Molybdenum and tungsten oxygen transferases – structural and functional diversity within a common active site motif
Abstract
Molybdenum and tungsten are the only second and third-row transition elements with a known function in living organisms. The molybdenum and tungsten enzymes show common structural features, with the metal being bound by a pyranopterin-dithiolene cofactor called molybdopterin. They catalyze a variety of oxygen transferase reactions coupled with two-electron redox chemistry in which the metal cycles between the +6 and +4 oxidation states usually with water, either product or substrate, providing the oxygen. The functional roles filled by the molybdenum and tungsten enzymes are diverse; for example, they play essential roles in microbial respiration, in the uptake of nitrogen in green plants, and in human health. Together, the enzymes form a superfamily which is among the most prevalent known, being found in all kingdoms of life. This review discusses what is known of the active site structures and the mechanisms, together with some recent insights into the evolution of these important enzyme systems.
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Tungsten is used by primitive anaerobic prokaryotes and mostly filled roles now played by Mo.
“Tungsten is used by primitive anaerobic prokaryotes and mostly filled roles now played by Mo (Williams et al., 2002;Pushie et al., 2014).”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Pushie et al., 2014
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The metabolic and molecular bases of inherited disease
Chen, Y.-T. (2001) · Medical Entomology and Zoology · Cited by 6,928 · see citing works
Structural basis of biological nitrogen fixation
Rees, D. C., Tezcan, F. A., Haynes, C. A., Walton, M. Y., Andrade, S. L. A., Einsle, O., & Howard, J. B. (2005) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2004.1539 · Cited by 1,121 · see citing works
How do bacterial cells ensure that metalloproteins get the correct metal?
Waldron, K. J., & Robinson, N. J. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro2057 · Cited by 835 · 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
Boyington, J. C., Gladyshev, V. N., Khangulov, S. V., Stadtman, T. C., & Sun, P. D. (1997) · Science · doi:10.1126/science.275.5304.1305 · Cited by 596 · see citing works
Structure of a Hyperthermophilic Tungstopterin Enzyme, Aldehyde Ferredoxin Oxidoreductase
Chan, M. K., Mukund, S., Kletzin, A., Adams, M. W. W., & Rees, D. C. (1995) · Science · doi:10.1126/science.7878465 · Cited by 544 · see citing works
Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A
Bertero, M. G., Rothery, R. A., Palak, M., Hou, C., Lim, D., Blasco, F., Weiner, J. H., & Strynadka, N. C. J. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb969 · Cited by 494 · see citing works
Zinoni, F., Birkmann, A., Stadtman, T. C., & Böck, A. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.13.4650 · Cited by 486 · see citing works
Molecular Basis of Sulfite Oxidase Deficiency from the Structure of Sulfite Oxidase
Kisker, C., Schindelin, H., Pacheco, A. A., Wehbi, W. A., Garrett, R. M., Rajagopalan, K. V., Enemark, J. H., & Rees, D. C. (1997) · Cell · doi:10.1016/s0092-8674(00)80488-2 · Cited by 485 · see citing works
Catalysis at a dinuclear [CuSMo(O)OH] cluster in a CO dehydrogenase resolved at 1.1-Å resolution
Dobbek, H., Gremer, L., Kiefersauer, R. A., Huber, R., & Meyer, O. O. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.212640899 · Cited by 387 · see citing works
Chemical variations and regional diversity observed in MORB
Arévalo, R., & McDonough, W. F. (2009) · Chemical Geology · doi:10.1016/j.chemgeo.2009.12.013 · Cited by 374 · see citing works
Microbial metalloproteomes are largely uncharacterized
Cvetkovic, A., Menon, A. L., Thorgersen, M. P., Scott, J. W., Poole, F. L., Jenney, F. E., Lancaster, W. A., Praissman, J. L., Shanmukh, S., Vaccaro, B. J., et al. (2010) · Nature · doi:10.1038/nature09265 · Cited by 363 · see citing works
Tungsten in biological systems
Kletzin, A., & Adams, M. W. W. (1996) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.1996.tb00226.x · Cited by 361 · see citing works
When did oxygenic photosynthesis evolve?
Buick, R. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0041 · Cited by 352 · see citing works
Hyperthermophiles in the history of life
STETTER, K. O. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1907 · Cited by 291 · see citing works
Johnson, J. L., Hainline, B. E., & Rajagopalan, K. V. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85945-8 · Cited by 279 · see citing works
Structural and metabolic relationship between the molybdenum cofactor and urothione.
