FMN fluorescence in inducible NOS constructs reveals a series of conformational states involved in the reductase catalytic cycle

FEBS Journal

Volumn 279, Issue 7, 2012, Pages 1306-1317

  Ghosh, Dipak K ^a,c   Ray, Krishanu ^b   Rogers, Albert J ^a   Nahm, Nicholas J ^a   Salerno, John C ^c  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c KENNESAW STATE UNIVERSITY   (United States)

Author keywords

calmodulin; fluorescence; FMN; mechanism; nitric oxide synthase

Indexed keywords

CYTOCHROME P450 REDUCTASE; EDETIC ACID; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; HOLOENZYME; INDUCIBLE NITRIC OXIDE SYNTHASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME BINDING; ENZYME CONFORMATION; ENZYME SUBSTRATE COMPLEX; FLUORESCENCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUANTUM YIELD;

CALMODULIN; CATALYSIS; FLAVIN MONONUCLEOTIDE; MOLECULAR CONFORMATION; NITRIC OXIDE SYNTHASE TYPE II; OXIDATION-REDUCTION; OXIDOREDUCTASES; SPECTROMETRY, FLUORESCENCE;

EID: 84859097238     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08525.x     Document Type: Article

References (48)

1. Furchgott RF, (1988) Vascular smooth muscle, peptides, autonomic nerves and endothelium. In Vasoldilation (, Vanhouette PM, ed.), pp. 401-404. Raven Press, New York.
2. Ignarro LJ, Buga GM, Wood KS, Byrns RE, &, Chadhuri G, (1987) Endothelium derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 24, 9265-9269.
3. Garthwaite J, Charles SL, &, Chess-Williams R, (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336, 385-388.
4. Gally JA, Montague PR, Reeke GN Jr, &, Edelman GM, (1990) Nitric oxide: linking space and time in the brain. Proc Natl Acad Sci USA 87, 3547-3551.
5. Bredt DS, Hwang PM, &, Snyder SH, (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347, 768-770.
6. Knowles RG, Merrett M, Salter M, &, Moncada S, (1990) Differential induction of brain, lung and liver nitric oxide synthase by endotoxin in the rat. Biochem J 270, 833-836.
7. Marletta MA, Yoon PS, Iyengar R, Leaf CD, &, Wishnok JS, (1988) Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry 27, 8706-8711.
8. Stuehr DJ, Gross SS, Sakuma I, Levi R, &, Nathan CF, (1989) Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium-derived relaxing factor and the chemical reactivity of nitric oxide. J Exp Med 169, 1011-1020.
9. Abu-Soud HM, &, Stuehr DJ, (1993) Electron transfer in the nitric-oxide synthases. Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. Proc Natl Acad Sci USA 90, 10769-10772.
10. Cho HJ, Xie QW, Calaycay J, Mumford RA, Swiderek KM, Lee TD, &, Nathan C, (1992) Calmodulin is a subunit of nitric oxide synthase from macrophages. J Exp Med 176, 599-604.
11. Ghosh DK, &, Salerno JC, (2003) Nitric oxide synthases: domain structure and alignment in enzyme function and control. Front Biosci 8, D193-D209.
12. Daff S, (2010) NO synthase: structures and mechanisms. Nitric Oxide 23, 1-11.
13. Li H, &, Poulos TL, (2005) Structure-function studies on nitric oxide synthases. J Inorg Biochem 99, 293-305.
14. Salerno JC, &, Ghosh DK, (2009) Space, time and nitric oxide-neuronal nitric oxide synthase generates signal pulses. FEBS J 276, 6677-6688.
15. Roman LJ, Martásek P, &, Masters BS, (2002) Intrinsic and extrinsic modulation of nitric oxide synthase activity. Chem Rev 102, 1179-1190.
16. Stuehr DJ, Tejero J, &, Haque MM, (2009) Structural and mechanistic aspects of flavoproteins: electron transfer through the nitric oxide synthase flavoprotein domain. FEBS J 276, 3959-3974.
