Nitrite reduction by xanthine oxidase family enzymes: a new class of nitrite reductases
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Mammalian xanthine oxidase (XO) and Desulfovibrio gigas aldehyde oxidoreductase (AOR) are members of the XO family of mononuclear molybdoenzymes that catalyse the oxidative hydroxylation of a wide range of aldehydes and heterocyclic compounds. Much less known is the XO ability to catalyse the nitrite reduction to nitric oxide radical (NO). To assess the competence of other XO family enzymes to catalyse the nitrite reduction and to shed some light onto the molecular mechanism of this reaction, we characterised the anaerobic XO- and AOR-catalysed nitrite reduction. The identification of NO as the reaction product was done with a NO-selective electrode and by electron paramagnetic resonance (EPR) spectroscopy. The steady-state kinetic characterisation corroborated the XO-catalysed nitrite reduction and demonstrated, for the first time, that the prokaryotic AOR does catalyse the nitrite reduction to NO, in the presence of any electron donor to the enzyme, substrate (aldehyde) or not (dithionite). Nitrite binding and reduction was shown by EPR spectroscopy to occur on a reduced molybdenum centre. A molecular mechanism of AOR- and XO-catalysed nitrite reduction is discussed, in which the higher oxidation states of molybdenum seem to be involved in oxygen-atom insertion, whereas the lower oxidation states would favour oxygen-atom abstraction. Our results define a new catalytic performance for AOR-the nitrite reduction-and propose a new class of molybdenum-containing nitrite reductases.
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The flavoprotein domain binds the cofactor FAD and includes a binding site for NADPH.
“The transmembrane domain includes four conserved histidines that serve as binding sites for two heme moieties bound between helices III and V (288, 613), and the flavoprotein domain binds the cofactor FAD and includes a binding site for NADPH (49, 480, 613, 980).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [613]
The transmembrane domain includes four conserved histidines that serve as binding sites for two heme moieties bound between helices III and V.
“The transmembrane domain includes four conserved histidines that serve as binding sites for two heme moieties bound between helices III and V (288, 613), and the flavoprotein domain binds the cofactor FAD and includes a binding site for NADPH (49, 480, 613, 980).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [613]
The crystal structure of NOX5 has been determined and is consistent with the presence of six transmembrane α helices with five connecting loops.
“Recently, the crystal structure of a NOX core subunit (NOX5) has been determined (613). This structure is consistent with previous evidence suggesting the presence of six transmembrane α helices with five connecting loops (FIGURE 7) (613).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [613]
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Cites
Structural and Functional Aspects of Metal Sites in Biology
Holm, R. H., Kennepohl, P., & Solomon, E. I. (1996) · Chemical Reviews · doi:10.1021/cr9500390 · Cited by 2,536 · see citing works
Fundamentals of Enzyme Kinetics
Cornish-Bowden, A. J. (1979) · Elsevier eBooks · doi:10.1016/c2013-0-04130-8 · Cited by 2,079 · see citing works
The mononuclear molybdenum enzymes
Hille, R., Hall, J., & Basu, P. (2014) · Chemical Reviews · doi:10.1021/cr400443z · Cited by 1,738 · see citing works
The Mononuclear Molybdenum Enzymes
Hille, R. (1996) · Chemical Reviews · doi:10.1021/cr950061t · Cited by 1,501 · see citing works
Stamler (2001) · doi:10.1016/s0092-8674(01)00495-0 · Cited by 1,261 · see citing works
Metal-centered oxygen atom transfer reactions
Holm, R. H. (1987) · Chemical Reviews · doi:10.1021/cr00082a005 · Cited by 957 · see citing works
Molybdenum cofactors, enzymes and pathways
Schwarz, G., Mendel, R. R., & Ribbe, M. W. (2009) · Nature · doi:10.1038/nature08302 · Cited by 872 · see citing works
Enroth, C., Eger, B. T., Okamoto, K., Nishino, T., Nishino, T., & Pai, E. F. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.20.10723 · Cited by 733 · see citing works
Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver
Duranski, M. R., Greer, J. J. M., Dejam, A., Jaganmohan, S., Hogg, N., Langston, W., Patel, R. P., Yet, S.-F., Wang, X., Kevil, C. G., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci22493 · Cited by 674 · see citing works
Fundamentals of enzyme kinetics
(1996) · Choice Reviews Online · doi:10.5860/choice.33-4507 · Cited by 658 · see citing works
Nitrate and nitrite in biology, nutrition and therapeutics