Johnson, J. L., & Rajagopalan, K. V. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.22.6856 · Cited by 266 · see citing works
Dobbek, H., Gremer, L., Meyer, O. O., & Huber, R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.16.8884 · Cited by 255 · see citing works
Tomatsu, H., Takano, J., Takahashi, H., Watanabe‐Takahashi, A., Shibagaki, N., & Fujiwara, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706373104 · Cited by 248 · see citing works
The Continuing Puzzle of the Great Oxidation Event
Sessions, A. L., Doughty, D. M., Welander, P. V., Summons, R. E., & Newman, D. K. (2009) · Current Biology · doi:10.1016/j.cub.2009.05.054 · Cited by 232 · see citing works
Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism
Kuper, J., Llamas, Á., Hecht, H., Mendel, R. R., & Schwarz, G. (2004) · Nature · doi:10.1038/nature02681 · Cited by 215 · see citing works
Architecture of NarGH Reveals a Structural Classification of Mo-bisMGD Enzymes
Jormakka, M., Richardson, D. J., Byrne, B., & Iwata, S. (2004) · Structure · doi:10.1016/j.str.2003.11.020 · Cited by 212 · see citing works
Molybdoproteomes and Evolution of Molybdenum Utilization
Zhang, Y., & Gladyshev, V. N. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.03.051 · Cited by 194 · see citing works
THOMSON, A. J., & Gray, H. B. (1998) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(98)80056-2 · Cited by 191 · see citing works
Raaijmakers, H. C. A., Macieira, S., Dias, J. M. L., Teixeira, S. C. M., Bursakov, S. A., Huber, R., Moura, J. J. G., Moura, I., & Romão, M. J. (2002) · Structure · doi:10.1016/s0969-2126(02)00826-2 · Cited by 186 · see citing works
The involvement of molybdenum in life
Williams, R. J. P., & Fraústo da Silva, J. J. R. (2002) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2002.6518 · Cited by 181 · see citing works
Arsenite oxidase, an ancient bioenergetic enzyme.
Lebrun, É., Brugna, M., Baymann, F., Muller, D. A. E., Lièvremont, D., Lett, M., & Nitschke, W. (2003) · Molecular biology and evolution · doi:10.1093/molbev/msg071 · Cited by 179 · see citing works
Licht, S. L. (1988) · Journal of The Electrochemical Society · doi:10.1149/1.2095471 · Cited by 178 · see citing works
Molybdenum sites of sulfite oxidase and xanthine dehydrogenase. A comparison by EXAFS
Cramer, S. P., Wahl, R. C., & Rajagopalan, K. V. (1981) · Journal of the American Chemical Society · doi:10.1021/ja00416a005 · Cited by 177 · see citing works
Williams-Smith, D. L., Bray, R. C., Barber, M. J., Tsopanakis, A. D., & Vincent, S. P. (1977) · Biochemical Journal · doi:10.1042/bj1670593 · Cited by 175 · see citing works
Raaijmakers, H. C. A., & Romão, M. J. (2006) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-006-0129-2 · Cited by 167 · see citing works
X-ray-induced photo-chemistry and X-ray absorption spectroscopy of biological samples
George, G. N., Pickering, I. J., Pushie, M. J., Nienaber, K. H., Hackett, M. J., Ascone, I., Hedman, B., Hodgson, K. O., Aitken, J. B., Levina, A., et al. (2012) · Journal of Synchrotron Radiation · doi:10.1107/s090904951203943x · Cited by 163 · see citing works
Hydrocarbon oxidation by high-valent Group VI oxides
Rappé, A. K., & Goddard, W. A. (1982) · Journal of the American Chemical Society · doi:10.1021/ja00376a006 · Cited by 159 · see citing works
Fischer-Schrader, K., Barbier, G. G., Hecht, H. J., Mendel, R. R., Campbell, W. H., & Schwarz, G. (2005) · The Plant Cell · doi:10.1105/tpc.104.029694 · Cited by 157 · see citing works
Stallmeyer, B., Schwarz, G., Schulze, J., Nerlich, M. L., Reiss, J., Kirsch, J., & Mendel, R. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1333 · Cited by 155 · see citing works
MOLYBDENUM AND NITRATE REDUCTASE
Nicholas, D. J. D., & Nason, A. (1954) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)71275-1 · Cited by 148 · see citing works
Structure of the non-redox-active tungsten/[4Fe:4S] enzyme acetylene hydratase
