Nitrite reductase activity of rat and human xanthine oxidase, xanthine dehydrogenase, and aldehyde oxidase: Evaluation of their contribution to NO formation in vivo

Biochemistry

Volumn 54, Issue 3, 2015, Pages 685-710

  Maia, Luisa B ^a   Pereira, Vaînia ^b   Mira, Lurdes ^b   Moura, José J G ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDES; CELL CULTURE; ENZYME ACTIVITY; ENZYMES; MAMMALS; RATS;

CHEMICAL EQUATIONS; KINETIC CHARACTERIZATION; MOLECULAR MECHANISM; NITRITE REDUCTASE; NITRITE REDUCTION; ONE-ELECTRON REDUCTIONS; RELATIVE CONTRIBUTION; XANTHINE DEHYDROGENASE;

REDUCTION;

ALDEHYDE OXIDASE; NITRIC OXIDE; NITRITE REDUCTASE; XANTHINE DEHYDROGENASE; XANTHINE OXIDASE; ALDEHYDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NITRITE; OXYGEN; XANTHINE;

ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; HYPOXIA; IN VIVO STUDY; NONHUMAN; PH; PRIORITY JOURNAL; RAT; REDUCTION; ANIMAL; BIOCATALYSIS; CHEMICAL STRUCTURE; CYTOLOGY; ENDOTHELIUM CELL; HEPG2 CELL LINE; KINETICS; MALE; METABOLISM; MICROVASCULATURE; OXIDATION REDUCTION REACTION; SPRAGUE DAWLEY RAT; TIME;

MAMMALIA; RATTUS;

ALDEHYDE OXIDASE; ALDEHYDES; ANIMALS; BIOCATALYSIS; ENDOTHELIAL CELLS; HEP G2 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MALE; MICROVESSELS; MODELS, MOLECULAR; NAD; NITRIC OXIDE; NITRITE REDUCTASES; NITRITES; OXIDATION-REDUCTION; OXYGEN; RATS, SPRAGUE-DAWLEY; SUBSTRATE SPECIFICITY; TIME FACTORS; XANTHINE; XANTHINE DEHYDROGENASE; XANTHINE OXIDASE;

EID: 84921841743     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500987w     Document Type: Article

References (164)

1. Moncada, S., Palmer, R. M. J., and Higgs, E. A. (1991) Nitric oxide: Physiology, pathophysiology, and pharmacology Pharmacol. Rev. 43, 109-142
2. Eiserich, J. P., Patel, R. P., and O'Donnell, V. B. (1998) Pathophysiology of nitric oxide and related species: Free radical reactions and modification of biomolecules Mol. Aspects Med. 19, 221-357
3. Pfeiffer, S., Mayer, B., and Hemmens, B. (1999) Nitric oxide: Chemical puzzles posed by a biological messenger Angew. Chem., Int. Ed. 38, 1714-1731
4. Stuehr, D. J. (1999) Mammalian nitric oxide synthases Biochim. Biophys. Acta 1411, 217-230
5. Alderton, W. K., Cooper, C. E., and Knowles, R. G. (2001) Nitric oxide synthases: Structure, function and inhibition Biochem. J. 357, 593-615
6. Beckman, J. S. and Koppenol, W. H. (1996) Nitric oxide, superoxide and peroxynitrite: The good, the bad and the ugly Am. J. Physiol. 271, C1424-C1437
7. Feelisch, M., Rassaf, T., Mnaimneh, S., Singh, N., Bryan, N. S., Jourd'Heuil, D., and Kelm, M. (2002) Concomitant S-, N-, and heme-nitros(yl)ation in biological tissues and fluids: Implications for the fate of NO in vivo FASEB J. 16, 1775-1785
8. Bryan, N. S., Rassaf, T., Maloney, R. E., Rodriguez, C. M., Saijo, F., Rodriguez, J. R., and Feelisch, M. (2004) Cellular targets and mechanisms of nitros(yl)ation: An insight into their nature and kinetics in vivo Proc. Natl. Acad. Sci. U.S.A. 101, 4308-4313
9. Toledo, J. C., Jr. and Augusto, O. (2012) Connecting the chemical and biological properties of nitric oxide Chem. Res. Toxicol. 25, 975-989
10. 2 reaction Chem. Res. Toxicol. 6, 23-27