Lundberg, J. O., Gladwin, M. T., Ahluwalia, A., Benjamin, N., Bryan, N. S., Butler, A., Cabrales, P., Fago, A., Feelisch, M., Ford, P. C., et al. (2009) · Nature Chemical Biology · doi:10.1038/nchembio.260 · Cited by 617 · see citing works
Webb, A., Bond, R., McLean, P., Uppal, R., Benjamin, N., & Ahluwalia, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402927101 · Cited by 608 · see citing works
Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., & Blake, D. R. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00430-x · Cited by 491 · see citing works
Nitrite as Regulator of Hypoxic Signaling in Mammalian Physiology
van Faassen, E. E., Bahrami, S., Feelisch, M., Hogg, N., Kelm, M., Kim‐Shapiro, D. B., Kozlov, A. V., Li, H., Lundberg, J. O., Mason, R., et al. (2009) · Medicinal Research Reviews · doi:10.1002/med.20151 · Cited by 435 · see citing works
Molybdenum and tungsten in biology
Hille, R. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(02)02107-2 · Cited by 430 · see citing works
Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase
Godber, B. L. J., Doel, J. J., Sapkota, G. P., Blake, D. R., Stevens, C. R., Eisenthal, R., & Harrison, R. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.11.7757 · Cited by 411 · see citing works
Massey, V., Komai, H., Palmer, G., & Elion, G. B. (1970) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)63065-0 · Cited by 380 · see citing works
On the Mechanism of Inactivation of Xanthine Oxidase by Cyanide
Massey, V., & Edmondson, D. E. (1970) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)62575-x · Cited by 368 · see citing works
A comparison of the specificities of xanthine oxidase and aldehyde oxidase
Krenitsky, T. A., Neil, S. M., Elion, G. B., & Hitchings, G. H. (1972) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(72)90078-1 · Cited by 341 · see citing works
NO Generation From Nitrite and Its Role in Vascular Control
Lundberg, J. O., & Weitzberg, E. (2005) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000161048.72004.c2 · Cited by 341 · see citing works
The Mechanism of Action of Xanthine Oxidase
Olson, J. S., Ballou, D. P., Palmer, G., & Massey, V. (1974) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)42428-9 · Cited by 331 · see citing works
Molybdenum-containing hydroxylases
Hille, R. (2004) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2004.08.012 · Cited by 319 · see citing works
Kone, B. C., Kuncewicz, T., Zhang, W., & Yu, Z.-Y. (2003) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00048.2003 · Cited by 305 · see citing works
Okamoto, K., Matsumoto, K., Hille, R., Eger, B. T., Pai, E. F., & Nishino, T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400973101 · Cited by 286 · see citing works
NO-mediated cytoprotection: Instant adaptation to oxidative stress in bacteria
Gusarov, I., & Nudler, E. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504307102 · Cited by 282 · see citing works
Characterization of the Magnitude and Kinetics of Xanthine Oxidase-catalyzed Nitrite Reduction
Li, H., Samouilov, A., Liu, X., & Zweier, J. L. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011648200 · Cited by 280 · see citing works
Nitric Oxide Production from Nitrite Occurs Primarily in Tissues Not in the Blood
Li, H., Cui, H., Kundu, T. K., Alzawahra, W., & Zweier, J. L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801785200 · Cited by 269 · see citing works
Zhang, Z., Naughton, D., Winyard, P. G., Benjamin, N., Blake, D. R., & Symons, M. C. R. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9226 · Cited by 246 · see citing works
The prokaryotic complex iron–sulfur molybdoenzyme family
Rothery, R. A., Workun, G. J., & Weiner, J. H. (2007) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2007.09.002 · Cited by 224 · see citing works
An Electron Spin Resonance Study of Some Complexes of Iron, Nitric Oxide, and Anionic Ligands
McDonald, C. C., Phillips, W. D., & Mower, H. F. (1965) · Journal of the American Chemical Society · doi:10.1021/ja01093a007 · Cited by 192 · see citing works
Fridovich, I., & Handler, P. (1962) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)60393-x · Cited by 189 · see citing works
Mammalian aldehyde oxidases: genetics, evolution and biochemistry
Garattini, E., Fratelli, M., & Terao, M. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7398-y · Cited by 188 · see citing works
Feng, C., Tollin, G., & Enemark, J. H. (2007) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2007.03.006 · Cited by 185 · see citing works
Li, H., Samouilov, A., Liu, X., & Zweier, J. L. (2003) · Biochemistry · doi:10.1021/bi026385a · Cited by 180 · see citing works
Studies on the oxidative half-reaction of xanthine oxidase.
