Thermodynamic analysis of interactions between cofactor and neuronal nitric oxide synthase

Biochemistry

Volumn 50, Issue 10, 2011, Pages 1714-1722

  Sanae, Ryuhei ^a   Kurokawa, Fumiaki ^a   Oda, Masayuki ^a   Ishijima, Sumio ^a   Sagami, Ikuko ^a  

^a KYOTO PREFECTURAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITIES; BINDING CONSTANT; COFACTOR BINDING; COFACTORS; CONFORMATIONAL CHANGE; CYTOCHROME C; DELETION MUTANTS; ELECTRON TRANSFER; ENTHALPY GAIN; ENTROPY CHANGES; HEAT CAPACITY CHANGE; ISOTHERMAL TITRATION CALORIMETRY; KINETIC MODELS; NITRIC-OXIDE SYNTHASE; THERMO DYNAMIC ANALYSIS;

AMIDES; BINDING ENERGY; NITRIC OXIDE; STOICHIOMETRY; THERMOANALYSIS; THERMODYNAMICS;

CAMS;

2',5' ADENOSINE DIPHOSPHATE; ADENOSINE; ADENOSINE DIPHOSPHATE; CALCIUM ION; CALMODULIN; NEURONAL NITRIC OXIDE SYNTHASE; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; ELECTRON TRANSPORT; ENTHALPY; ENTROPY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME KINETICS; HEAT; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY; THERMODYNAMICS;

ANIMALS; BINDING SITES; BIOCATALYSIS; CALMODULIN; CATTLE; MODELS, MOLECULAR; NITRIC OXIDE SYNTHASE TYPE I; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; RATS; THERMODYNAMICS;

EID: 79952377875     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101575u     Document Type: Article

References (54)