11. Goldstein, S. and Czapski, G. (1995) Kinetics of nitric oxide autoxidation in aqueous solution in the absence and presence of various reductants. The nature of the oxidizing intermediates J. Am. Chem. Soc. 117, 12078-12084
12. Shiva, S., Wang, X., Ringwood, L. A., Xu, X., Yuditskaya, S., Annavajjhala, V., Miyajima, H., Hogg, N., Harris, Z. L., and Gladwin, M. T. (2006) Ceruloplasmin is a NO oxidase and nitrite synthase that determines endocrine NO homeostasis Nat. Chem. Biol. 2, 486-493
13. Gow, A. J., Luchsinger, B. P., Pawloski, J. R., Singel, D. J., and Stamler, J. S. (1999) The oxyhemoglobin reaction of nitric oxide Proc. Natl. Acad. Sci. U.S.A. 96, 9027-9032
14. Flögel, U., Merx, M. W., Gödecke, A., Decking, U. K. M., and Schrader, J. (2001) Myoglobin: A scavenger of bioactive NO Proc. Natl. Acad. Sci. U.S.A. 98, 735-740
15. Herold, S., Exner, M., and Nauser, T. (2001) Kinetic and mechanistic studies of the NO-mediated oxidation of oxymyoglobin and oxyhemoglobin Biochemistry 40, 3385-3395
16. Joshi, M. S., Ferguson, T. B., Jr., Han, T. H., Hyduke, D. R., Liao, J. C., Rassaf, T., Bryan, N., Feelisch, M., and Lancaster, J. R., Jr. (2002) Nitric oxide is consumed, rather than conserved, by reaction with oxyhemoglobin under physiological conditions Proc. Natl. Acad. Sci. U.S.A. 99, 10341-10346
17. Cosby, K., Partovi, K. S., Crawford, J. H., Patel, R. P., Reiter, C. D., Martyr, S., Yang, B. K., Waclawiw, M. A., Zalos, G., Xu, X., Huang, K. T., Shields, H., Kim-Shapiro, D. B., Schechter, A. N., Cannon, R. O., III, and Gladwin, M. T. (2003) Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation Nat. Med. 9, 1498-1505
18. Webb, A., Bond, R., McLean, P., Uppal, R., Benjamin, N., and Ahluwalia, A. (2004) Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage Proc. Natl. Acad. Sci. U.S.A. 101, 13683-13688
19. Duranski, M. R., Greer, J. J., Dejam, A., Jaganmohan, S., Hogg, N., Langston, W., Patel, R. P., Yet, S. F., Wang, X., Kevil, C. G., Gladwin, M. T., and Lefer, D. J. (2005) Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver J. Clin. Invest. 115, 1232-1240
20. Lu, P., Liu, F., Yao, Z., Wang, C. Y., Chen, D. D., Tian, Y., Zhang, J. H., and Wu, Y. H. (2005) Nitrite-derived nitric oxide by xanthine oxidoreductase protects the liver against ischemia-reperfusion injury Hepatobiliary & Pancreatic Diseases International 4, 350-355
21. Baker, J. E., Su, J., Fu, X., Hsu, A., Gross, G. J., Tweddell, J. S., and Hogg, N. (2007) Nitrite confers protection against myocardial infarction: Role of xanthine oxidoreductase, NADPH oxidase and K(ATP) channels J. Mol. Cell. Cardiol. 43, 437-444
22. Dejam, A., Hunter, C. J., Tremonti, C., Pluta, R. M., Hon, Y. Y., Grimes, G., Partovi, K., Pelletier, M. M., Oldfield, E. H., Cannon, R. O., Schechter, A. N., and Gladwin, M. T. (2007) Nitrite infusion in humans and nonhuman primates: Endocrine effects, pharmacokinetics, and tolerance formation Circulation 116, 1821-1831
23. Tripatara, P., Patel, N. S., Webb, A., Rathod, K., Lecomte, F. M., Mazzon, E., Cuzzocrea, S., Yaqoob, M. M., Ahluwalia, A., and Thiemermann, C. (2007) Nitrite-derived nitric oxide protects the rat kidney against ischemia/reperfusion injury in vivo: Role for xanthine oxidoreductase J. Am. Soc. Nephrol. 18, 570-580