17. Salerno JC, Harris DE, Irizarry K, Patel B, Morales AJ, Smith SM, Martasek P, Roman LJ, Masters BS, Jones CL, et al. (1997) An autoinhibitory control element defines calcium-regulated isoforms of nitric oxide synthase. J Biol Chem 272, 29769-29777.
18. Daff S, (2003) Calmodulin-dependent regulation of mammalian nitric oxide synthase. Biochem Soc Trans 31, 502-505.
19. Tiso M, Tejero J, Panda K, Aulak KS, &, Stuehr DJ, (2007) Versatile regulation of neuronal nitric oxide synthase by specific regions of its C-terminal tail. Biochemistry 46, 14418-14428.
20. Roman LJ, Martásek P, Miller RT, Harris DE, de La Garza MA, Shea TM, Kim JJ, &, Masters BS, (2000) The C termini of constitutive nitric-oxide synthases control electron flow through the flavin and heme domains and affect modulation by calmodulin. J Biol Chem 275, 29225-29232.
21. Ghosh DK, Holliday MA, Thomas C, Weinberg JB, Smith SM, &, Salerno JC, (2006) Towards a NOS output state: design and properties of NOS oxygenase/FMN domain construct. J Biol Chem 281, 14173-14183.
22. Feng C, Thomas C, Holliday MA, Tollin G, Salerno JC, Ghosh DK, &, Enemark JH, (2006) Direct measurement by laser flash photolysis of intramolecular electron transfer in a two-domain construct of murine inducible nitric oxide synthase. J Am Chem Soc 128, 3808-3811.
23. Feng C, Thomas C, Holliday MA, Tollin G, Salerno JC, Enemark JH, &, Ghosh DK, (2006) Intraprotein, electron transfer in a two-domain construct of neuronal nitric oxide synthase: the output state in nitric oxide formation. Biochemistry 45, 6354-6362.
24. Feng C, Tollin G, Hazzard JT, Nahm NJ, Guillemette JG, Salerno JC, &, Ghosh DK, (2007) Direct measurement by laser flash photolysis of intraprotein electron transfer in a rat neuronal nitric oxide synthase. J Am Chem Soc 129, 5621-5629.
25. Li H, Das A, Sibhatu H, Jamal J, Sligar SG, &, Poulos TL, (2008) Exploring the electron transfer properties of neuronal nitric-oxide synthase by reversal of the FMN redox potential. J Biol Chem 283, 34762-34772.
26. Ilagan RP, Tejero J, Aulak KS, Ray SS, Hemann C, Wang ZQ, Gangoda M, Zweier JL, &, Stuehr DJ, (2009) Regulation of FMN subdomain interactions and function in neuronal nitric oxide synthase. Biochemistry 48, 3864-3876.
27. Jáchymová M, Martásek P, Panda S, Roman LJ, Panda M, Shea TM, Ishimura Y, Kim JJ, &, Masters BS, (2005) Recruitment of governing elements for electron transfer in the nitric oxide synthase family. Proc Natl Acad Sci USA 102, 15833-15838.
28. Gachui R, Presta A, Bentley DF, Abu-Soud HM, McArthur R, Brudvig G, Ghosh DK, &, Stuehr DJ, (1996) Characterization of the reductase domain of rat neuronal NO synthase generated in the methylotrophic yeast Pichia pastaris. J Biol Chem 271, 20594-20602.
29. Newman E, Spratt DE, Mosher J, Cheyne B, Montgomery HJ, Wilson DL, Weinberg JB, Smith SM, Salerno JC, Ghosh DK, et al. (2004) Differential activation of nitric oxide synthase isozymes by calmodulin-troponin C chimeras. J Biol Chem 279, 33547-33557.
30. Roman LJ, &, Masters BS, (2006) Electron transfer by neuronal nitric-oxide synthase is regulated by concerted interaction of calmodulin and two intrinsic regulatory elements. J Biol Chem 281, 23111-23118.
31. Salerno JC, Ghosh DK, Ray K, Adrados M, Nahm N, Li H, Poulos TI, &, Lakowicz J, (2010) FMN fluorescence in iNOS constructs reveals a series of conformational states involved in the reductase catalytic cycle. Nitric Oxide-Biol Ch 22, S12.
