Distinct conformational behaviors of four mammalian dual‐flavin reductases (cytochrome P450 reductase, methionine synthase reductase, neuronal nitric oxide synthase, endothelial nitric oxide synthase) determine their unique catalytic profiles
dc.contributor.author | Haque, Mohammad M. | en_US |
dc.contributor.author | Bayachou, Mekki | en_US |
dc.contributor.author | Tejero, Jesus | en_US |
dc.contributor.author | Kenney, Claire T. | en_US |
dc.contributor.author | Pearl, Naw M. | en_US |
dc.contributor.author | Im, Sang‐choul | en_US |
dc.contributor.author | Waskell, Lucy | en_US |
dc.contributor.author | Stuehr, Dennis J. | en_US |
dc.date.accessioned | 2014-12-09T16:54:07Z | |
dc.date.available | WITHHELD_13_MONTHS | en_US |
dc.date.available | 2014-12-09T16:54:07Z | |
dc.date.issued | 2014-12 | en_US |
dc.identifier.citation | Haque, Mohammad M.; Bayachou, Mekki; Tejero, Jesus; Kenney, Claire T.; Pearl, Naw M.; Im, Sang‐choul ; Waskell, Lucy; Stuehr, Dennis J. (2014). "Distinct conformational behaviors of four mammalian dualâ flavin reductases (cytochrome P450 reductase, methionine synthase reductase, neuronal nitric oxide synthase, endothelial nitric oxide synthase) determine their unique catalytic profiles." FEBS Journal 281(23): 5325-5340. | en_US |
dc.identifier.issn | 1742-464X | en_US |
dc.identifier.issn | 1742-4658 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/109651 | |
dc.publisher | Wiley Periodicals, Inc. | en_US |
dc.subject.other | Conformational Equilibrium | en_US |
dc.subject.other | Flavoprotein | en_US |
dc.subject.other | Kinetic Model | en_US |
dc.subject.other | Nitric Oxide | en_US |
dc.subject.other | Electron Transfer | en_US |
dc.title | Distinct conformational behaviors of four mammalian dual‐flavin reductases (cytochrome P450 reductase, methionine synthase reductase, neuronal nitric oxide synthase, endothelial nitric oxide synthase) determine their unique catalytic profiles | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Biological Chemistry | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/109651/1/febs13073.pdf | |
dc.identifier.doi | 10.1111/febs.13073 | en_US |
dc.identifier.source | FEBS Journal | en_US |
dc.identifier.citedreference | Brenner S, Hay S, Munro AW & Scrutton NS ( 2008 ) Inter‐flavin electron transfer in cytochrome P450 reductase ‐ effects of solvent and pH identify hidden complexity in mechanism. FEBS J 275, 4540 – 4557. | en_US |
dc.identifier.citedreference | Hay S, Brenner S, Khara B, Quinn AM, Rigby SE & Scrutton NS ( 2010 ) Nature of the energy landscape for gated electron transfer in a dynamic redox protein. J Am Chem Soc 132, 9738 – 9745. | en_US |
dc.identifier.citedreference | Ellis J, Gutierrez A, Barsukov IL, Huang WC, Grossmann JG & Roberts GC ( 2009 ) Domain motion in cytochrome P450 reductase: conformational equilibria revealed by NMR and small‐angle x‐ray scattering. J Biol Chem 284, 36628 – 36637. | en_US |
dc.identifier.citedreference | Huang WC, Ellis J, Moody PC, Raven EL & Roberts GC ( 2013 ) Redox‐linked domain movements in the catalytic cycle of cytochrome p450 reductase. Structure 21, 1581 – 1589. | en_US |
dc.identifier.citedreference | Persechini A, Tran QK, Black DJ & Gogol EP ( 2013 ) Calmodulin‐induced structural changes in endothelial nitric oxide synthase. FEBS Lett 587, 297 – 301. | en_US |
dc.identifier.citedreference | Leys D, Basran J, Talfournier F, Sutcliffe MJ & Scrutton NS ( 2003 ) Extensive conformational sampling in a ternary electron transfer complex. Nat Struct Biol 10, 219 – 225. | en_US |
dc.identifier.citedreference | Toogood HS, Leys D & Scrutton NS ( 2007 ) Dynamics driving function: new insights from electron transferring flavoproteins and partner complexes. FEBS J 274, 5481 – 5504. | en_US |
dc.identifier.citedreference | Pudney CR, Khara B, Johannissen LO & Scrutton NS ( 2011 ) Coupled motions direct electrons along human microsomal P450 Chains. PLoS Biol 9, e1001222. | en_US |