Seiffert, G. B., Ullmann, G. M., Messerschmidt, A., Schink, B., Kroneck, P. M. H., & Einsle, O. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610407104 · Cited by 145 · see citing works
Wang, M., Jiang, Y.-Y., Kim, K. M., Qu, G., Ji, H.-F., Mittenthal, J. E., Zhang, H. Y., & Caetano‐Anollés, G. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq232 · Cited by 144 · see citing works
Khangulov, S. V., Gladyshev, V. N., Dismukes, G. C., & Stadtman, T. C. (1998) · Biochemistry · doi:10.1021/bi972177k · Cited by 141 · see citing works
A high-affinity molybdate transporter in eukaryotes
Tejada‐Jiménez, M., Llamas, Á., Sanz‐Luque, E., Galván, A., & Fernández, E. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704646104 · Cited by 141 · see citing works
Li, H., Temple, C. A., Rajagopalan, K. V., & Schindelin, H. (2000) · Journal of the American Chemical Society · doi:10.1021/ja000643e · Cited by 139 · see citing works
Leimkühler, S., Wuebbens, M. M., & Rajagopalan, K. V. (2010) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2010.12.003 · Cited by 136 · see citing works
Structure of the Molybdenum Site of Dimethyl Sulfoxide Reductase
George, G. N., Hilton, J. C., Temple, C. A., Prince, R. C., & Rajagopalan, K. V. (1999) · Journal of the American Chemical Society · doi:10.1021/ja982843k · Cited by 124 · see citing works
Inscore, F. E., McNaughton, R. L., Westcott, B. L., Helton, M. E., Jones, R. M., Dhawan, I. K., Enemark, J. H., & Kirk, M. L. (1999) · Inorganic Chemistry · doi:10.1021/ic981126o · Cited by 120 · see citing works
Schoepp‐Cothenet, B., van Lis, R., Philippot, P., Magalon, A., Russell, M. J., & Nitschke, W. (2012) · Scientific Reports · doi:10.1038/srep00263 · Cited by 119 · see citing works
Rosner, B. M., & Schink, B. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.20.5767-5772.1995 · Cited by 118 · see citing works
Algae and humans share a molybdate transporter
Tejada‐Jiménez, M., Galván, A., & Fernández, E. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100700108 · Cited by 117 · see citing works
Gnida, M., Ferner, R., Gremer, L., Meyer, O. O., & Meyer‐Klaucke, W. (2002) · Biochemistry · doi:10.1021/bi026514n · Cited by 117 · see citing works
Najmudin, S., González, P. J., Trincão, J., Coelho, C., Mukhopadhyay, A., Cerqueira, N. M. F. S. A., Romão, C. C., Moura, I., Moura, J. J. G., Brondino, C. D., et al. (2008) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-008-0359-6 · Cited by 116 · see citing works
The role of metal ions in RNA catalysis
Fedor, M. J. (2002) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(02)00324-x · Cited by 113 · see citing works
Primary haematite formation in an oxygenated sea 3.46 billion years ago
Hoashi, M., Bevacqua, D., Otake, T., Watanabe, Y., Hickman, A., Utsunomiya, S., & Ohmoto, H. (2009) · Nature Geoscience · doi:10.1038/ngeo465 · Cited by 105 · see citing works
Li, H., Temple, K. L., Rajagopalan, K. V., & Schindelin, H. (2000) · Worldwide Protein Data Bank · doi:10.2210/pdb1eu1/pdb · Cited by 104 · see citing works
George, G. N., Garrett, R. M., Prince, R. C., & Rajagopalan, K. V. (1996) · Journal of the American Chemical Society · doi:10.1021/ja961218h · Cited by 100 · see citing works
Neoarchaean seawater sulphate concentrations from sulphur isotopes in massive sulphide ore
Jamieson, J. W., Wing, B. A., Farquhar, J. D., & Hannington, M. D. (2012) · Nature Geoscience · doi:10.1038/ngeo1647 · Cited by 100 · see citing works
Molybdenum cofactor biosynthesis in plants and humans
Mendel, R. R., & Schwarz, G. (2011) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2011.01.054 · Cited by 99 · see citing works
Pyranopterin conformation defines the function of molybdenum and tungsten enzymes
Rothery, R. A., Stein, B. W., Solomonson, M., Kirk, M. L., & Weiner, J. H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200671109 · Cited by 98 · see citing works
