Cloning, expression, and characterization of recombinant nitric oxide synthase-like protein from Bacillus anthracis

Biochemical and Biophysical Research Communications

Volumn 336, Issue 1, 2005, Pages 346-356

  Midha, Shuchi ^a   Mishra, Rajeev ^a   Aziz, Mohd Azhar ^a   Sharma, Meenakshi ^a   Mishra, Ashish ^a   Khandelwal, Puneet ^a   Bhatnagar, Rakesh ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

Bacillus anthracis; Heme substrate interaction; Nitric oxide synthase; Optical spectral perturbation

Indexed keywords

IMIDAZOLE; NITRIC OXIDE SYNTHASE;

ARTICLE; BACILLUS ANTHRACIS; CONTROLLED STUDY; ENZYME DEGRADATION; ESCHERICHIA COLI; MACROPHAGE; MOLECULAR CLONING; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BACILLUS ANTHRACIS; CLONING, MOLECULAR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NITRIC OXIDE SYNTHASE; RATS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTRUM ANALYSIS;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 24344458101     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.08.083     Document Type: Article

References (62)

1. O.W. Griffith, and D.J. Stuehr Nitric oxide synthases properties and catalytic mechanism Annu. Rev. Physiol. 57 1995 707 736
2. H.M. Abu-Soud, and D.J. Stuehr Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer Proc. Natl. Acad. Sci. USA 90 1993 10769 10772
3. H.M. Abu-Soud, R. Gachhui, F.M. Raushel, and D.J. Stuehr The ferrous-dioxy complex of neuronal nitric oxide synthase: divergent effects of l-arginine and tetrahydrobiopterin on its stability J. Biol. Chem. 272 1997 17349 17353
4. N. Bec, A.C.F. Gorren, C. Voelkar, B. Mayer, and R. Lange Reaction of neuronal nitric-oxide synthase with oxygen at low temperature J. Biol. Chem. 273 1998 13502 13508
5. D.J. Stuehr, J. Santolini, Z. Wang, C. Wei, and S. Adak Update on mechanism and catalytic regulation in the NO synthases J. Biol. Chem. 279 2004 36167 36170
6. M.A. Marletta, A.K. Hurshman, and K.M. Rusche Catalysis by nitric oxide synthase Curr. Opin. Chem. Biol. 2 1998 656 663
7. B. Hemmens, and B. Mayer M.A. Titheradge Enzymology of Nitric Oxide Synthases Methods in Molecular Biology vol. 100 1997 Humana Press Totowa, NJ 1 32
8. D.J. Stuehr, N.S. Kwon, C.F. Nathan, O.W. Griffith, P.L. Feldman, and J. Wiseman N-omega-hydroxy-l-arginine is an intermediate in the biosynthesis of nitric oxide from l-arginine J. Biol. Chem. 266 1991 6259 6263
9. P. Klatt, K. Schmidt, G. Uray, and B. Mayer Multiple catalytic functions of brain nitric oxide synthase. Biochemical characterization, cofactor-requirement, and the role of N omega-hydroxy-l-arginine as an intermediate J. Biol. Chem. 268 1993 14781 14787
10. D.J. Stuehr, and M. Ikeda-Saito Spectral characterization of brain and macrophage nitric oxide synthases. Cytochrome P-450-like hemeproteins that contain a flavin semiquinone radical J. Biol. Chem. 267 1992 20547 20550
11. G-hydroxy-l- arginine by nitric oxide synthase: evidence for the involvement of the heme in catalysis Biochem. Biophy. Res. Commun. 193 1993 963 970
12. J. Wang, D.J. Stuehr, M. Ikeda-Saito, and D.L. Rousseau Heme coordination and structure of the catalytic site in nitric oxide synthase J. Biol. Chem. 268 1993 22255 22258
13. L.J. Roman, E.A. Sheta, P. Marta Sek, S.S. Gross, W.C. Sessa, and B.S. Masters High-level expression of functional rat neuronal nitric oxide synthase in Escherichia coli Proc. Natl. Acad. Sci. USA 92 1995 8428 8432
14. W.S. Choi, M.S. Chang, J.W. Han, S.Y. Hong, and H.W. Lee Identification of nitric oxide synthase in Staphylococcus aureus Biochem. Biophy. Res. Commun. 237 1997 554 558
15. S. Adak, A.M. Bilwes, K. Panda, D. Hosfield, K.S. Aulak, J.F. McDonald, J.A. Tainer, E.D. Getzoff, B.R. Crane, and D.J. Stuehr Cloning, expression, and characterization of a nitric oxide synthase protein from Deinococcus radiodurans Proc. Natl. Acad. Sci. USA 99 2002 107 112
16. S. Adak, K.S. Aulak, and D.J. Stuehr Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis J. Biol. Chem. 277 2002 16167 16171
17. U. Muller The nitric oxide system in insects Prog. Neurobiol. 51 1997 363 381