Hille, R., & Massey, V. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52512-1 · Cited by 161 · see citing works
Bacterial Nitric-oxide Synthases Operate without a Dedicated Redox Partner
Gusarov, I., Starodubtseva, M., Wang, Z.-Q., McQuade, L. E., Lippard, S. J., Stuehr, D. J., & Nudler, E. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m710178200 · Cited by 161 · see citing works
NO generation from inorganic nitrate and nitrite: Role in physiology, nutrition and therapeutics
Lundberg, J. O., & Weitzberg, E. (2009) · Archives of Pharmacal Research · doi:10.1007/s12272-009-1803-z · Cited by 153 · see citing works
Characterization of the effects of oxygen on xanthine oxidase-mediated nitric oxide formation
Li, H., Samouilov, A., Liu, X., & Zweier, J. L. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m314336200 · Cited by 146 · see citing works
Electron spin resonance of iron-nitric oxide complexes with amino acids, peptides and proteins
Woolum, J. C., Tiezzi, E., & Commoner, B. (1968) · Biochimica et Biophysica Acta (BBA) - Protein Structure · doi:10.1016/0005-2795(68)90204-3 · Cited by 143 · see citing works
Endothelial nitric oxide synthase reduces nitrite anions to NO under anoxia
Gautier, C., van Faassen, E., Mikula, I., Martasek, P., & Slama-Schwok, A. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.01.031 · Cited by 143 · see citing works
Baker, J. E., Su, J., Fu, X., Hsu, A., Gross, G. J., Tweddell, J. S., & Hogg, N. (2007) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2007.07.057 · Cited by 137 · see citing works
Direct measurement of nitric oxide generation from nitric oxide synthase
Xia, Y., & Zweier, J. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12705 · Cited by 136 · see citing works
Stiefel, E. I. (1973) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.70.4.988 · Cited by 132 · see citing works
Mechanisms of nitrite reduction to nitric oxide in the heart and vessel wall
Zweier, J. L., Li, H., Samouilov, A., & Liu, X. (2010) · Nitric Oxide · doi:10.1016/j.niox.2009.12.004 · Cited by 132 · see citing works
Structure and Function of Xanthine Oxidoreductase
Hille, R. (2006) · European Journal of Inorganic Chemistry · doi:10.1002/ejic.200600087 · Cited by 131 · see citing works
Li, H., Kundu, T. K., & Zweier, J. L. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.019125 · Cited by 126 · see citing works
Okamoto, K., Eger, B. T., Nishino, T., PAI, E. F., & Nishino, T. (2008) · Nucleosides Nucleotides & Nucleic Acids · doi:10.1080/15257770802146577 · Cited by 117 · see citing works
Molybdenum and tungsten enzymes: the xanthine oxidase family
Brondino, C. D., Romão, M. J., Moura, I., & Moura, J. J. G. (2006) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2006.01.034 · Cited by 109 · see citing works
Self-citationHarlan, E. W., Berg, J. M., & Holm, R. H. (1986) · Journal of the American Chemical Society · doi:10.1021/ja00282a025 · Cited by 98 · see citing works
Structure refinement of the aldehyde oxidoreductase from Desulfovibrio gigas (MOP) at 1.28 Å
Rebelo, J., Dias, J., Huber, R., Moura, J. J. G., & Romão, M. J. (2001) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s007750100255 · Cited by 95 · see citing works
Self-citationSubstrate Orientation in Xanthine Oxidase
Pauff, J. M., Zhang, J., Bell, C. E., & Hille, R. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m707918200 · Cited by 90 · see citing works
Schultz, B. E., Hille, R., & Holm, R. H. (1995) · Journal of the American Chemical Society · doi:10.1021/ja00107a031 · Cited by 88 · see citing works
Molybdenum enzymes, cofactors, and systems: The chemical uniqueness of molybdenum
Burgmayer, S. J. N., & Stiefel, E. I. (1985) · Journal of Chemical Education · doi:10.1021/ed062p943 · Cited by 87 · see citing works
Mechanisms of inactivation of molybdoenzymes by cyanide.