Reversible Biological Birch Reduction at an Extremely Low Redox Potential
Kung, J. W., Baumann, S., von Bergen�, M., Müller, M., Hagedoorn, P., Hagen, W. R., & Boll, M. (2010) · Journal of the American Chemical Society · doi:10.1021/ja103448u · Cited by 98 · see citing works
Tungsten in north pacific waters
Sohrin, Y., Isshiki, K., Kuwamoto, T., & Nakayama, E. (1987) · Marine Chemistry · doi:10.1016/0304-4203(87)90051-x · Cited by 92 · see citing works
Schwarz, G., Schulze, J., Bittner, F., Eilers, T., Kuper, J., Bollmann, G., Nerlich, A., Brinkmann, H., & Mendel, R. R. (2000) · The Plant Cell · doi:10.1105/tpc.12.12.2455 · Cited by 90 · see citing works
A Novel Protein-Bound Copper−Molybdenum Cluster
George, G. N., Pickering, I. J., Yu, E. Y., Prince, R. C., Bursakov, S. A., Gavel, O. Y., Moura, I., & Moura, J. J. G. (2000) · Journal of the American Chemical Society · doi:10.1021/ja000955h · Cited by 89 · see citing works
Spectroscopic studies of molybdenum and tungsten enzymes
Pushie, M. J., & George, G. N. (2011) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2011.01.056 · Cited by 86 · see citing works
Tungsten enriched in submarine hydrothermal fluids
Kishida, K., Sohrin, Y., Okamura, K., & Ishibashi, J.-I. (2004) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2004.03.034 · Cited by 86 · see citing works
Hänzelmann, P., Dobbek, H., Gremer, L., Huber, R., & Meyer, O. O. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4023 · Cited by 85 · see citing works
Dithiolene complexes and the nature of molybdopterin
Hine, F. J., Taylor, A., & Garner, C. D. (2010) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2010.01.017 · Cited by 85 · see citing works
Zhang, B., Hemann, C. F., & Hille, R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.076851 · Cited by 82 · see citing works
Milner‐White, E. J., & Russell, M. J. (2005) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-005-4582-7 · Cited by 81 · see citing works
Nature of the Catalytically Labile Oxygen at the Active Site of Xanthine Oxidase
Doonan, C. J., Stockert, A., Hille, R., & George, G. N. (2005) · Journal of the American Chemical Society · doi:10.1021/ja042500o · Cited by 81 · see citing works
X-ray Absorption Spectroscopy of the Molybdenum Site of Escherichia coli Formate Dehydrogenase
George, G. N., Colangelo, C. M., Dong, J., Scott, R. A., Khangulov, S. V., Gladyshev, V. N., & Stadtman, T. C. (1998) · Journal of the American Chemical Society · doi:10.1021/ja973004l · Cited by 79 · see citing works
Cotelesage, J. J. H., Pushie, M. J., Grochulski, P., Pickering, I. J., & George, G. N. (2012) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2012.06.019 · Cited by 79 · see citing works
Izumi, Y., Glaser, T., Rose, K., McMaster, J., Basu, P., Enemark, J. H., Hedman, B., Hodgson, K. O., & Solomon, E. I. (1999) · Journal of the American Chemical Society · doi:10.1021/ja9903678 · Cited by 74 · see citing works
THE NATURE OF THE XANTHINE OXIDASE FACTOR
Renzo, E. C. D., Kaleita, E., Heytler, P. G., Oleson, J. J., Hutchings, B. L., & Williams, J. H. (1953) · Journal of the American Chemical Society · doi:10.1021/ja01099a515 · Cited by 71 · see citing works
Hawkes, T. R., & Bray, R. C. (1984) · Biochemical Journal · doi:10.1042/bj2190481 · Cited by 70 · see citing works
George, G. N., Prince, R. C., Mukund, S., & Adams, M. W. W. (1992) · Journal of the American Chemical Society · doi:10.1021/ja00035a055 · Cited by 68 · see citing works
The mechanism of Mo-/Cu-dependent CO dehydrogenase
Hofmann, M., Kassube, J. K., & Graf, T. (2005) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-005-0661-5 · Cited by 63 · see citing works
X-ray Absorption Spectroscopy of Chicken Sulfite Oxidase Crystals
George, G. N., Pickering, I. J., & Kisker, C. (1999) · Inorganic Chemistry · doi:10.1021/ic981451b · Cited by 61 · see citing works
Xanthine oxidase, a molybdo-flavoprotein