24. Hendgen-Cotta, U. B., Merx, M. W., Shiva, S., Schmitz, J., Becher, S., Klare, J. P., Steinhoff, H., Goedecke, A., Schrader, J., Gladwin, M. T., Kelm, M., and Rassaf, T. (2008) Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury Proc. Natl. Acad. Sci. U.S.A. 105, 10256-10261
25. Webb, A. J., Milsom, A. B., Rathod, K. S., Chu, W. L., Qureshi, S., Lovell, M. J., Lecomte, F. M., Perrett, D., Raimondo, C., Khoshbin, E., Ahmed, Z., Uppal, R., Benjamin, N., Hobbs, A. J., and Ahluwalia, A. (2008) Mechanisms underlying erythrocyte and endothelial nitrite reduction to nitric oxide in hypoxia: Role for xanthine oxidoreductase and endothelial nitric oxide synthase Circ. Res. 103, 957-964
26. Casey, D. B., Badejo, A. M., Dhaliwal, J. S., Murthy, S. N., Hyman, A. L., Nossaman, B. D., and Kadowitz, P. J. (2009) Pulmonary vasodilator responses to sodium nitrite are mediated by an allopurinol-sensitive mechanism in the rat Am. J. Physiol. 296, H524-H533
27. Zuckerbraun, B. S., Shiva, S., Ifedigbo, E., Mathier, M. A., Mollen, K. P., Rao, J., Bauer, P. M., Choi, J. J., Curtis, E., Choi, A. M., and Gladwin, M. T. (2010) Nitrite potently inhibits hypoxic and inflammatory pulmonary arterial hypertension and smooth muscle proliferation via xanthine oxidoreductase-dependent nitric oxide generation Circulation 121, 98-109
28. Baliga, R. S., Milsom, A. B., Ghosh, S. M., Trinder, S. L., Macallister, R. J., Ahluwalia, A., and Hobbs, A. J. (2012) Dietary nitrate ameliorates pulmonary hypertension: Cytoprotective role for endothelial nitric oxide synthase and xanthine oxidoreductase Circulation 125, 2922-2932
29. Cantu-Medellin, N. and Kelley, E. E. (2013) Xanthine oxidoreductase-catalyzed reduction of nitrite to nitric oxide: Insights regarding where, when and how Nitric Oxide 34, 19-26
30. Ghosh, S. M., Kapil, V., Fuentes-Calvo, I., Bubb, K. J., Pearl, V., Milsom, A. B., Khambata, R., Maleki-Toyserkani, S., Yousuf, M., Benjamin, N., Webb, A. J., Caulfield, M. J., Hobbs, A. J., and Ahluwalia, A. (2013) Enhanced vasodilator activity of nitrite in hypertension: Critical role for erythrocytic xanthine oxidoreductase and translational potential Hypertension 61, 1091-1102
31. Helms, C. and Kim-Shapiro, D. B. (2013) Hemoglobin-mediated nitric oxide signaling Free Radical Biol. Med. 61, 464-472
32. Akrawinthawong, K., Park, J. W., Piknova, B., Sibmooh, N., Fucharoen, S., and Schechter, A. N. (2014) A flow cytometric analysis of the inhibition of platelet reactivity due to nitrite reduction by deoxygenated erythrocytes PLoS One 9, e92435
33. Maia, L. and Moura, J. J. G. (2014) How biology handles nitrite Chem. Rev. 114, 5273-5357
34. Maia, L. and Moura, J. J. G. (2014) Nitrite reduction by molybdoenzymes: A new class of nitric oxide-forming nitrite reductases J. Biol. Inorg. Chem. 10.1007/s00775-014-1234-2
35. Omar, S. A. and Webb, A. (2014) Nitrite reduction and cardiovascular protection J. Mol. Cell. Cardiol. 73, 57-69
36. Giraldez, R. R., Panda, A., Xia, Y., Sanders, S. P., and Zweier, J. L. (1997) Decreased nitric-oxide synthase activity causes impaired endothelium-dependent relaxation in the postischemic heart J. Biol. Chem. 272, 21420-21426
37. Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., and Blake, D. R. (1998) Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions FEBS Lett. 427, 225-228
38. Zhang, Z., Naughton, D., Winyard, P. G., Benjamin, N., Blake, D. R., and Symons, M. C. (1998) Generation of nitric oxide by a nitrite reductase activity of xanthine oxidase: A potential pathway for nitric oxide formation in the absence of nitric oxide synthase activity Biochem. Biophys. Res. Commun. 249, 767-772
39. Godber, H. L. J., Doel, J. J., Sapkota, G. P., Blake, D. R., Stevens, C. R., Eisenthal, R., and Harrison, R. (2000) Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase J. Biol. Chem. 275, 7757-7763
40. Li, H., Samouilov, A., Liu, X., and Zweier, J. L. (2001) Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrite reduction: Evaluation of its role in nitric oxide generation in anoxic tissues J. Biol. Chem. 276, 24482-24489
41. Li, H., Samouilov, A., Liu, X., and Zweier, J. L. (2004) Characterization of the effects of oxygen on xanthine oxidase-mediated nitric oxide formation J. Biol. Chem. 279, 16939-16946
42. Li, H., Cui, H., Kundu, T. K., Alzawahra, W., and Zweier, J. L. (2008) Nitric oxide production from nitrite occurs primarily in tissues not in the blood: Citical role of xanthine oxidase and aldehyde oxidase J. Biol. Chem. 283, 17855-17863
43. Maia, L. and Moura, J. J. G. (2011) Nitrite reduction by xanthine oxidase family enzymes: A new class of nitrite reductases JBIC, J. Biol. Inorg. Chem. 16, 443-460
44. Li, H., Kundu, T. K., and Zweier, J. L. (2009) Characterization of the magnitude and mechanism of aldehyde oxidase-mediated nitric oxide production from nitrite J. Biol. Chem. 284, 33850-33858
45. Wang, J., Krizowski, S., Fischer, K., Niks, D., Tejero, J., Sparacino-Watkins, C., Wang, L., Ragireddy, P., Frizzell, S., Kelley, E. E., Zhang, Y., Basu, P., Hille, R., Schwarz, G., and Gladwin, M. T. (2014) Sulfite oxidase catalyzes single electron transfer at molybdenum domain to reduce nitrite to nitric oxide Antioxid. Redox Signaling 10.1089/ars.2013.5397
46. Sparacino-Watkins, C. E., Tejero, J., Sun, B., Gauthier, M. C., Thomas, J., Ragireddy, V., Merchant, B. A., Wang, J., Azarov, I., Basu, P., and Gladwin, M. T. (2014) Nitrite reductase and NO synthase activity of the mitochondrial molybdopterin enzymes mARC1 and mARC2 J. Biol. Chem. 289, 10345-10358
47. Huang, Z., Shiva, S., Kim-Shapiro, D. B., Patel, R. P., Ringwood, L. A., Irby, C. E., Huang, K. T., Ho, C., Hogg, N., Schechter, A. N., and Gladwin, M. T. (2005) Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control J. Clin. Invest. 115, 2099-2107
48. Gladwin, M. T. and Kim-Shapiro, D. B. (2008) The functional nitrite reductase activity of the heme-globins Blood 112, 2636-2647
49. Tiso, M., Tejero, J., Basu, S., Azarov, I., Wang, X., Simplaceanu, V., Frizzell, S., Jayaraman, T., Geary, L., Shapiro, C., Ho, C., Shiva, S., Kim-Shapiro, D. B., and Gladwin, M. T. (2011) Human neuroglobin functions as a redox-regulated nitrite reductase J. Biol. Chem. 286, 18277-18289
50. Li, H., Hemann, C., Abdelghany, T. M., El-Mahdy, M. A., and Zweier, J. L. (2012) Characterization of the mechanism and magnitude of cytoglobin-mediated nitrite reduction and nitric oxide generation under anaerobic conditions J. Biol. Chem. 287, 36623-36633