dc.identifier.citedreference | Gutierrez A, Munro AW, Grunau A, Wolf CR, Scrutton NS & Roberts GC ( 2003 ) Interflavin electron transfer in human cytochrome P450 reductase is enhanced by coenzyme binding. Relaxation kinetic studies with coenzyme analogues. Eur J Biochem 270, 2612 – 2621. | en_US |
dc.identifier.citedreference | Leferink NG, Pudney CR, Brenner S, Heyes DJ, Eady RR, Samar HS, Hay S, Rigby SE & Scrutton NS ( 2012 ) Gating mechanisms for biological electron transfer: integrating structure with biophysics reveals the nature of redox control in cytochrome P450 reductase and copper‐dependent nitrite reductase. FEBS Lett 586, 578 – 584. | en_US |
dc.identifier.citedreference | Gutierrez A, Grunau A, Paine M, Munro AW, Wolf CR, Roberts GC & Scrutton NS ( 2003 ) Electron transfer in human cytochrome P450 reductase. Biochem Soc Trans 31, 497 – 501. | en_US |
dc.identifier.citedreference | Abu‐Soud HM, Yoho LL & Stuehr DJ ( 1994 ) Calmodulin controls neuronal nitric‐oxide synthase by a dual mechanism. Activation of intra‐ and interdomain electron transfer. J Biol Chem 269, 32047 – 32050. | en_US |
dc.identifier.citedreference | Chen PF & Wu KK ( 2003 ) Structural elements contribute to the calcium/calmodulin dependence on enzyme activation in human endothelial nitric‐oxide synthase. J Biol Chem 278, 52392 – 52400. | en_US |
dc.identifier.citedreference | Daff S ( 2003 ) Calmodulin‐dependent regulation of mammalian nitric oxide synthase. Biochem Soc Trans 31, 502 – 505. | en_US |
dc.identifier.citedreference | Matsuda H & 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. | en_US |
dc.identifier.citedreference | Wu PR, Kuo CC, Yet SF, Liou JY, Wu KK & Chen PF ( 2012 ) Lobe‐specific calcium binding in calmodulin regulates endothelial nitric oxide synthase activation. PLoS One 7, e39851. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Haque MM, Panda K, Tejero J, Aulak KS, Fadlalla MA, Mustovich AT & Stuehr DJ ( 2007 ) A connecting hinge represses the activity of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 104, 9254 – 9259. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Wolthers KR, Lou X, Toogood HS, Leys D & Scrutton NS ( 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. | en_US |
dc.identifier.citedreference | Grunau A, Geraki K, Grossmann JG & 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. | en_US |
dc.identifier.citedreference | Haque MM, Fadlalla MA, Aulak KS, Ghosh A, Durra D & Stuehr DJ ( 2012 ) Control of electron transfer and catalysis in neuronal nitric‐oxide synthase (nNOS) by a hinge connecting its FMN and FAD‐NADPH domains. J Biol Chem 287, 30105 – 30116. | en_US |
dc.identifier.citedreference | Mendes P ( 1993 ) GEPASI: a software package for modelling the dynamics, steady states and control of biochemical and other systems. Comput Appl Biosci 9, 563 – 571. | en_US |
dc.identifier.citedreference | Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L et al. ( 2014 ) SWISS‐MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42, W252 – W258. | en_US |
dc.identifier.citedreference | Basse MJ, Betzi S, Bourgeas R, Bouzidi S, Chetrit B, Hamon V, Morelli X & Roche P ( 2013 ) 2P2Idb: a structural database dedicated to orthosteric modulation of protein‐protein interactions. Nucleic Acids Res 41, D824 – D827. | en_US |
dc.identifier.citedreference | Aigrain L, Fatemi F, Frances O, Lescop E & Truan G ( 2012 ) Dynamic control of electron transfers in diflavin reductases. Int J Mol Sci 13, 15012 – 15041. | en_US |
dc.identifier.citedreference | De Colibus L & Mattevi A ( 2006 ) New frontiers in structural flavoenzymology. Curr Opin Struct Biol 16, 722 – 728. | en_US |
dc.identifier.citedreference | Iyanagi T ( 2005 ) Structure and function of NADPH‐cytochrome P450 reductase and nitric oxide synthase reductase domain. Biochem Biophys Res Commun 338, 520 – 528. | en_US |
dc.identifier.citedreference | Joosten V & van Berkel WJ ( 2007 ) Flavoenzymes. Curr Opin Chem Biol 11, 195 – 202. | en_US |