1. Schmidt, H. H. and Walter, U. (1994) NO at work Cell 78, 919-925 (Pubitemid 24292320)
2. Mayer, B., Ed. (2000) Handb. Exp. Pharmacol. 143, 206 - 234.
3. Bredt, D. S. and Snyder, S. H. (1994) Nitric oxide: a physiologic messenger molecule Annu. Rev. Biochem. 63, 175-195
4. Stuehr, D. J. (1999) Mammalian nitric oxide synthases Biochim. Biophys. Acta 1411, 217-230 (Pubitemid 29221951)
5. Alderton, W. K., Cooper, C. E., and Knowles, R. G. (2001) Nitric oxide synthases: structure, function and inhibition Biochem. J. 357, 593-615 (Pubitemid 32735142)
6. Li, H. and Poulos, T. L. (2005) Structure-function studies on nitric oxide synthases J. Inorg. Biochem. 99, 293-305 (Pubitemid 39642983)
7. Crane, B. R., Arvai, A. S., Ghosh, D. K., Wu, C., Getzoff, E. D., Stuehr, D. J., and Tainer, J. A. (1998) Structure of nitric oxide synthase oxygenase dimer with pterin and substrate Science 279, 2121-2126 (Pubitemid 28196359)
8. Raman, C. S., Li, J., Martásek, P., Kral, V., Masters, B. S. S., and Poulos, T. L. (1998) Crystal structure of constitutive endothelial nitric oxide synthase: a paradigm for pterin function involving a novel metal center Cell 95, 939-950 (Pubitemid 29019046)
9. Garcin, E. D., Bruns, C. M., Lloyd, S. J., Hosfield, D. J., Tiso, M., Gachhui, R., Stuehr, D. J., Tainer, J. A., and Getzoff, E. D. (2004) Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase J. Biol. Chem. 279, 37918-37927 (Pubitemid 39195507)
10. Wang, M., Roberts, D. L., Paschke, R., Shea, T. M., Masters, B. S. S., and Kim, J. J. (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes Proc. Natl. Acad. Sci. U.S.A. 94, 8411-8416 (Pubitemid 27335052)
11. Gruez, A., Pignol, D., Zeghouf, M., Coves, J., Fontecave, M., Ferrer, J.-L., and Fontecilla-Camps, J. C. (2000) Four crystal structures of the 60 kDa flavoprotein monomer of the sulfite reductase indicate a disordered flavodoxin-like module J. Mol. Biol. 299, 199-212
12. Wolthers, K. R., Lou, X., Toogood, H. S., Leys, D., and Scrutton, N. S. (2007) Mechanism of coenzyme binding to human methionine synthase reductase revealed through the crystal structure of the FNR-like module and isothermal titration calorimetry Biochemistry 46, 11833-11844 (Pubitemid 47623751)
13. Siddhanta, U., Presta, A., Fan, B. C., Wolan, D., Rosseau, D. L., and Stuehr, D. J. (1998) Domain swapping in inducible nitric oxide synthase. Electron transfer occurs mainly between flavin and heme groups located on adjacent subunits in the dimmer J. Biol. Chem. 273, 18950-18958 (Pubitemid 28366284)
14. Sagami, I., Daff, S., and Shimizu, T. (2001) Intrasubunit and intersubunit electron transfer in neuronal nitric-oxide synthase: effect of calmodulin on heterodimer catalysis J. Biol. Chem. 276, 30036-30042
15. Abu-Soud, H. M., Yoho, L. L., and Stuehr, D. J. (1994) Calmodulin controls neuronal nitric-oxide synthase by a dual mechanism. Activation of intra- and interdomain electron transfer J. Biol. Chem. 269, 32047-32050
16. Matsuda, H. and Iyanagi, T. (1999) Calmodulin activates intramolecular electron transfer between the two flavins of neuronal nitric oxide synthase flavin domain Biochim. Biophys. Acta 1473, 345-355
17. Salerno, J. C., Harris, D. E., Irizarry., K., Patel, B., Morales, A. J., Smith, S. M. E., Martásek, P., Roman, L. J., Masters, B. S. S., Jones, C. L., Weismann, B. A., Lane, P., Liu, Q., and Gross, S. S. (1997) An autoinhibitory control element defines calcium-regulated isoforms of nitric oxide synthase J. Biol. Chem. 272, 29769-29777 (Pubitemid 27508072)
18. Daff, S., Sagami, I., and Shimizu, T. (1999) The 42-amino acid insert in the FMN domain of neuronal nitric-oxide synthase exerts control over Ca(2+)/calmodulin-dependent electron transfer J. Biol. Chem. 274, 30589-30595