51. Basu, S., Azarova, N. A., Font, M. D., King, S. B., Hogg, N., Gladwin, M. T., Shiva, S., and Kim-Shapiro, D. B. (2008) Nitrite reductase activity of cytochrome c J. Biol. Chem. 283, 32590-32597
52. Li, H., Liu, X., Cui, H., Chen, Y. R., Cardounel, A. J., and Zweier, J. L. (2006) Characterization of the mechanism of cytochrome P450 reductase-cytochrome P450-mediated nitric oxide and nitrosothiol generation from organic nitrates J. Biol. Chem. 281, 12546-12554
53. Hendrychova, T., Anzenbacherova, E., Hudecek, J., Skopalik, J., Lange, R., Hildebrandt, P., Otyepka, M., and Anzenbacher, P. (2011) Flexibility of human cytochrome P450 enzymes: Molecular dynamics and spectroscopy reveal important function-related variations Biochim. Biophys. Acta 1814, 58-68
54. Castello, P. R., David, P. S., McClure, T., Crook, Z., and Poyton, R. O. (2006) Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: Implications for oxygen sensing and hypoxic signaling in eukaryotes Cell Metab. 3, 277-287
55. Castello, P. R., Woo, D. K., Ball, K., Wojcik, J., Liu, L., and Poyton, R. O. (2008) Oxygen-regulated isoforms of cytochrome c oxidase have differential effects on its nitric oxide production and on hypoxic signaling Proc. Natl. Acad. Sci. U.S.A. 105, 8203-8208
56. Aamand, R., Dalsgaard, T., Jensen, F. B., Simonsen, U., Roepstorff, A., and Fago, A. (2009) Generation of nitric oxide from nitrite by carbonic anhydrase: A possible link between metabolic activity and vasodilation Am. J. Physiol. 297, H2068-H2074
57. Badejo, A. M., Jr., Hodnette, C., Dhaliwal, J. S., Casey, D. B., Pankey, E., Murthy, S. N., Nossaman, B. D., Hyman, A. L., and Kadowitz, P. (2010) Mitochondrial aldehyde dehydrogenase mediates vasodilator responses of glyceryl trinitrate and sodium nitrite in the pulmonary vascular bed of the rat Am. J. Physiol. H819-H826
58. Hille, R. and Nishino, T. (1995) Xanthine oxidase and xanthine dehydrogenase FASEB J. 9, 995-1003
59. Hille, R. (1996) The mononuclear molybdenum enzymes Chem. Rev. 96, 2757-2816
60. Hille, R. (2005) Molybdenum-containing hydroxylases Arch. Biochem. Biophys. 433, 107-116
61. Hille, R. (2006) Structure and function of xanthine oxidoreductase Eur. J. Inorg. Chem. 1913-1926
62. Nishino, T., Okamoto, K., Eger, B. T., Pai, E. F., and Nishino, T. (2008) Mammalian xanthine oxidoreductase: Mechanism of transition from xanthine dehydrogenase to xanthine oxidase FEBS J. 275, 3278-3289
63. Hille, R., Nishino, T., and Bittner, F. (2011) Molybdenum enzymes in higher organisms Coord. Chem. Rev. 255, 1179-1205
64. Okamoto, K., Kusano, T., and Nishino, T. (2013) Chemical nature and reaction mechanisms of the molybdenum cofactor of xanthine oxidoreductase Curr. Pharm. Des. 19, 2606-2614
65. Della Corte, E., Gozzetti, G., Novello, F., and Stirpe, F. (1969) Properties of the xanthine oxidase from human liver Biochim. Biophys. Acta 191, 164-166
66. Parks, D. A. and Granger, D. N. (1986) Xanthine oxidase: Biochemistry, distribution and physiology Acta Physiol. Scand., Suppl. 548, 87-99
67. Ichikawa, M., Nishino, T., and Ichikawa, A. (1992) Subcellular localization of xanthine oxidase in rat hepatocytes: High-resolution immunoelectron microscopic study combined with biochemical analysis J. Histochem. Cytochem. 40, 1097-1103