Green, D. E., & Beinert, H. (1953) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(53)90111-5 · Cited by 61 · see citing works
Belaidi, A. A., & Schwarz, G. (2012) · Biochemical Journal · doi:10.1042/bj20121078 · Cited by 58 · see citing works
Messerschmidt, A., Niessen, H., Abt, D. J., Einsle, O., Schink, B., & Kroneck, P. M. H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404378101 · Cited by 52 · see citing works
Active-Site Stereochemical Control of Oxygen Atom Transfer Reactivity in Sulfite Oxidase
Peariso, K., McNaughton, R. L., & Kirk, M. L. (2002) · Journal of the American Chemical Society · doi:10.1021/ja017217t · Cited by 51 · see citing works
Williams, B. R., Fu, Y., Yap, G. P. A., & Burgmayer, S. J. N. (2012) · Journal of the American Chemical Society · doi:10.1021/ja310018e · Cited by 48 · see citing works
Tungsten, a biologically active metal
Ljungdahl, L. G. (1976) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(76)80193-4 · Cited by 44 · see citing works
Observation of Ligand-Based Redox Chemistry at the Active Site of a Molybdenum Enzyme
George, G. N., Costa, C., Moura, J. J. G., & Moura, I. (1999) · Journal of the American Chemical Society · doi:10.1021/ja9841761 · Cited by 43 · see citing works
McNaughton, R. L., Helton, M. E., Rubie, N. D., & Kirk, M. L. (2000) · Inorganic Chemistry · doi:10.1021/ic000474z · Cited by 42 · see citing works
George, G. N., Mertens, J. A., & Campbell, W. H. (1999) · Journal of the American Chemical Society · doi:10.1021/ja990310l · Cited by 39 · see citing works
Boll, M., Schink, B., Messerschmidt, A., & Kroneck, P. M. H. (2005) · Biological Chemistry · doi:10.1515/bc.2005.116 · Cited by 38 · see citing works
Wilcoxen, J., Snider, S., & Hille, R. (2011) · Journal of the American Chemical Society · doi:10.1021/ja205073j · Cited by 34 · see citing works
Kerrich, R. W., & Said, N. (2010) · Chemical Geology · doi:10.1016/j.chemgeo.2010.11.012 · Cited by 33 · see citing works
Taveirne, M. E., Sikes, M. L., & Olson, J. W. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06901.x · Cited by 32 · see citing works
Kerrich, R. W., Said, N., Manikyamba, C., & Wyman, D. A. (2012) · Gondwana Research · doi:10.1016/j.gr.2012.02.007 · Cited by 29 · see citing works
George, G. N., Garrett, R. M., Prince, R. C., & Rajagopalan, K. V. (2004) · Inorganic Chemistry · doi:10.1021/ic0489847 · Cited by 29 · see citing works
Peariso, K., Helton, M. E., Duesler, E. N., Shadle, S. E., & Kirk, M. L. (2007) · Inorganic Chemistry · doi:10.1021/ic061150z · Cited by 29 · see citing works
A Crystalline Material with Xanthine Oxidase Activity
Avis, P. G., Bergel, F., Bray, R. C., & SHOOTER, K. V. (1954) · Nature · doi:10.1038/1731230a0 · Cited by 29 · see citing works
The Janus face of copper: its expanding roles in biology and the pathophysiology of disease
Leary, S. C., & Winge, D. R. (2007) · EMBO Reports · doi:10.1038/sj.embor.7400915 · Cited by 29 · 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
Oxyanion Selectivity in Sulfate and Molybdate Transport Proteins: An ab Initio/CDM Study
Dudev, T., & Lim, C. (2004) · Journal of the American Chemical Society · doi:10.1021/ja047951n · Cited by 26 · see citing works
Qiu, J. A., Wilson, H. L., Pushie, M. J., Kisker, C., George, G. N., & Rajagopalan, K. V. (2010) · Biochemistry · doi:10.1021/bi1001954 · Cited by 26 · see citing works
Coelho, C., González, P. J., Trincão, J., Carvalho, A. L., Najmudin, S., Hettman, T., Dieckman, S., Moura, J. J. G., Moura, I., & Romão, M. J. (2007) · Acta Crystallographica Section F Structural Biology and Crystallization Communications · doi:10.1107/s1744309107022129 · Cited by 24 · see citing works
Qiu, J. A., Wilson, H. L., & Rajagopalan, K. V. (2012) · Biochemistry · doi:10.1021/bi201206v · Cited by 15 · see citing works
Metalloproteins – a new challenge for metrology
Swart, C., Fisicaro, P., Infante, H. G., & Zakel, S. (2012) · Metallomics · doi:10.1039/c2mt90049a · Cited by 8 · see citing works