19. Montgomery, H. J., Romanov, V., and Guillemette, J. G. (2000) Removal of a putative inhibitory element reduces the calcium-dependent calmodulin activation of neuronal nitric-oxide synthase J. Biol. Chem. 275, 5052-5058
20. Roman, L. J., Martásek, P., Miller, R. T., Harris, D. E., de la Garza, M. A., Shea, T. M., Kim, J.-J. P., and Masters, B. S. S. (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 (Pubitemid 32043790)
21. Stuehr, D. J., Jesu′ s Tejero, J, and Haque, M. M. (2009) Structural and mechanistic aspects of flavoproteins: electron transfer through the nitric oxide synthase flavoprotein domain FEBS J. 276, 3959-3974
22. Welland, A, Garnaud, P. E., Kitamura, M, Miles, C. S., and Daff, S. (2008) Importance of the domain-domain interface to the catalytic action of the NO synthase reductase domain Biochemistry 47, 9771-9780
23. Fulton, D., Gratton, J. P., McCabe, T. J, Fontana, J., Fujio, Y., Walsh, K., Franke, T. F., Papapetropoulos, A., and Sessa, W. C. (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt Nature 399, 597-601
24. Adak, S., Santolini, J., Tikunova, S., Wang, Q., Johnson, J. D., and Stuehr, D. J. (2001) Neuronal nitric-oxide synthase mutant (Ser-1412 → Asp) demonstrates surprising connections between heme reduction, NO complex formation, and catalysis J. Biol. Chem. 276, 1244-1252 (Pubitemid 32096552)
25. 2+ concentrations required for calmodulin to bind and activate the enzyme Biochemistry 47, 7557-7566 (Pubitemid 351991032)
26. Daff, S., Noble, M. A., Craig, D. H., Rivers, S. L., Chapman, S. K., Munro, A. W., Fujiwara, S., Rozhkova, E., Sagami, I., and Shimizu, T. (2001) Control of electron transfer in neuronal NO synthase Biochem. Soc. Trans. 29, 147-152 (Pubitemid 32587494)
27. Craig, D. H., Chapman, S. K., and Daff, S. (2002) Calmodulin activates electron transfer through neuronal nitric-oxide synthase reductase domain by releasing an NADPH-dependent conformational lock J. Biol. Chem. 277, 33987-33994
28. Adak, S., Sharma, M., Meade, A. L., and Stuehr, D. J. (2002) A conserved flavin-shielding residue regulates NO synthase electron transfer and nicotinamide coenzyme specificity Proc. Natl. Acad. Sci. U.S.A. 99, 13516-13521 (Pubitemid 35215413)
29. + affinity and a conformational equilibrium within the flavoprotein domain J. Biol. Chem. 279, 35412-35425 (Pubitemid 39100541)
30. Jachymova, M., Martásek, P., Panda, S., Roman, L. J., Panda, M., Shea, T. M., Ishimura, Y., Kim, J.-J. P., and Masters, B. S. S. (2005) Recruitment of governing elements for electron transfer in the nitric oxide synthase family Proc. Natl. Acad. Sci. U.S.A. 102, 15833-15838 (Pubitemid 41552828)
31. Tiso, M., Konas, D. W., Panda, K., Garcin, E. D., Sharma, M., Getzoff, E. D., and Stuehr, D. J. (2005) C-terminal tail residue Arg1400 enables NADPH to regulate electron transfer in neuronal nitric-oxide synthase J. Biol. Chem. 280, 39208-39219 (Pubitemid 41713873)
32. Tiso, M., Tejero, J., Panda, K., Aulak, K. S., and Stuehr, D. J. (2007) Versatile regulation of neuronal nitric oxide synthase by specific regions of its C-terminal tail Biochemistry 46, 14418-14428 (Pubitemid 350276349)
33. Ilagan, R. P., Tejero, J., Aulak, K. S., Ray, S. S., Hemann, C., Wang, Z. Q., Gangoda, M., Zweier, J. L., and Stuehr, D. J. (2009) Regulation of FMN subdomain interactions and function in neuronal nitric oxide synthase Biochemistry 48, 3864-3876
34. Guan, Z. W., Haque, M. M., Wei, C. C, Garcin, E. D., Getzoff, E. D., and Stuehr, D. J. (2010) Lys842 in neuronal nitric-oxide synthase enables the autoinhibitory insert to antagonize calmodulin binding, increase FMN shielding, and suppress interflavin electron transfer J. Biol. Chem. 285, 3064-3075
35. Knight, K. and Scrutton, N. S. (2002) Stopped-flow kinetic studies of electron transfer in the reductase domain of neuronal nitric oxide synthase: reevaluation of the kinetic mechanism reveals new enzyme intermediates and variation with cytochrome P450 reductase Biochem. J. 367, 19-30 (Pubitemid 35176887)