Coughlan, M. P., Johnson, J. L., & Rajagopalan, K. V. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85792-7 · Cited by 82 · see citing works
The molybdenum iron-sulphur protein from Desulfovibrio gigas as a form of aldehyde oxidase
Turner, N. A., Barata, B., Bray, R. C., Deistung, J., LeGall, J., & Moura, J. J. G. (1987) · Biochemical Journal · doi:10.1042/bj2430755 · Cited by 72 · see citing works
Self-citationBarata, B. A. S., LeGall, J., & Moura, J. J. G. (1993) · Biochemistry · doi:10.1021/bi00094a012 · Cited by 62 · see citing works
Self-citationA molybdenum-containing iron-sulphur protein from desulphovibrio gigas
Moura, J. J. G., Xavier, A. V., Bruschi, M., LeGall, J., Hall, D. O., & Cammack, R. (1976) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(76)80201-x · Cited by 61 · see citing works
Self-citationHawkes, T. R., George, G. N., & Bray, R. C. (1984) · Biochemical Journal · doi:10.1042/bj2180961 · Cited by 55 · see citing works
Brondino, C. D., Rivas, M. G., Romão, M. J., Moura, J. J. G., & Moura, I. (2006) · Accounts of Chemical Research · doi:10.1021/ar050104k · Cited by 49 · see citing works
Self-citationMaia, L. B., Duarte, R. O., Freire, A. P., Moura, J. J. G., & Mira, L. (2007) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-007-0229-7 · Cited by 48 · see citing works
Self-citationA new non-functional form of milk xanthine oxidase containing stable quinquivalent molybdenum
Lowe, D. J., Barber, M. J., Pawlik, R. T., & Bray, R. C. (1976) · Biochemical Journal · doi:10.1042/bj1550081 · Cited by 42 · see citing works
Bursakov, S. A., Gavel, O. Y., Rocco, G. D., Lampreia, J., Calvete, J. J., Pereira, A. S., Moura, J. J. G., & Moura, I. (2003) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2003.12.002 · Cited by 35 · see citing works
Self-citationSantos‐Silva, T., Ferroni, F. M., Thapper, A., Marangon, J., González, P. J., Rizzi, A. C., Moura, I., Moura, J. J. G., Romão, M. J., & Brondino, C. D. (2009) · Journal of the American Chemical Society · doi:10.1021/ja809448r · Cited by 32 · see citing works
Self-citationStudies of the reductive half-reaction of milk xanthine dehydrogenase.
Hunt, J., & Massey, V. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32253-6 · Cited by 31 · see citing works
Tungsten-Dependent Aldehyde Oxidoreductase: A New Family of Enzymes Containing the Pterin Cofactor
Roy, R., & Adams, M. W. W. (2002) · CRC Press eBooks · doi:10.1201/9780203909331-28 · Cited by 31 · see citing works
Dixon, M., & Thurlow, S. (1924) · Biochemical Journal · doi:10.1042/bj0180989 · Cited by 30 · see citing works
Rajapakshe, A., Snyder, R. A., Astashkin, A. V., Bernardson, P., Evans, D. J., Young, C. G., Evans, D. H., & Enemark, J. H. (2009) · Inorganica Chimica Acta · doi:10.1016/j.ica.2009.05.040 · Cited by 30 · see citing works
Rivas, M. G., Carepo, M. S. P., Mota, C., Korbas, M., Durand, M.-C., Lopes, A. T., Brondino, C. D., Pereira, A. S., George, G. N., Dolla, A. R., et al. (2009) · Biochemistry · doi:10.1021/bi801773t · Cited by 27 · see citing works
Self-citationHowes, B. D., Pinhal, N. M., Turner, N. A., Bray, R. C., Anger, G., Ehrenberg, A., Raynor, J. B., & Lowe, D. J. (1990) · Biochemistry · doi:10.1021/bi00478a002 · Cited by 23 · see citing works
Fridovich, I., & Handler, P. (1957) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)70690-x · Cited by 21 · see citing works
Modelling the Electron‐Transfer Complex Between Aldehyde Oxidoreductase and Flavodoxin
Krippahl, L., Palma, P. N., Moura, I., & Moura, J. J. G. (2006) · European Journal of Inorganic Chemistry · doi:10.1002/ejic.200600418 · Cited by 13 · see citing works
Self-citation
Flagged first, then by citations
1 of the 72 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation
Tejero, J., Shiva, S., & Gladwin, M. T. (2019) · Physiological Reviews · doi:10.1152/physrev.00036.2017 · Cited by 541 · see citing works
Nitrate and periplasmic nitrate reductases
Sparacino-Watkins, C., Stolz, J. F., & Basu, P. (2014) · Chem. Soc. Rev. · doi:10.1039/c3cs60249d · Cited by 426 · see citing works
Maia, L. B., & Moura, J. J. G. (2014) · Chemical Reviews · doi:10.1021/cr400518y · Cited by 401 · see citing works
Self-citationConnecting the Chemical and Biological Properties of Nitric Oxide
Toledo, J. C., & Augusto, O. (2012) · Chemical Research in Toxicology · doi:10.1021/tx300042g · Cited by 285 · see citing works
Lehnert, N., Kim, E., Dong, H. T., Harland, J. B., Hunt, A. P., Manickas, E. C., Oakley, K. M., Pham, J., Reed, G. C., & Alfaro, V. S. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00253 · Cited by 277 · see citing works
Cantu-Medellin, N., & Kelley, E. E. (2013) · Redox Biology · doi:10.1016/j.redox.2013.05.002 · Cited by 237 · see citing works
Sparacino-Watkins, C. E., Tejero, J., Sun, B., Gauthier, M. C., Thomas, J., Ragireddy, V., Merchant, B. A., Wang, J., Azarov, I., Basu, P., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.555177 · Cited by 169 · see citing works
Nitrite and nitrate chemical biology and signalling
DeMartino, A. W., Kim‐Shapiro, D. B., Patel, R. P., & Gladwin, M. T. (2018) · British Journal of Pharmacology · doi:10.1111/bph.14484 · Cited by 156 · see citing works
Bachschmid, M. M., Schildknecht, S., Matsui, R., Zee, R. S., Haeussler, D. J., Cohen, R. A., Pimental, D. R., & van der Loo, B. (2012) · Annals of Medicine · doi:10.3109/07853890.2011.645498 · Cited by 154 · see citing works
Cantú‐Medellín, N., & Kelley, E. E. (2013) · Nitric Oxide · doi:10.1016/j.niox.2013.02.081 · Cited by 148 · see citing works
Woessner, M., Smoliga, J. M., Tarzia, B., Stabler, T., Van Bruggen, M., & Allen, J. D. (2016) · Nitric Oxide · doi:10.1016/j.niox.2016.01.002 · Cited by 137 · see citing works
Wei, L., Derrien, B., Gautier, A., Houille-Vernes, L., Boulouis, A., Saint‐Marcoux, D., Malnoë, A., Rappaport, F., de Vitry, C., Vallon, O., et al. (2014) · The Plant Cell · doi:10.1105/tpc.113.120121 · Cited by 125 · see citing works
Nitrite Reduction and Cardiovascular Protection
Omar, S. A., & Webb, A. J. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.01.012 · Cited by 121 · see citing works
Al‐Shehri, S. S., Knox, C. L., Liley, H. G., Cowley, D. M., Wright, J. D., Henman, M. G., Hewavitharana, A. K., Charles, B. G., Shaw, P. N., Sweeney, E. L., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135047 · Cited by 112 · see citing works
Skeletal muscle as an endogenous nitrate reservoir
Piknova, B., Park, J. W., Swanson, K. M., Dey, S., Noguchi, C. T., & Schechter, A. N. (2015) · Nitric Oxide · doi:10.1016/j.niox.2015.02.145 · Cited by 108 · see citing works
Nishino, T., & Okamoto, K. (2014) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-014-1210-x · Cited by 99 · see citing works
Modulating endothelial nitric oxide synthase: a new cardiovascular therapeutic strategy
Zhang, Y., Janssens, S. P., Wingler, K., Schmidt, H. H. H. W., & Moens, A. L. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01315.2010 · Cited by 96 · see citing works
Chemical Nature and Reaction Mechanisms of the Molybdenum Cofactor of Xanthine Oxidoreductase
Okamoto, K., Kusano, T., & Nishino, T. (2013) · Current Pharmaceutical Design · doi:10.2174/1381612811319140010 · Cited by 91 · see citing works
Nitrite reduction by molybdoenzymes: a new class of nitric oxide-forming nitrite reductases
Maia, L. B., & Moura, J. J. G. (2015) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-014-1234-2 · Cited by 86 · see citing works
Self-citationA new paradigm for XOR-catalyzed reactive species generation in the endothelium
