Dissociation and unfolding of inducible nitric oxide synthase oxygenase domain identifies structural role of tetrahydrobiopterin in modulating the heme environment

Molecular and Cellular Biochemistry

Volumn 284, Issue 1-2, 2006, Pages 117-126

  Sengupta, Rajib ^a   Sahoo, Rupam ^a   Ray, Sougata Sinha ^a   Dutta, Tanmay ^a   Dasgupta, Anjan ^a   Ghosh, Sanjay ^a  

^a UNIVERSITY OF CALCUTTA   (India)

Author keywords

Dynamic light scattering; Heme retention capacity; Inducible nitric oxide synthase; Oxygenase domain; Tetrahydrobiopterin; Transverse urea gradient gel electrophoresis

Indexed keywords

HEME; INDUCIBLE NITRIC OXIDE SYNTHASE; TETRAHYDROBIOPTERIN; 5,6,7,8-TETRAHYDROBIOPTERIN; BIOPTERIN; DRUG DERIVATIVE; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; RECOMBINANT PROTEIN; UREA;

ARTICLE; CONFORMATIONAL TRANSITION; DISSOCIATION; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME REGULATION; ENZYME STRUCTURE; GEL ELECTROPHORESIS; GEL FILTRATION; GENE EXPRESSION SYSTEM; INCUBATION TIME; LIGHT SCATTERING; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; ANIMAL; BIOSYNTHESIS; CHEMISTRY; ESCHERICHIA COLI; GENETICS; LIGHT; METABOLISM; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; RADIATION SCATTERING; ULTRAVIOLET SPECTROPHOTOMETRY;

ANIMALS; BIOPTERIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; HEME; INDICATORS AND REAGENTS; LIGHT; MICE; NITRIC OXIDE SYNTHASE TYPE II; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SCATTERING, RADIATION; SPECTROPHOTOMETRY, ULTRAVIOLET; UREA;

EID: 33745882369     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-005-9027-0     Document Type: Article

References (52)