Moracci, M., & Rossi, M. (1999) · Protein Science · doi:10.1110/ps.8.7.1564 · Cited by 2 · see citing works
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Trace elements at the intersection of marine biological and geochemical evolution
Robbins, L. J., Lalonde, S. V., Planavsky, N. J., Partin, C. A., Reinhard, C. T., Kendall, B., Scott, C., Hardisty, D. S., Gill, B. C., Alessi, D. S., et al. (2016) · Earth-Science Reviews · doi:10.1016/j.earscirev.2016.10.013 · Cited by 227 · see citing works
Bioinformatics of Metalloproteins and Metalloproteomes
Zhang, Y., & Zheng, J. (2020) · Molecules · doi:10.3390/molecules25153366 · Cited by 86 · see citing works
Formate Dehydrogenases Reduce CO2 Rather than HCO3−: An Electrochemical Demonstration
Meneghello, M., Oliveira, A. R., Jacq‐Bailly, A., Pereira, I. A. C., Léger, C., & Fourmond, V. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202101167 · Cited by 73 · see citing works
Structural basis of enzymatic benzene ring reduction
Weinert, T., Huwiler, S. G., Kung, J. W., Weidenweber, S., Hellwig, P., Stärk, H., Biskup, T., Weber, S., Cotelesage, J. J. H., George, G. N., et al. (2015) · Nature Chemical Biology · doi:10.1038/nchembio.1849 · Cited by 63 · see citing works
Heinze, K. (2015) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2015.04.010 · Cited by 61 · see citing works
Effect of the Heat Treatment on the Corrosion Resistance of Duplex Stainless Steels
Pezzato, L., Lago, M., Brunelli, K., Breda, M., & Calliari, I. (2018) · Journal of Materials Engineering and Performance · doi:10.1007/s11665-018-3408-5 · Cited by 60 · see citing works
Cornish-Bowden, A. J., & Cárdenas, M. L. (2017) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2017.05.023 · Cited by 55 · see citing works
Tungstoenzymes: Occurrence, Catalytic Diversity and Cofactor Synthesis
Seelmann, C. S., Willistein, M., Heider, J., & Boll, M. (2020) · Inorganics · doi:10.3390/inorganics8080044 · Cited by 52 · see citing works
Comparative genomics of molybdenum utilization in prokaryotes and eukaryotes
Peng, T., Xu, Y., & Zhang, Y. (2018) · BMC Genomics · doi:10.1186/s12864-018-5068-0 · Cited by 48 · see citing works
Shifting the metallocentric molybdoenzyme paradigm: the importance of pyranopterin coordination
Rothery, R. A., & Weiner, J. H. (2014) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-014-1194-6 · Cited by 40 · see citing works
Majumdar, A. (2014) · Dalton Transactions · doi:10.1039/c4dt00631c · Cited by 37 · see citing works
Boll, M., Einsle, O., Ermler, U., Kroneck, P. M. H., & Ullmann, G. M. (2016) · Microbial Physiology · doi:10.1159/000440805 · Cited by 37 · see citing works
Cui, M., Mohajerin, T. J., Adebayo, S., Datta, S., & Johannesson, K. H. (2020) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2020.04.004 · Cited by 35 · see citing works
Acetylene hydratase: a non-redox enzyme with tungsten and iron–sulfur centers at the active site
Kroneck, P. M. H. (2016) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-015-1330-y · Cited by 32 · see citing works
The active site structure and catalytic mechanism of arsenite oxidase
Warelow, T. P., Pushie, M. J., Cotelesage, J. J. H., Santini, J. M., & George, G. N. (2017) · Scientific Reports · doi:10.1038/s41598-017-01840-y · Cited by 32 · see citing works
Ehweiner, M. A., Wiedemaier, F., Belaj, F., & Zanetti, N. C. (2020) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.0c02412 · Cited by 31 · see citing works
Recent developments in the study of molybdoenzyme models
Basu, P., & Burgmayer, S. J. N. (2015) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-014-1228-0 · Cited by 31 · see citing works
Maurya, M. R., Uprety, B., & Avecilla, F. (2016) · European Journal of Inorganic Chemistry · doi:10.1002/ejic.201600694 · Cited by 30 · see citing works
Comparative genomics and metagenomics of the metallomes