36. Daff, S. (2004) An appraisal of multiple NADPH binding-site models proposed for cytochrome P450 reductase, NO synthase, and related diflavin reductase systems Biochemistry 43, 3929-3932 (Pubitemid 38437059)
37. Grunau, A, Paine, M. J., Ladbury, J. E., and Gutierrez, A. (2006) Global effects of the energetics of coenzyme binding: NADPH controls the protein interaction properties of human cytochrome P450 reductase Biochemistry 45, 1421-1434 (Pubitemid 43214807)
38. Sato, Y., Sagami, I., and Shimizu, T. (2004) Identification of caveolin-1-interacting sites in neuronal nitric-oxide synthase. Molecular mechanism for inhibition of NO formation J. Biol. Chem. 279, 8827-8836 (Pubitemid 38295941)
39. Rozhkova, E. A., Fujimoto, N., Sagami, I., Daff, S. N., and Shimizu, T. (2002) Interactions between the isolated oxygenase and reductase domains of neuronal nitric-oxide synthase: assessing the role of calmodulin J. Biol. Chem. 277, 16888-16894 (Pubitemid 34967714)
40. Goloubinoff, P., Gatenby, A. A., and Lorimer, G. H. (1989) GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli Nature 337, 44-47 (Pubitemid 19022550)
41. Gutierrez, A., Lian, L. Y., Wolf, C. R., Scrutton, N. S., and Roberts, G. C. (2001) Stopped-flow kinetic studies of flavin reduction in human cytochrome P450 reductase and its component domains Biochemistry 40, 1964-1975 (Pubitemid 32165665)
42. Roitel, O., Scrutton, N. S., and Munro, A. W. (2003) Electron transfer in flavocytochrome P450 BM3: kinetics of flavin reduction and oxidation, the role of cysteine 999, and relationships with mammalian cytochrome P450 reductase Biochemistry 42, 10809-10821 (Pubitemid 37102121)
43. 2+-activated calmodulin on the kinetic mechanism Biochemstry 40, 4722-4737 (Pubitemid 32377289)
44. Dunford, A. J., Rigby, S. E., Hay, S., Munro, A. W., and Scrutton, N. S. (2007) Conformational and thermodynamic control of electron transfer in neuronal nitric oxide synthase Biochemistry 46, 5018-5029 (Pubitemid 46683000)
45. Lumry, R. (2003) Uses of enthalpy-entropy compensation in protein research Biophys. Chem. 105, 545-557 (Pubitemid 37123083)
46. Sturtevant, J. M. (1977) Heat capacity and entropy changes in processes involving proteins Proc. Natl. Acad. Sci. U.S.A. 74, 2236-2240 (Pubitemid 8110685)
47. Luque, I., Todd, M. J., Gomez, J., Semo, N., and Freire, E. (1998) Molecular basis of resistance to HIV-1 protease inhibition: a plausible hypothesis Biochemistry 37, 5791-5797 (Pubitemid 28196730)
48. Spolar, R. S. and Record, M. T., Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA Science 263, 777-784 (Pubitemid 24093205)
49. Gomez, J., Hilser, V. J., Xie, D., and Freire, E. (1995) The heat capacity of proteins Proteins 22, 404-412
50. Bergqvist, S., Williams, M. A., O'Brien, R., and Ladbury, J. E. (2004) Heat capacity effects of water molecules and ions at a protein-DNA interface J. Mol. Biol. 4, 829-842 (Pubitemid 38201534)
51. Grunau, A., Geraki, K., Grossmann, J. G, and Gutierrez, A. (2007) Conformational dynamics and the energetics of protein-ligand interactions: role of interdomain loop in human cytochrome P450 reductase Biochemistry 46, 8244-8255 (Pubitemid 47075964)
52. Xia, C., Misra, I., Iyanagi, T., and Kim, J.-J. P. (2009) Regulation of interdomain interactions by calmodulin in inducible nitric-oxide synthase J. Biol. Chem. 284, 30708-30717
53. Frederick, K. K., Marlow, M. S., Valentine, K. G., and Wand, A. J. (2007) Heat capacity and entropy changes in processes involving proteins Nature 448, 325-329
54. Marlow, M. S., Dogan, J., Frederick, K. K., Valentine, K. G., and Wand, A. J. (2010) The role of conformational entropy in molecular recognition by calmodulin Nat. Chem. Biol. 6, 352-358