68. Sarnesto, A., Linder, N., and Raivio, K. O. (1996) Organ distribution and molecular forms of human xanthine dehydrogenase/xanthine oxidase protein Lab. Invest. 74, 48-56
69. Adachi, T., Fukushima, T., Usami, Y., and Hirano, K. (1993) Binding of human xanthine oxidase to sulphated glycosaminoglycans on the endothelial-cell surface Biochem. J. 289, 523-527
70. Radi, R., Rubbo, H., Bush, K., and Freeman, B. A. (1997) Xanthine oxidase binding to glycosaminoglycans: Kinetics and superoxide dismutase interactions of immobilized xanthine oxidase-heparin complexes Arch. Biochem. Biophys. 339, 125-135
71. Rouquette, M., Page, S., Bryant, R., Benboubetra, M., Stevens, C. R., Blake, D. R., Whish, W. D., Harrison, R., and Tosh, D. (1998) Xanthine oxidoreductase is asymmetrically localised on the outer surface of human endothelial and epithelial cells in culture FEBS Lett. 426, 397-401
72. Vickers, S., Schiller, H. J., Hildreth, J. E., and Bulkley, G. B. (1998) Immunoaffinity localization of the enzyme xanthine oxidase on the outside surface of the endothelial cell plasma membrane Surgery 124, 551-560
73. Kelley, E. E., Hock, T., Khoo, N. K., Richardson, G. R., Johnson, K. K., Powell, P. C., Giles, G. I., Agarwal, A., Lancaster, J. R., Jr., and Tarpey, M. M. (2006) Moderate hypoxia induces xanthine oxidoreductase activity in arterial endothelial cells Free Radical Biol. Med. 40, 952-959
74. Turner, N. A., Doyle, W. A., Ventom, A. M., and Bray, R. C. (1995) Properties of rabbit liver aldehyde oxidase and the relationship of the enzyme to xanthine oxidase and dehydrogenase Eur. J. Biochem. 232, 646-657
75. Garattini, E. and Terao, M. (2011) Increasing recognition of the importance of aldehyde oxidase in drug development and discovery Drug Metab. Rev. 43, 374-386
76. Enroth, C., Eger, B. T., Okamoto, K., Nishino, T., Nishino, T., and Pai, E. F. (2000) Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: Structure-based mechanism of conversion Proc. Natl. Acad. Sci. U.S.A. 97, 10723-10728
77. Ishikita, H., Eger, B. T., Okamoto, K., Nishino, T., and Pai, E. F. (2012) Protein conformational gating of enzymatic activity in xanthine oxidoreductase J. Am. Chem. Soc. 134, 999-1009
78. Kooij, A., Schiller, H. J., Schijns, M., Van Noorden, C. J., and Frederiks, W. M. (1994) Conversion of xanthine dehydrogenase into xanthine oxidase in rat liver and plasma at the onset of reperfusion after ischemia Hepatology 19, 1488-1495
79. Garattini, E., Fratelli, M., and Terao, M. (2008) Mammalian aldehyde oxidases: Genetics, evolution and biochemistry Cell. Mol. Life Sci. 65, 1019-1048
80. Pryde, D. C., Dalvie, D., Hu, Q., Jones, P., Obach, R. S., and Tran, T. D. (2010) Aldehyde oxidase: An enzyme of emerging importance in drug discovery J. Med. Chem. 53, 8441-8460
81. Swenson, T. L. and Casida, J. E. (2013) Aldehyde oxidase importance in vivo in xenobiotic metabolism: Imidacloprid nitroreduction in mice Toxicol. Sci. 133, 22-28
82. Landon, E. J. and Myles, M. (1967) NADH oxidation by hypoxanthine dehydrogenase of avian kidney Biochim. Biophys. Acta 143, 429-431
83. Massey, V., Brumby, P. E., Komai, H., and Palmer, G. (1969) Studies on milk xanthine oxidase: Some spectral and kinetic properties J. Biol. Chem. 244, 1682-1691