Zhang, Y., Ying, H., & Xu, Y. (2019) · Metallomics · doi:10.1039/c9mt00023b · Cited by 29 · see citing works
Scott, I. M., Rubinstein, G. M., Lipscomb, G. L., Basen, M., Schut, G. J., Williams-Rhaesa, A. M., Lancaster, W. A., Poole, F. L., Kelly, R. M., & Adams, M. W. W. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.01634-15 · Cited by 28 · see citing works
Transient Catalytic Voltammetry of Sulfite Oxidase Reveals Rate Limiting Conformational Changes
Zeng, T., Leimkühler, S., Wollenberger, U., & Fourmond, V. (2017) · Journal of the American Chemical Society · doi:10.1021/jacs.7b05480 · Cited by 27 · see citing works
Culka, M., Huwiler, S. G., Boll, M., & Ullmann, G. M. (2017) · Journal of the American Chemical Society · doi:10.1021/jacs.7b07012 · Cited by 24 · see citing works
Malta, P. O., Condé, B. L., Assumpção, R. F., Perasoli, D. B., Sicupira, D. C., & Santos, D. B. (2019) · Metallurgical and Materials Transactions A · doi:10.1007/s11661-019-05193-1 · Cited by 23 · see citing works
Nandy, M., Shit, S., Corrado Rizzoli, B., Pilet, G., & Mitra, S. (2014) · Polyhedron · doi:10.1016/j.poly.2014.12.017 · Cited by 22 · see citing works
Paudel, J., Pokhrel, A., Kirk, M. L., & Li, F. (2019) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.8b03093 · Cited by 19 · see citing works
Mondal, R., Bonagani, S. K., Lodh, A., Sharma, T., Sivaprasad, P. V., Chai, G., Kain, V., & Samajdar, I. (2019) · CORROSION · doi:10.5006/3091 · Cited by 16 · see citing works
Maurya, M. R., Mengesha, B., Uprety, B., Jangra, N., Tomar, R., & Avecilla, F. (2018) · New Journal of Chemistry · doi:10.1039/c7nj03551a · Cited by 15 · see citing works
Stipdonk, M. J. V., Basu, P., Dille, S. A., Gibson, J. K., Berden, G., & Oomens, J. (2014) · The Journal of Physical Chemistry A · doi:10.1021/jp503222v · Cited by 13 · see citing works
Paoletti, N. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-823974-2.00007-3 · Cited by 10 · see citing works
Supramolecular inorganic chemistry leading to functional materials
Basu, O., & Das, S. K. (2020) · Journal of Chemical Sciences · doi:10.1007/s12039-020-1744-0 · Cited by 9 · see citing works
Zhang, Y., Wang, Z., Li, M., & Liao, R. (2022) · Journal of Catalysis · doi:10.1016/j.jcat.2022.09.002 · Cited by 9 · see citing works
The Catalytic Mechanisms of the Molybdenum and Tungsten Enzymes
Crawford, A. M., Cotelesage, J. J. H., Prince, R. C., & George, G. N. (2018) · Structure and bonding · doi:10.1007/430_2018_30 · Cited by 9 · see citing works
Mononuclear Sulfido-Tungsten(V) Complexes: Completing the Tp*MEXY (M = Mo, W; E = O, S) Series
Sproules, S. A., Eagle, A. A., George, G. N., White, J. M., & Young, C. G. (2017) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.7b00331 · Cited by 8 · see citing works
Bioinspired Tungsten Complexes Employing a Thioether Scorpionate Ligand
Ehweiner, M. A., Vidovič, C., Belaj, F., & Zanetti, N. C. (2019) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.9b00973 · Cited by 7 · see citing works
An Introduction to the Role of Molybdenum and Tungsten in Biology
Marques, H. M. (2025) · Inorganics · doi:10.3390/inorganics13070219 · Cited by 6 · see citing works
Synthesis and structural characterization of copper–cuprizone complexes
Pushie, M. J., Summers, K. L., Nienaber, K. H., Pickering, I. J., & George, G. N. (2022) · Dalton Transactions · doi:10.1039/d2dt01475k · Cited by 6 · see citing works
Sala, S., Altskär, A. I., Pingel, T., Gianoncelli, A., Žižić, M. V., Rivard, C., Olsson, E., Nielsen, T. J., & Lorén, N. (2024) · LWT · doi:10.1016/j.lwt.2024.116787 · Cited by 5 · see citing works
Formate Dehydrogenases Reduce CO2 Rather than HCO3−: An Electrochemical Demonstration
Meneghello, M., Oliveira, A. R., Jacq‐Bailly, A., Pereira, I. A. C., Léger, C., & Fourmond, V. (2021) · Angewandte Chemie · doi:10.1002/ange.202101167 · Cited by 5 · see citing works
Direct Electrochemistry of Molybdenum and Tungsten Enzymes