18. D.F. Klesig, J. Durner, R. Noad, D.A. Navarre, D. Wendehenne, D. Kumar, J.M. Zhou, J. Shah, S. Zhang, and P. Kachroo Nitric oxide and salicylic acid signaling in plant defense Proc. Natl. Acad. Sci. USA 97 2000 8849 8855
19. G. Golderer, E.R. Werner, S. Leitner, P. Grobner, and G. Werner-Felmayer Nitric oxide synthase is induced in sporulation of Physarum polycephalum Genes Dev. 15 2001 1209 1299
20. H. Ninnemann, and J. Maier Indications for the occurrence of nitric oxide synthases in fungi and plants and the involvement in photoconidiation of Neurospora crassa Photochem. Photobiol. 64 1996 393 398
21. M.W. Radomski, J.F. Martin, and S. Moncada Synthesis of nitric-oxide by the hemocytes of the american horseshoe-crab (limulus-polyphemus) Philos. Trans. R. Soc. London B 334 1991 129 133
22. A.M. Friedlander Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process J. Biol. Chem. 261 1986 7123 7126
23. S.H. Leppla Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells Proc. Natl. Acad. Sci. USA 79 1982 3162 3166
24. P. Kumar, N. Ahuja, and R. Bhatnagar Purification of anthrax edema factor from Escherichia coli and identification of residues required for binding to protective antigen Infect. Immun. 69 2001 6532 6536
25. M.H. Vodkin, and S.H. Leppla Cloning of the protective antigen gene of Bacillus anthracis Cell 34 1983 693 697
26. P. Gupta, S.M. Waheed, and R. Bhatnagar Expression and purification of the recombinant protective antigen of Bacillus anthracis Prot. Exp. Pur. 16 1999 369 376
27. T. Bragg, and D.L. Robertson Nucleotide sequence and analysis of the Bacillus anthracis lethal factor gene (lef) Gene 81 1989 45 54
28. P. Gupta, S. Khetarpal, A.P. Chopra, Y. Singh, and R. Bhatnagar Expression and purification of the recombinant lethal factor of Bacillus anthracis Infect. Immun. 66 1998 862 865
29. D.L. Robertson, M.T. Tippetts, and S.H. Leppla Nucleotide sequence of the Bacillus anthracis edema factor gene (cya): a calmodulin-dependent adenylate cyclase Gene 73 1988 363 371
30. P. Kumar, N. Ahuja, and R. Bhatnagar Anthrax edema toxin requires influx of calcium for inducing cAMP toxicity in target cells Infect. Immun. 70 2002 4997 5007
31. K.A. White, and M.A. Marletta Nitric oxide synthase is a cytochrome P-450 type hemoprotein Biochemistry 31 1992 6627 6631
32. T.O. Fischmann, A. Hruza, X.D. Niu, J.D. Fossetta, C.A. Lunn, E. Dolphin, A.J. Prongay, P. Reichert, D.J. Lundell, S.K. Narula, and P.C. Weber Structural characterization of nitric oxide synthase isoforms reveals striking active-site conservation Nat. Struct. Biol. 6 1999 233 242
33. D.S. Bredt, and S.H. Synder Nitric oxide: a physiologic messenger molecule Annu. Rev. Biochem. 63 1994 175 195
34. C.S. Raman, H. Li, P. Martasek, V. Kral, B.S. Masters, and T.L. Poulos Crystal structure of constitutive endotelial nitric oxide synthase: a paradigm for pterin function involving a novel metal center Cell 95 1998 939 950
35. M.M. Bradford Rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye Anal. Biochem. 72 1967 248 254
36. J.A. Kers, M.J. Wach, S.B. Krasnoff, J. Widom, K.D. Cameron, R.A. Bukhalid, D.M. Gibson, B.R. Crane, and R. Loria Nitration of a peptide phytotoxin by bacterial nitric oxide synthase Nature 429 2004 79 82
37. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680
38. J.A. Cuff, M.E. Clamp, A.S. Siddiqui, M. Finlay, and G.J. Barton Jpred: a consensus secondary structure prediction server Bioinformatics 14 1998 892 893
39. L.A. Kelley, R.M. MacCallum, and M.J. Sternberg Enhanced genome annotation using structural profiles in the program 3D-PSSM J. Mol. Biol. 299 2000 499 520
40. A. Fiser, and A. Sali Modeller: generation and refinement of homology-based protein structure models Methods Enzymol. 374 2003 461 491
41. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Hornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26 1993 283 291
42. K. McMillan, and B.S.S. Masters Optical difference spectrophotometry as a probe of rat brain nitric oxide synthase heme-substrate interaction Biochemistry 38 1993 9875 9880