Kelley, E. E. (2015) · Pharmacological Reports · doi:10.1016/j.pharep.2015.05.004 · Cited by 78 · see citing works
Castiglione, N., Rinaldo, S., Giardina, G., Stelitano, V., & Cutruzzolà, F. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4196 · Cited by 79 · see citing works
Maia, L. B., Pereira, V., Mira, L., & Moura, J. J. G. (2014) · Biochemistry · doi:10.1021/bi500987w · Cited by 62 · see citing works
Self-citationMechanisms impairing blood pressure responses to nitrite and nitrate
Oliveira‐Paula, G. H., Pinheiro, L. C., & Tanus-Santos, J. E. (2019) · Nitric Oxide · doi:10.1016/j.niox.2019.01.015 · Cited by 60 · see citing works
Maia, L. B., & Moura, J. J. G. (2018) · Redox Biology · doi:10.1016/j.redox.2018.08.020 · Cited by 56 · see citing works
Self-citationTherapeutic Potential of the Nitrite-Generated NO Pathway in Vascular Dysfunction
Madigan, M. C., & Zuckerbraun, B. S. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00174 · Cited by 51 · see citing works
Oxygen Regulates Tissue Nitrite Metabolism
Curtis, E., Hsu, L. L., Noguchi, A. C., Geary, L., & Shiva, S. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4242 · Cited by 46 · see citing works
Yang, J., Giles, L. J., Ruppelt, C., Mendel, R. R., Bittner, F., & Kirk, M. L. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b01112 · Cited by 43 · see citing works
Roles of Molybdenum in Plants and Improvement of Its Acquisition and Use Efficiency
Tejada‐Jiménez, M., Chamizo‐Ampudia, A., Llamas, Á., Galván, A., & Fernández, E. M. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-812104-7.00009-5 · Cited by 44 · see citing works
Nitric Oxide Remodels the Photosynthetic Apparatus upon S-Starvation in Chlamydomonas reinhardtii
de Mia, M., Lemaire, S. D., Choquet, Y., & Wollman, F.-A. (2018) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.01164 · Cited by 42 · see citing works
From the Eukaryotic Molybdenum Cofactor Biosynthesis to the Moonlighting Enzyme mARC
Tejada‐Jiménez, M., Chamizo‐Ampudia, A., Calatrava, V., Galván, A., Fernández, E. M., & Llamas, Á. (2018) · Molecules · doi:10.3390/molecules23123287 · Cited by 38 · see citing works
Endogenous Hemoprotein-Dependent Signaling Pathways of Nitric Oxide and Nitrite
Dent, M. R., DeMartino, A. W., Tejero, J., & Gladwin, M. T. (2021) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.1c01048 · Cited by 35 · see citing works
MacGregor, B. J., Biddle, J. F., Harbort, C. J., Matthysse, A. G., & Teske, A. (2013) · Marine Genomics · doi:10.1016/j.margen.2013.08.001 · Cited by 35 · see citing works
Nitrite-stimulated Gastric Formation of S-nitrosothiols As An Antihypertensive Therapeutic Strategy
Oliveira‐Paula, G. H., & Tanus-Santos, J. E. (2018) · Current Drug Targets · doi:10.2174/1389450119666180816120816 · Cited by 33 · see citing works
Liu, T., Schroeder, H. J., Power, G. G., & Blood, A. B. (2022) · Redox Biology · doi:10.1016/j.redox.2022.102327 · Cited by 30 · see citing works
Ledo, A., Lourenço, C. F., Cadenas, E., Barbosa, R. M., & Laranjinha, J. A. N. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.11.005 · Cited by 30 · see citing works
Sekine, M., Okamoto, K., & Ichida, K. (2021) · Biomedicines · doi:10.3390/biomedicines9111723 · Cited by 30 · see citing works
Stefano, G. B., & Kream, R. M. (2011) · Medical Science Monitor · doi:10.12659/msm.881972 · Cited by 27 · see citing works
Molybdenum-containing nitrite reductases: Spectroscopic characterization and redox mechanism
Wang, J., Keceli, G., Cao, R., Su, J., & Mi, Z. (2016) · Redox Report · doi:10.1080/13510002.2016.1206175 · Cited by 24 · see citing works
Nitric oxide and nitrite-based therapeutic opportunities in intimal hyperplasia
Alef, M. J., Tzeng, E., & Zuckerbraun, B. S. (2012) · Nitric Oxide · doi:10.1016/j.niox.2012.03.014 · Cited by 20 · see citing works
Nitrite Reductases in Biomedicine: From Natural Enzymes to Artificial Mimics