1. Ignarro LJ, (ed.): Nitric oxide, Biology and Pathobiology. Aademic Press, San Diego, 2000
2. FurchgotA RF: Nitric oxide: a unique endogenous signaling molecule in vascular biology. Biosci Rep 19: 235-251, 1999
3. Nathan CJ: Inducible nitricWoxide synthase: what difference does it make. J Clin Invest 100: 2417-2423, 1997
4. Michel T, Feron OJW Nitric oxide synthases: which, where, how and why. J Clin Invest 100: 2146-2152, 1997
5. PfeifferCS, Mayer B, Hemmens B: Nitric oxide: chemical puzzles posed by a biological messenger. Angew Chem Int Ed Engl 38: 1715-1731, 1999
6. Griffith OW, StuehP DJ: Nitric oxide synthases: properties and catalytic mechanism. Annu Rev Physiol 57: 707-736, 1995
7. Marletta MA, Hurshman AR, Rusch KM: Catalysis by nitric oxide synthase. Curr Opin Chem Biol 2: 656-663, 1997
8. Roman LJ, Martasek P, Masters BS: Intrinsic and extrinsic modulation of nitric oxide synthase activity. Chem Rev 102: 1179-1190, 2002
9. Ghosh S, Gachhui R, Crooks C, Wu C, Lisanti MP, Stuehr DJ: Interaction between Caveolin-1 and the reductase domain of endothelial nitric-oxide synthase. J Biol Chem 273: 22267-22271, 1998
10. Stuehr DJ, Ikeda-Saito M: Spectral characterization of brain and macrophage nitric oxide synthases. Cytochrome P-450-like heme-proteins that contain a flavin semiquinone radical. J Biol Chem 267: 20547-20550, 1992
11. Ghosh S, Wolan D, Adak S, Crane BR, Kwon NS, Tainer JA, Getzoff ED, Stuehr DJ: Mutational analysis of the tetrahydrobiopterin binding site in inducible nitric oxide synthase. J Biol Chem 274: 24100-24112, 1999
12. Crane BR, Arvai AS, Ghosh DK, Wu C, Getzoff ED, Stuehr DJ, Tainer JA: Structure of nitric oxide synthase oxygenase dimer with pterin and substrate. Science 279: 2121-2126, 1998
13. Ghosh DK, Abu-Soud HM, Stuehr DJ: Domains of macrophage NO synthase have divergent roles in forming and stabilizing the active dimeric enzyme. Biochemistry 35: 1444-1449, 1996
14. Craig DH, Chapman SK, Daff S: Calmodulin activates electron transfer through neuronal nitric-oxide synthase reductase domain by releasing an NADPH-dependent conformational lock. J Biol Chem 277: 33987-33994, 2002
15. Cho HJ, Martin E, Xie Q, Sassa S, Nathan C: Inducible nitric oxide synthase: Identification of amino acid residues essential for dimerization and binding of tetrahydrobiopterin. Proc Natl Acad Sci U S A 92: 11514-11518, 1995
16. Crane BR, Arvai AS, Gachhui R, Wu C, Ghosh DK, Getzoff ED, Stuehr DJ, Tainer JA: The structure of nitric oxide synthase oxygenase domain and inhibitor complexes. Science 278: 425-431, 1997
17. Raman CS, Li H, Martasek P, Kral V, Masters BS, Poulos TL: Crystal structure of constitutive endothelial nitric oxide synthase: A paradigm for pterin function involving a novel metal center. Cell 95: 939-950, 1998
18. Fischmann TO, Hruza A, Niu XD, Fossetta JD, Lunn CA, Dolphin E, Prongay AJ, Reichert P, Lundell DJ, Narula SK, Weber PC: Structural characterization of nitric oxide synthase isoforms reveals sriking active-site conservation. Nat Struct Biol 6: 233-242, 1999
19. Rodriguez-Crespo I, Gerber NC, Ortiz de Montellano PR: Endothelial nitric-oxide synthase. Expression in Escherichia coli, spectroscopic characterization, and role of tetrahydrobiopterin in dimer formation. J Biol Chem 271: 11462-11467, 1996
20. Rodriguez-Crespo I, Moenne-Loccoz P, Loehr TM, Ortiz de Montellano PR: Endothelial nitric oxide synthase: Modulations of the distal heme site produced by progressive N-terminal deletions. Biochemistry 36: 8530-8538, 1997
21. Caroll LJ, Xu Y, Thrall SH, Martin BM, Dunaway-Mariano D: Substrate binding domains in pyruvate phosphate dikinase. Biochemistry 33: 1134-1142, 1994
22. Stuehr DJ: Structure-function aspect in the nitric oxide synthases. Annu Rev pharmacol Toxicol 37: 339-359, 1997
23. Stuehr DJ: Mammalian nitric oxide synthases. Biochim Biophys Acta Bioenerg 1411: 217-230, 1999
24. Chen PF, Tsai AL, Berka V, Wu KK: Endothelial nitric-oxide synthase. Evidence for bidomain structure and successful reconstitution of catalytic activity from two separate domains generated by a baculovirus expression system. J Biol Chem 271: 14631-14635, 1996
25. Ghosh DK, Wu C, Pitters E, Moloney M, Werner ER, Meyer B, Stuehr DJ: Characterization of the inducible nitric oxide synthase oxygenase domain identifies a 49 amino acid segment required for subunit dimerization and tetrahydrobiopterin interaction. Biochemistry 36: 10609-10619, 1997
26. Abu-Soud HM, Loftus M, Stuehr DJ: Subunit dissociation and unfolding of macrophage NO synthase: Relationship between enzyme structure, prosthetic group binding, and catalytic function. Biochemistry 34(1995): 11167-11175, 1995
27. Hemmens B, Goessler W, Schimidt K, Mayer B: Role of bound zinc in dimer stabilization but not enzyme activity of neuronal nitric-oxide synthase. J Biol Chem 275: 35786-35791, 2000
