. 10.1271/bbb.69.819, 15849423.
44. Schneider K, Kienow L, Schmelzer E, Colby T, Bartsch M, Miersch O, Wasternack C, Kombrink E, Stuible HP. A new type of peroxisomal acyl-coenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. J Biol Chem 2005, 280(14):13962-13972. 10.1074/jbc.M413578200, 15677481.
45. de Azevedo Souza C, Kim SS, Koch S, Kienow L, Schneider K, McKim SM, Haughn GW, Kombrink E, Douglas CJ. A novel fatty Acyl-CoA Synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell 2009, 21(2):507-525. 10.1105/tpc.108.062513, 2660628, 19218397.
46. Souza Cde A, Barbazuk B, Ralph SG, Bohlmann J, Hamberger B, Douglas CJ. Genome-wide analysis of a land plant-specific acyl:coenzyme A synthetase (ACS) gene family in Arabidopsis, poplar, rice and Physcomitrella. New Phytol 2008, 179(4):987-1003.
47. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
48. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. GenBank: update. Nucleic Acids Res 2004, (32 Database):D23-26. 10.1093/nar/gkh045, 308779, 14681350.
49. Eddy SR. Profile hidden Markov models. Bioinformatics 1998, 14(9):755-763. 10.1093/bioinformatics/14.9.755, 9918945.
50. Lichtarge O, Bourne HR, Cohen FE. An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol 1996, 257(2):342-358. 10.1006/jmbi.1996.0167, 8609628.
51. Oba Y, Ojika M, Inouye S. Firefly luciferase is a bifunctional enzyme: ATP-dependent monooxygenase and a long chain fatty acyl-CoA synthetase. FEBS Lett 2003, 540(1-3):251-254. 10.1016/S0014-5793(03)00272-2, 12681517.
52. Ingram-Smith C, Woods BI, Smith KS. Characterization of the acyl substrate binding pocket of acetyl-CoA synthetase. Biochemistry 2006, 45(38):11482-11490. 10.1021/bi061023e, 16981708.
53. Branchini BR, Murtiashaw MH, Magyar RA, Anderson SM. The role of lysine 529, a conserved residue of the acyl-adenylate-forming enzyme superfamily, in firefly luciferase. Biochemistry 2000, 39(18):5433-5440. 10.1021/bi9928804, 10820015.
54. Branchini BR, Magyar RA, Murtiashaw MH, Anderson SM, Helgerson LC, Zimmer M. Site-directed mutagenesis of firefly luciferase active site amino acids: a proposed model for bioluminescence color. Biochemistry 1999, 38(40):13223-13230. 10.1021/bi991181o, 10529195.
55. An JH, Lee GY, Jung JW, Lee W, Kim YS. Identification of residues essential for a two-step |reaction by malonyl-CoA synthetase from Rhizobium trifolii. Biochem J 1999, 344(Pt 1):159-166. 10.1042/0264-6021:3440159, 1220626, 10548546.
56. Jung JW, An JH, Na KB, Kim YS, Lee W. The active site and substrates binding mode of malonyl-CoA synthetase determined by transferred nuclear Overhauser effect spectroscopy, site-directed mutagenesis, and comparative modeling studies. Protein Sci 2000, 9(7):1294-1303. 10.1110/ps.9.7.1294, 2144687, 10933494.
57. Jones DT. GenTHREADER: an efficient and reliable protein fold recognition method for genomic sequences. J Mol Biol 1999, 287(4):797-815. 10.1006/jmbi.1999.2583, 10191147.
58. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 1993, 234(3):779-815. 10.1006/jmbi.1993.1626, 8254673.
59. Choudhury D. Functional Implications of Macromolecular Recognition: Assembly of Adhesive Pili and enzyme substrate interactions. Ph.D. Thesis. 2001, Uppsala: Swedish University of Agricultural Sciences, Uppsala.
60. Ehlting J, Buttner D, Wang Q, Douglas CJ, Somssich IE, Kombrink E. Three 4-coumarate:coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J 1999, 19(1):9-20. 10.1046/j.1365-313X.1999.00491.x, 10417722.
61. Branchini BR, Magyar RA, Murtiashaw MH, Portier NC. The role of active site residue arginine 218 in firefly luciferase bioluminescence. Biochemistry 2001, 40(8):2410-2418. 10.1021/bi002246m, 11327861.
62. Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000, 16(6):276-277. 10.1016/S0168-9525(00)02024-2, 10827456.
63. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
64. Thompson JD, Higgins DG, Gibson TJ. improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22(22):4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
65. Garrett M, Morris DSG, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. Journal of Computational Chemistry 1998, 19(14):1639-1662.