dc.identifier.citedreference | Gomez‐Moreno C ( 2009 ) New roles of flavoproteins in molecular cell biology. FEBS J 276, 4289. | en_US |
dc.identifier.citedreference | Iyanagi T, Xia C & Kim JJ ( 2012 ) NADPH‐cytochrome P450 oxidoreductase: prototypic member of the diflavin reductase family. Arch Biochem Biophys 528, 72 – 89. | en_US |
dc.identifier.citedreference | Porter TD & Kasper CB ( 1986 ) NADPH‐cytochrome P‐450 oxidoreductase: flavin mononucleotide and flavin adenine dinucleotide domains evolved from different flavoproteins. Biochemistry 25, 1682 – 1687. | en_US |
dc.identifier.citedreference | Porter TD ( 1991 ) An unusual yet strongly conserved flavoprotein reductase in bacteria and mammals. Trends Biochem Sci 16, 154 – 158. | en_US |
dc.identifier.citedreference | Murataliev MB, Feyereisen R & Walker FA ( 2004 ) Electron transfer by diflavin reductases. Biochim Biophys Acta 1698, 1 – 26. | en_US |
dc.identifier.citedreference | Iyanagi T & Mason HS ( 1973 ) Some properties of hepatic reduced nicotinamide adenine dinucleotide phosphate‐cytochrome c reductase. Biochemistry 12, 2297 – 2308. | en_US |
dc.identifier.citedreference | Vermilion JL & Coon MJ ( 1978 ) Purified liver microsomal NADPH‐cytochrome P‐450 reductase. Spectral characterization of oxidation‐reduction states. J Biol Chem 253, 2694 – 2704. | en_US |
dc.identifier.citedreference | Shen AL, O'Leary KA & Kasper CB ( 2002 ) Association of multiple developmental defects and embryonic lethality with loss of microsomal NADPH‐cytochrome P450 oxidoreductase. J Biol Chem 277, 6536 – 6541. | en_US |
dc.identifier.citedreference | Daff S ( 2010 ) NO synthase: structures and mechanisms. Nitric Oxide 23, 1 – 11. | en_US |
dc.identifier.citedreference | Feng C ( 2012 ) Mechanism of nitric oxide synthase regulation: electron transfer and interdomain interactions. Coord Chem Rev 256, 393 – 411. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Leclerc D, Wilson A, Dumas R, Gafuik C, Song D, Watkins D, Heng HH, Rommens JM, Scherer SW, Rosenblatt DS et al. ( 1998 ) Cloning and mapping of a cDNA for methionine synthase reductase, a flavoprotein defective in patients with homocystinuria. Proc Natl Acad Sci USA 95, 3059 – 3064. | en_US |
dc.identifier.citedreference | Olteanu H & Banerjee R ( 2001 ) Human methionine synthase reductase, a soluble P‐450 reductase‐like dual flavoprotein, is sufficient for NADPH‐dependent methionine synthase activation. J Biol Chem 276, 35558 – 35563. | en_US |
dc.identifier.citedreference | Wolthers KR & Scrutton NS ( 2007 ) Protein interactions in the human methionine synthase‐methionine synthase reductase complex and implications for the mechanism of enzyme reactivation. Biochemistry 46, 6696 – 6709. | en_US |
dc.identifier.citedreference | Paine MJ, Garner AP, Powell D, Sibbald J, Sales M, Pratt N, Smith T, Tew DG & Wolf CR ( 2000 ) Cloning and characterization of a novel human dual flavin reductase. J Biol Chem 275, 1471 – 1478. | en_US |
dc.identifier.citedreference | Ostrowski J, Barber MJ, Rueger DC, Miller BE, Siegel LM & Kredich NM ( 1989 ) Characterization of the flavoprotein moieties of NADPH‐sulfite reductase from Salmonella typhimurium and Escherichia coli. Physicochemical and catalytic properties, amino acid sequence deduced from DNA sequence of cysJ, and comparison with NADPH‐cytochrome P‐450 reductase. J Biol Chem 264, 15796 – 15808. | en_US |
dc.identifier.citedreference | Munro AW, Leys DG, McLean KJ, Marshall KR, Ost TW, Daff S, Miles CS, Chapman SK, Lysek DA, Moser CC et al. ( 2002 ) P450 BM3: the very model of a modern flavocytochrome. Trends Biochem Sci 27, 250 – 257. | en_US |