28. Venema RC, Ju H, Zou R, Ryan JW, Venema VJ: Subunit interactions of endothelial nitric-oxide synthase. Comparisons to the neuronal and inducible nitric-oxide synthase isoforms, J Biol Chem 272: 1276-1282, 1997
29. Panda K, Rosenfeld RJ, Ghosh S, Meade AL, Getzoff ED, Stuehr DJ: Distinct dimer interaction and regulation in nitric oxide synthase type I, II and III. J Biol Chem 277: 31020-31030, 2002
30. 4B promotes assembly of enzyme subunits into an active dimer. Proc Natl Acad Sci USA 92: 11771-11775, 1995
31. Klatt P, Schmidt K, Lehner D, Glatter O, Bachinger HP, Meyer B: structural analysis of porcine brain nitric oxide synthase reveals a role for tetrahydrobiopterin and L-arginine in the formation of an SDS-resistance dimmer. EMBO J 14: 3687-3695, 1995
32. Panda K, Ghosh S, Stuehr DJ: Calmodulin activates intersubunit electron transfer in the neuronal nitric-oxide synthase dimer. J Biol Chem 276: 23356, 2001
33. Klatt P, Pfeiffer S, List BM, Lehner D, Otto G, Bachinger HP, Werner ER, Schmidt K, Mayer B: Characterization of Heme-deficient Neuronal Nitric-oxide Synthase Reveals a Role for Heme in Subunit Dimerization and Binding of the Amino Acid Substrate and Tetrahydrobiopterin. J Biol Chem 271: 7336-7342, 1996
34. Sengupta R, Sahoo R, Mukherjee S, Regulski M, Tully T, Stuehr DJ, Ghosh S: Characterization of Drosophila nitric oxide sAnthase: a biochemical study. Biochem Biophys Res Com 306: 590-597, 2003
35. Ghosh DK, Stuehr DJ: Reconstitution of the second step in NO synthesis using the isolated oxygenase and reductase domains of macrophage NO synthase. Biochemistry 34: 801-807, 1995
36. Lowe PN, Smith D, Stammers DK, Rivorose-Moreno V, Moncada S, Charles I: A. Boyhan, Identification of the domains of neuronal nitric oxide synthase by limited proteolysis. Biochem J 314: 55-62, 1996
37. Abu-Soud HM, Wang J, Rousseau DL, Fukuto JM, Ignarro LJ, Stuehr DJ: Neuronal nitric oxide synthase self-inactivates by forming a ferrous-nitrosyl complex during aerobic catalysis. J Biol Chem 270: 22997-23006, 1995
38. Siddhanta U, Wu C, Abu-Saud HM, Zhang J, Ghosh DK, Stuehr DJ: Heme iron reduction and catalysis by a nitric oxide synthase heterodimer containing one reductase and two oxygenase domains. J Biol Chem 271: 7309-7312, 1996
39. Pufahl PA, Wishonok JS, Marletta MA: Hydrogen peroxide-supported oxidation of NG-hydroxy-L-arginine by nitric oxide synthase. Biochemistry 34: 1930-1941, 1995
40. Adak S, Wang Q, Stuehr DJ: Arginine conversion to nitroxide by tetrahydrobiopterin-free neuronal nitric-oxide synthase. J Biol Chem 275: 33554-33561, 2000
41. Creighton TE, Shortle D: Electrophoretic characterization of the denatured states of staphylococcal nuclease. J Mol Biol 242: 670-682, 1994
42. Goldenburg DPA Protein structure: a practical approach. IRL press, London, 1997
43. McMillan K, Masters BS: Optical difference spectrophotometry as a probe of rat brain nitric oxide synthase heme-substrate interaction. Biochemistry 32: 9875-9880, 1993
44. Creighton TE: Electrophoretic analysis of the unfolding of proteins by urea. J Mol Biol 129: 235-264, 1979
45. Crane BR, Rosenfeld RJ, Arvai AS, Ghosh DK, Ghosh S, Tainer JA, Stuehr DJ, Getzoff ED: N-terminal domain swapping and metal ion binding in nitric oxide synthase dimerization. EMBO J 18: 6271-6281, 1999
46. Li D, Stuehr DJ, Yeh SR, Rousseau DL: Heme distortion modulated by ligand-protein interactions in inducible nitric oxide synthase. J Biol Chem 279: 26489-26499, 2004
47. Li H, Raman CS, Glaser CB, Blasko E, Young TA, Parkinson JF, Whitlow M, Poulos TL: Crystal structures of zinc-free and -bound heme domain of human inducible nitric-oxide synthase. Implications for dimer stability and comparison with endothelial nitric-oxide synthase. J Biol Chem 274: 21276-21284, 1999
48. Morris Jr. SM, Kepka-Lenhart D, Chen LC: Differential regulation of arginases and inducible nitric oxide synthase in murine macrophage cells. Am J Physiol 275: E740-E747, 1998
49. Que LG, Kantrow SP, Jenkinson CP, Piantadosi CA, Huang YC: Induction of arginase isoforms in the lung during hyperoxia. Am J Physiol 275: L96-L102, 1998
50. Geller DA, Di Silvio M, Billiar TR, Hatakeyama K: GTP cyclohydrolase I is coinduced in hepatocytes stimulated to produce nitric oxide. Biochem Biophys Res Commun 276: 633-641, 2000
51. Sakai N, Kaufman S, Milstein S: Tetrahydrobiopterin is required for cytokine-induced nitric oxide production in a murine macrophage cell line (RAW 264). Mol Pharmacol 43: 6-10, 1993
52. Wilson DK, Rafferty SP, Konermann L: Kinetic unfolding mechanism of the nitric oxide synthase domain determined by time-resolved electrospray mass spectrometry. Biochemistry 44: 2276-2283, 2005