43. B.R. Crane, R.J. Rosenfeld, A.S. Arvai, D.K. Ghosh, S. Ghosh, J.A. Tainer, D.J. Stuehr, and E.D. Getzoff N-terminal domain swapping and metal ion binding in nitric oxide synthase dimerization EMBO J. 18 1999 6271 6281
44. K. McMillan, and B.S.S Masters Prokaryotic expression of the heme- and flavin-binding domains of rat neuronal nitric oxide synthase as distinct polypeptides: identification of the heme-binding proximal thiolate ligand as cysteine-415 Biochemistry 34 1995 3686 3693
45. S. Adak, Q. Wang, and D.J. Stuehr Arginine conversion to nitroxide by tetrahydrobiopterin-free neuronal nitric-oxide synthase. Implications for mechanism J. Biol. Chem. 275 2000 33554 33561
46. C. Jung, D.J. Stuehr, and D.K. Ghosh FT-infrared spectroscopic studies of the iron ligand CO stretch mode of iNOS oxygenase domain: effect of arginine and tetrahydrobiopterin Biochemistry 39 2000 10163 10171
47. H.M. Abu-Soud, C. Wu, D.K. Ghosh, and D.J. Stuehr Stopped-flow analysis of CO and NO binding to inducible nitric oxide synthase Biochemistry 37 1998 3777 3786
48. J. Wang, D.J. Stuehr, and D.L. Rousseau Tetrahydrobiopterin-deficient nitric-oxide synthase has a modified heme environment and forms a cytochrome P-420 analogue Biochemistry 34 1995 7080 7087
49. D.W. Nebert, D.R. Nelson, M.J. Coon, R.W. Estabrook, R. Feyereisen, Y. Fujii-Kuriyama, F.J. Gonzalez, F.P. Guengerich, I.C. Gunsalus, and E.F. Johnson The P450 superfamily: update on new sequences, gene mapping, and recommended nomenclature DNA Cell Biol. 10 1991 1 14
50. M. Sono, D.J. Stuehr, M. Ikeda-Saito, and J.H. Dawson Identification of nitric oxide synthase as a thiolate-ligand heme protein using magnetic circular dichroism spectroscopy: comparison with cytochrome P-450-cam and chloroperoxidase J. Biol. Chem. 270 1995 19943 19948
51. J.B. Schenkman, H. Remmer, and R.W. Estabrook Spectral studies of drug interaction with hepatic microsomal cytochrome Mol. Pharmcol. 3 1967 113 123
52. T.D. Rogerson, C.F. Wilkinson, and K. Hetarski Steric factors in the inhibitory interaction of imidazoles with microsomal enzymes Biochem. Pharmacol. 26 1977 1039 1042
53. J.B. Schenkman, S.G. Sligar, and D.L. Cinti Substrate interaction with cytochrome P-450 Pharmacol. Ther. 12 1981 43 71
54. R.A. Swanson, and K.M. Dus Specific covalent labeling of cytochrome P-450CAM with 1-(4-azidophenyl) imidazole, an inhibitor-derived photoaffinity probe for P-450 heme proteins J. Biol. Chem. 254 1979 7238 7246
55. G.A. Roberts, A. Celik, D.J.B. Hunter, T.W.B. Ost, J.H. White, S.K. Chapman, N.J. Turner, and S.L. Flitsch A self-sufficent cytochrome P450 with a primary structural organization that includes a flavin domain and a [2Fe2S] redox center J. Am. Chem. Soc. 278 2003 48914 48920
56. A.W. Munro, D.G. Leys, K.J. McLean, K.R. Marshall, T.W. Ost, S. Daff, C.S. Miles, S.K. Chapman, D.A. Lysek, C.C. Moser, C.C. Page, and P.L. Dutton P450 BM3: the very model of a modern flavocytochrome Trends Biochem. Sci. 27 2002 250 257
57. R. Bhatnagar, N. Ahuja, R. Goila, S. Khetarpal, S.M. Waheed, and P. Gupta Activation of phospholipase C and protein kinase C is required for expression of anthrax lethal toxin cytotoxicity in J774A. 1 cells Cell. Signal. 11 1999 111 118
58. R. Bhatnagar, and S. Batra Anthrax toxin Crit. Rev. Microbiol. 27 2001 167 200
59. N. Ahuja, P. Kumar, and R. Bhatnagar Adenylate cyclase toxins Crit. Rev. Microbiol. 30 2004 187 196
60. W. Siess, and E.G. Lapetina Functional relationship between cyclic AMP-dependent protein phosphorylation and platelet inhibition Biochem. J. 271 1990 815 819
61. D.H. Maurice, and R.J. Haslam Molecular basis of the synergistic inhibition of platelet function by nitrovasodilators and activators of adenylate cyclase: inhibition of cyclic AMP breakdown by cyclic GMP Mol. Pharmacol. 37 1990 671 681
62. X. Zhang, and T.H. Hintze cAMP signal transduction cascade, a novel pathway for the regulation of endothelial nitric oxide production in coronary blood vessels Arterioscl. Thromb. Vasc. Biol. 21 2001 797 803