Zhu, S., Liu, Z., Hu, B., Feng, Y., & Pan, G. (2025) · Research · doi:10.34133/research.0710 · Cited by 20 · see citing works
Structure, Function, and Mechanism of Pyranopterin Molybdenum and Tungsten Enzymes
Ingersol, L. J., & Kirk, M. L. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-409547-2.14929-7 · Cited by 16 · see citing works
Maia, L. B., & Moura, J. J. G. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3600-7_8 · Cited by 17 · see citing works
Self-citation9. Molybdenum and Tungsten Cofactors and the Reactions They Catalyze
Kirk, M. L., & Khadanand, K. C. (2020) · De Gruyter eBooks · doi:10.1515/9783110589757-015 · Cited by 16 · see citing works
Gomes, F., Maia, L. B., Cordas, C. M., Delerue-Matos, C. M., Moura, I., Moura, J. J. G., & Morais, S. (2018) · Electroanalysis · doi:10.1002/elan.201800421 · Cited by 16 · see citing works
Self-citationSemenova, A. D., Glazachev, Y. I., Slepneva, I. A., & Glupov, V. V. (2014) · Nitric Oxide · doi:10.1016/j.niox.2013.12.011 · Cited by 15 · see citing works
Paulo, L. L., Cruz, J. C., Zhuge, Z., Carvalho‐Galvão, A., Brandão, M. C. R., Diniz, T. F., Haworth, S. M., de Athayde-Filho, P. F., Lemos, V. S., Lundberg, J. O., et al. (2017) · Redox Biology · doi:10.1016/j.redox.2017.12.004 · Cited by 15 · see citing works
Therapeutic Implications of Nitrite in Hypertension
Ling, W. C., Mustafa, M. R., & Murugan, D. D. (2019) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000000771 · Cited by 14 · see citing works
Advancing Our Understanding of Pyranopterin-Dithiolene Contributions to Moco Enzyme Catalysis
Burgmayer, S. J. N., & Kirk, M. L. (2023) · Molecules · doi:10.3390/molecules28227456 · Cited by 14 · see citing works
Reactive Oxygen Species and the Cardiovascular System
Montezano, A. C. I., & Touyz, R. M. (2012) · Colloquium Series on Integrated Systems Physiology From Molecule to Function · doi:10.4199/c00043ed1v01y201112isp032 · Cited by 13 · see citing works
EPR Spectroscopy on Mononuclear Molybdenum-Containing Enzymes
Maia, L. B., Moura, I., & Moura, J. J. G. (2017) · Biological magnetic resonance · doi:10.1007/978-3-319-59100-1_4 · Cited by 10 · see citing works
Self-citationModulation of oxidative neurometabolism in ischemia/reperfusion by nitrite
Dias, C., Lourenço, C. F., Laranjinha, J. A. N., & Ledo, A. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.11.021 · Cited by 10 · see citing works
Oxidative Stress and Cardiovascular Diseases
Hristova, M., & Penev, M. (2014) · Trakia Journal of Sciences · doi:10.15547/tjs.2014.03.012 · Cited by 9 · see citing works
Reactive Oxygen Species - Advances and Developments
Ahmad, R. (2023) · Biochemistry · doi:10.5772/intechopen.107774 · Cited by 9 · see citing works
Galinato, M. G. I., Fogle, R. S., Stetz, A., & Galan, J. F. (2015) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2015.10.010 · Cited by 8 · see citing works
Bringing Nitric Oxide to the Molybdenum World—A Personal Perspective
Maia, L. B. (2023) · Molecules · doi:10.3390/molecules28155819 · Cited by 7 · see citing works
Self-citationSeychell, B. C., Vella, M., Hunter, G. J., & Hunter, T. (2023) · Biochemistry · doi:10.5772/intechopen.112498 · Cited by 6 · see citing works
A terpyridine-based copper complex for electrochemical reduction of nitrite to nitric oxide
Biswas, J., Sanden, S., Bhardwaj, P., Siegmund, D., Kumar, P., & Apfel, U. (2024) · Dalton Transactions · doi:10.1039/d4dt02777a · Cited by 5 · see citing works
Buerk, D. G., Liu, Y., Zaccheo, K. A., Barbee, K. A., & Jaron, D. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.01053 · Cited by 5 · see citing works
Gupta, N., Ram, H., & Çakmak, İ. (2022) · Springer eBooks · doi:10.1007/978-981-16-3280-8_20 · Cited by 5 · see citing works
Nitric Oxide and Related Aspects Underlying Angina