32. Li W, Fan W, Elmore BO, &, Feng C, (2011) Effect of solution viscosity on intraprotein electron transfer between the FMN and heme domains in inducible nitric oxide synthase. FEBS Lett 585, 2622-2626.
33. Narayanasami R, Nishimura JS, McMillan K, Roman LJ, Shea TM, Robida AM, Horowitz PM, &, Masters BS, (1997) The influence of chaotropic reagents on neuronal nitric oxide synthase and its flavoprotein module. Urea and guanidine hydrochloride stimulate NADPH-cytochrome c reductase activity of both proteins. Nitric Oxide 1, 39-49.
34. Brunner K, Tortschanoff A, Hemmens B, Andrew PJ, Mayer B, &, Kungl AJ, (1998) Sensitivity of flavin fluorescence dynamics in neuronal nitric oxide synthase to cofactor-induced conformational changes and dimerization. Biochemistry 37, 17545-17553.
35. Bastiaens PIH, Bonants PJM, Mülle F, &, Visser AJWG, (1989) Time-resolved fluorescence spectroscopy of NADPH-cytochrome P-450 reductase: demonstration of energy transfer between the two prosthetic groups. Biochemistry 28, 8416-8425.
36. Climent T, González-Luque R, Merchán M, &, Serrano-Andrés L, (2006) Theoretical insight into the spectroscopy and photochemistry of isoalloxazine, the flavin core ring. J Phys Chem A 110, 13584.
37. Wang M, Roberts DL, Paschke R, Shea TM, Masters BS, &, Kim JJ, (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc Natl Acad Sci USA 94, 8411-8416.
38. Garcin ED, Bruns CM, Lloyd SJ, Hosfield DJ, Tiso M, Gachhui R, Stuehr DJ, Tainer JA, &, Getzoff ED, (2004) Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J Biol Chem 279, 37918-37927.
39. Marcus RA, (1993) Electron transfer reactions in chemistry: theory and experiment (Nobel lecture). Angew Chem Int Ed Engl 32, 1111-1121.
40. Moser CC, Page CC, &, Dutton PL, (2006) Darwin at the molecular scale: selection and variance in electron tunneling proteins including cyctochrome c oxidase. Philos Trans R Soc Lond B Biol Sci 361, 1295-1305.
41. Gray HB, &, Winkler JR, (2003) Electron tunneling through proteins. Q Rev Biophys 36, 341-372.
42. Prytkova TR, Kurnikov IV, &, Beratan DN, (2007) Coupling coherence distinguishes structure sensitivity in protein electron transfer. Science 315, 622-625.
43. Jasaitis A, Johansson MP, Wikström M, Vos MH, &, Verkhovsky MI, (2007) Nanosecond electron tunneling between the hemes in cytochrome bo3. Proc Natl Acad Sci USA 104, 20811-20814.
44. Astashkin AV, Elmore BO, Fan W, Guillemette JG, &, Feng C, (2010) Pulsed EPR determination of the distance between heme iron and FMN centers in a human inducible nitric oxide synthase. J Am Chem Soc 132, 12059-12067.
45. Salerno JC, (1985) EPR lineshapes of biological molecules: some effects of distributed parameters. Biochem Soc Trans 13, 611-615.
46. Ghosh DK, Rashid MB, Crane B, Taskar V, Mast M, Misukonis MA, Weinberg JB, &, Eissa NT, (2001) Characterization of key residues in the subdomain encoded by exons 8 and 9 of human inducible nitric oxide synthase: a critical role for Asp-280 in substrate binding and subunit interactions. Proc Natl Acad Sci USA 98, 10392-10397.
47. Ray K, Szmacinski H, &, Lakowicz JR, (2009) Enhanced fluorescence of proteins and label-free bioassays using aluminum nanostructures. Anal Chem 80, 7313-7318.
48. Lakowicz JR, (2006) Principles of Fluorescence Spectroscopy, 3rd edn. Springer, New York.