dc.identifier.citedreference | Munro AW, Girvan HM & McLean KJ ( 2007 ) Cytochrome P450–redox partner fusion enzymes. Biochim Biophys Acta 1770, 345 – 359. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Xia C, Panda SP, Marohnic CC, Martasek P, Masters BS & Kim JJ ( 2011 ) Structural basis for human NADPH‐cytochrome P450 oxidoreductase deficiency. Proc Natl Acad Sci USA 108, 13486 – 13491. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Xia C, Hamdane D, Shen AL, Choi V, Kasper CB, Pearl NM, Zhang H, Im SC, Waskell L & Kim JJ ( 2011 ) Conformational changes of NADPH‐cytochrome P450 oxidoreductase are essential for catalysis and cofactor binding. J Biol Chem 286, 16246 – 16260. | en_US |
dc.identifier.citedreference | Hamdane D, Xia C, Im SC, Zhang H, Kim JJ & Waskell L ( 2009 ) Structure and function of an NADPH‐cytochrome P450 oxidoreductase in an open conformation capable of reducing cytochrome P450. J Biol Chem 284, 11374 – 11384. | en_US |
dc.identifier.citedreference | Laursen T, Jensen K & Moller BL ( 2011 ) Conformational changes of the NADPH‐dependent cytochrome P450 reductase in the course of electron transfer to cytochromes P450. Biochim Biophys Acta 1814, 132 – 138. | en_US |
dc.identifier.citedreference | Meints CE, Gustafsson FS, Scrutton NS & Wolthers KR ( 2011 ) Tryptophan 697 modulates hydride and interflavin electron transfer in human methionine synthase reductase. Biochemistry 50, 11131 – 11142. | en_US |
dc.identifier.citedreference | Pudney CR, Heyes DJ, Khara B, Hay S, Rigby SE & Scrutton NS ( 2012 ) Kinetic and spectroscopic probes of motions and catalysis in the cytochrome P450 reductase family of enzymes. FEBS J 279, 1534 – 1544. | en_US |
dc.identifier.citedreference | Wolthers KR & Scrutton NS ( 2004 ) Electron transfer in human methionine synthase reductase studied by stopped‐flow spectrophotometry. Biochemistry 43, 490 – 500. | en_US |
dc.identifier.citedreference | Aigrain L, Pompon D, Morera S & Truan G ( 2009 ) Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase. EMBO Rep 10, 742 – 747. | en_US |
dc.identifier.citedreference | Ghosh DK, Ray K, Rogers AJ, Nahm NJ & Salerno JC ( 2012 ) FMN fluorescence in inducible NOS constructs reveals a series of conformational states involved in the reductase catalytic cycle. FEBS J 279, 1306 – 1317. | en_US |
dc.identifier.citedreference | Haque MM, Kenney C, Tejero J & Stuehr DJ ( 2011 ) A kinetic model linking protein conformational motions, interflavin electron transfer and electron flux through a dual‐flavin enzyme‐simulating the reductase activity of the endothelial and neuronal nitric oxide synthase flavoprotein domains. FEBS J 278, 4055 – 4069. | en_US |
dc.identifier.citedreference | Haque MM, Bayachou M, Fadlalla MA, Durra D & Stuehr DJ ( 2013 ) Charge Pairing Interactions Control the Conformational Setpoint and Motions of the FMN Domain in Neuronal Nitric Oxide Synthase. Biochem J 450, 607 – 617. | en_US |
dc.identifier.citedreference | Ilagan RP, Tiso M, Konas DW, Hemann C, Durra D, Hille R & Stuehr DJ ( 2008 ) Differences in a conformational equilibrium distinguish catalysis by the endothelial and neuronal nitric‐oxide synthase flavoproteins. J Biol Chem 283, 19603 – 19615. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Konas DW, Zhu K, Sharma M, Aulak KS, Brudvig GW & Stuehr DJ ( 2004 ) The FAD‐shielding residue Phe1395 regulates neuronal nitric‐oxide synthase catalysis by controlling NADP+ affinity and a conformational equilibrium within the flavoprotein domain. J Biol Chem 279, 35412 – 35425. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Craig DH, Chapman SK & 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. | en_US |
dc.identifier.citedreference | Gutierrez A, Paine M, Wolf CR, Scrutton NS & Roberts GC ( 2002 ) Relaxation kinetics of cytochrome P450 reductase: internal electron transfer is limited by conformational change and regulated by coenzyme binding. Biochemistry 41, 4626 – 4637. | en_US |
dc.identifier.citedreference | Grunau A, Paine MJ, Ladbury JE & 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. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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