Fourmond, V. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-409547-2.13354-2 · Cited by 5 · see citing works
Baker, A. T., George, G. N., & Harris, H. H. (2025) · Metallomics · doi:10.1093/mtomcs/mfaf038 · Cited by 4 · see citing works
Akashi, H., Machida, N., Kamada, T., Nihashi, H., Aya, D., Yamaguchi, K., Takagi, H., & Shibahara, T. (2017) · Bulletin of the Chemical Society of Japan · doi:10.1246/bcsj.20170024 · Cited by 4 · see citing works
Metabolic evolution of pyranopterin-dependent biochemistryPreprint
Goldford, J. E., Murali, R., Valentine, J. S., & Fischer, W. W. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.01.555371 · Cited by 3 · see citing works
Giri, N. C., Thach, T. T., Dhanabalan, K., Cesiunaite, M., Radhakrishnan, M., Wedasingha, L., Manicke, N. E., Wells, M., Szaleniec, M., Ramaswamy, S., et al. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110928 · 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
Assumpção, R. F., Santos, R. M., de Sousa, M. L. O., da Silva, N. M., Caires, A. J., Escobar, D. M. P., & Santos, D. B. (2023) · Journal of Materials Science · doi:10.1007/s10853-023-08401-x · Cited by 3 · see citing works
Effect of a Novel Heat Treatment on the Corrosion Resistance of Duplex Stainless Steel S32101
Zhang, X., Xiong, Z., & Cheng, X. (2025) · Journal of Materials Engineering and Performance · doi:10.1007/s11665-025-10728-2 · Cited by 3 · see citing works
Keighley, D. G., Boonsue, S., & Hall, D. (2018) · Geobiology · doi:10.1111/gbi.12310 · Cited by 3 · 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
Trace Elements in Medicinal Metallomics
Orlova, M. A., Kalmykov, S. N., Трофимова, Т. П., & Kuznetsov, D. A. (2024) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/0113895575333766240912162252 · Cited by 1 · see citing works
Calliari, I., Polyakova, M., Гулин, А. Е., Lago, M., Gennari, C., & Pezzato, L. (2020) · Metallography Microstructure and Analysis · doi:10.1007/s13632-020-00642-5
Sproules, S. A. (2021) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.1c01055
Dror, Y., & Stern, F. (2018) · Healthy ageing and longevity · doi:10.1007/978-3-030-03742-0_7
X-ray Absorption Spectroscopy of Metals in Biology
George, G. N., & Pickering, I. J. (2018) · Springer eBooks · doi:10.1007/978-3-642-35943-9_680-1
Comparative Study of Aqueous Acid–Base Properties of Tungstocene and Molybdocene Complexes
Stix, N., Ćorović, M. Z., Schiller, S. S., Dupé, A., & Zanetti, N. C. (2025) · Organometallics · doi:10.1021/acs.organomet.5c00345
A phylogenomic analysis of ancient transition metal biochemistry
Dhyani, K. M., & Badran, A. H. (2026) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2026.08.003
- Authors
- Pushie, M. J., Cotelesage, J. J., & George, G. N.
- Affiliations
- University of Saskatchewan (CA)
- Venue
- Metallomics
- Publisher
- Oxford University Press (OUP)
- Published
- 2014
- Volume
- 6
- Issue
- 1
- Pages
- 15-24
- ISSN
- 1756-5901 (ISSN-L)
- 1756-591X
- OpenAlex
- W2137509160
- Cited by
- 55
- References
- 100
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 3 · 2020: 6 · 2019: 5 · 2018: 7 · 2017: 8 · 2016: 4 · 2015: 4 · 2014: 4
- FWCI
- 0.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Metallomics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Saskatchewan
- Saskatchewan Health Research Foundation
- Canadian Institutes of Health Research
- Natural Sciences and Engineering Research Council of Canada
- 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
- molybdenum enzymes, tungsten enzymes, molybdopterin, enzyme active site structure, metal oxidation state, enzyme evolution, microbial respiration, nitrogen fixation, human health
- MeSH terms
- Molybdenum Cofactors, Binding Sites, Coenzymes, Metalloproteins, Models, Molecular, Molybdenum, Oxygen, Pteridines, Transferases, Tungsten, Molecular Structure, Protein Structure, Tertiary, Catalytic Domain
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