Restini, C. B. A., & Gonçalves, L. F. (2017) · The Open Cardiovascular Medicine Journal · doi:10.2174/1874192401711010033 · Cited by 5 · see citing works
Mononuclear Molybdenum-Containing Enzymes
Maia, L. B., & Moura, J. J. G. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-409547-2.13932-0 · Cited by 4 · see citing works
Self-citationMolybdenum Cofactor Biosynthesis and Cross Talk with Iron–Sulfur
Bittner, F., & Mendel, R. R. (2004) · Encyclopedia of Inorganic and Bioinorganic Chemistry · doi:10.1002/9781119951438.eibc2150 · Cited by 4 · see citing works
Bioelectrosynthesis of Signaling Molecules for Selective Modulation of Cell Signaling
Lee, M., Lee, J., Kim, Y., Lee, C., Oh, S. Y., Kim, J., & Park, J. (2025) · Angewandte Chemie International Edition · doi:10.1002/anie.202508192 · Cited by 3 · see citing works
Li, F., Talipov, M. R., Dong, C., Bali, S., & Ding, K. (2017) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-017-1518-4 · Cited by 3 · see citing works
Masero, F., & Mougel, V. (2023) · Chemical Communications · doi:10.1039/d3cc00572k · Cited by 3 · see citing works
Zahedi, S. M., Marjani, M., Rostami-Ahmadvandi, H., Alemian, M., Ikram, M., Gholami, R., Sarikhani, S., Ludwików, A., & Carillo, P. (2024) · South African Journal of Botany · doi:10.1016/j.sajb.2024.09.030 · Cited by 3 · see citing works
Liang, J., Huang, T., Li, J., Yang, Z., Ni, J., & Wang, Y. (2026) · RSC Advances · doi:10.1039/d6ra00317f · Cited by 2 · see citing works
Structure and function of periplasmic nitrate reductase
Mongkonpruthangkoon, C., Giri, N. C., & Basu, P. (2026) · Biochemical Society Transactions · doi:10.1042/bst20250033 · Cited by 2 · see citing works
Bovine xanthine oxidase electrocatalysis: substrate oxidation and its role in nitrite reduction
Giang, P. D., Niks, D., Hille, R., & Bernhardt, P. V. (2026) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-026-02146-z · Cited by 1 · see citing works
Inorganic nitrite and conduit artery function
Omar, S. A. (2015)
Chen, X.-M., Chang, D.-M., & Chen, C. (2022) · Sensors and Materials · doi:10.18494/sam4024
Bioelectrosynthesis of Signaling Molecules for Selective Modulation of Cell Signaling
Lee, M., Lee, J., Kim, Y., Lee, C., Oh, S. Y., Kim, J., & Park, J. (2025) · Angewandte Chemie · doi:10.1002/ange.202508192
Castello, P. R., Ball, K. A., & Poyton, R. Ο. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.09.743791
- Authors
- Maia, L. B., & Moura, J. J. G.
- Affiliations
- Universidade Nova de Lisboa (PT)
- Corresponding author
- Moura, José J. G.
- ORCID
- Moura, José J. G.
- Venue
- JBIC Journal of Biological Inorganic Chemistry
- Published
- 2010-12-19
- Volume
- 16
- Issue
- 3
- Pages
- 443-460
- ISSN
- 0949-8257 (ISSN-L)
- 1432-1327
- OpenAlex
- W1971908845
- Cited by
- 75
- References
- 72
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 4 · 2021: 3 · 2020: 3 · 2019: 2 · 2018: 9 · 2017: 6 · 2016: 3 · 2015: 7 · 2014: 9 · 2013: 6 · 2012: 5
- FWCI
- 2.09
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- JBIC Journal of Biological Inorganic Chemistry (publishedVersion)
- PubMed (publishedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, other-oa)
- Funders
- Ministério da Ciência, Tecnologia e Ensino Superior
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
- Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Keywords
- nitrite reduction, xanthine oxidase, aldehyde oxidoreductase, Desulfovibrio gigas, molybdenum enzymes, nitric oxide radical, nitrite reductase, molybdenum oxidation state, enzyme kinetics, nitrite binding
- MeSH terms
- Aldehyde Oxidoreductases, Electron Spin Resonance Spectroscopy, Models, Biological, Nitrite Reductases, Nitrites, Oxidation-Reduction, Xanthine Oxidase
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