84. Mira, L., Maia, L., Barreira, L., and Manso, C. F. (1995) Evidence for free radical generation due to NADH oxidation by aldehyde oxidase during ethanol metabolism Arch. Biochem. Biophys. 318, 53-58
85. Maia, L., Vala, A., and Mira, L. (2005) NADH oxidase activity of rat liver xanthine dehydrogenase and xanthine oxidase: Contribution for damage mechanisms Free Radical Res. 39, 979-986
86. Maia, L., Duarte, R. O., Ponces-Freire, A., Moura, J. J. G., and Mira, L. (2007) NADH oxidase activity of rat and human liver xanthine oxidoreductase: Potential role in superoxide production JBIC, J. Biol. Inorg. Chem. 12, 777-787
87. Kundu, T. K., Velayutham, M., and Zweier, J. L. (2012) Aldehyde oxidase functions as a superoxide generating NADH oxidase: An important redox regulated pathway of cellular oxygen radical formation Biochemistry 51, 2930-2939
88. Krenitsky, T. A., Neil, S. M., Elion, G. B., and Hitchings, G. H. (1972) A comparison of the specificities of xanthine oxidase and aldehyde oxidase Arch. Biochem. Biophys. 150, 585-599
89. Hall, W. W. and Krenitsky, T. A. (1986) Aldehyde oxidase from rabbit liver: Specificity toward purines and their analogs Arch. Biochem. Biophys. 251, 36-46
90. Li, H., Samouilov, A., Liu, X., and Zweier, J. L. (2003) Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrate reduction: Evaluation of its role in nitrite and nitric oxide generation in anoxic tissues Biochemistry 42, 1150-1159
91. Stone, J. R. and Yang, S. (2006) Hydrogen peroxide: A signaling messenger Antioxid. Redox Signaling 8, 243-270
92. Veal, E. A., Day, A. M., and Morgan, B. A. (2007) Hydrogen peroxide sensing and signaling Mol. Cell 26, 1-14
93. Wright, R. M. and Repine, J. E. (1997) The human molybdenum hydroxylase gene family: Co-conspirators in metabolic free-radical generation and disease Biochem. Soc. Trans. 25, 799-804
94. Harrison, R. (2002) Structure and function of xanthine oxidoreductase: Where are we now? Free Radical Biol. Med. 33, 774-797
95. Stirpe, F., Ravaioli, M., Battelli, M. G., Musiani, S., and Grazi, G. L. (2002) Xanthine oxidoreductase activity in human liver disease Am. J. Gastroenterol. 97, 2079-2085
96. Madamanchi, N. R. and Runge, M. S. (2013) Redox signaling in cardiovascular health and disease Free Radical Biol. Med. 61, 473-501
97. Granger, D. N., Rutili, G., and McCord, J. M. (1981) Superoxide radicals in feline intestinal ischemia Gastroenterology 81, 22-29
98. McCord, J. M. (1985) Oxygen-derived free radicals in postischemic tissue injury N. Engl. J. Med. 312, 159-163
99. Zweier, J. L., Kuppusamy, P., and Lutty, G. A. (1988) Measurement of endothelial cell free radical generation: Evidence for a central mechanism of free radical injury in postischemic tissues Proc. Natl. Acad. Sci. U.S.A. 85, 4046-4050
100. Nishino, T., Nakanishi, S., Okamoto, K., Mizushima, J., Hori, H., Iwasaki, T., Nishino, T., Ichimori, K., and Nakazawa, H. (1997) Conversion of xanthine dehydrogenase into oxidase and its role in reperfusion injury Biochem. Soc. Trans. 25, 783-786
101. Lieber, C. S. (1988) Biochemical and molecular basis of alcohol-induced injury to liver and other tissues N. Engl. J. Med. 319, 1639-1650
102. Kato, S., Kawase, T., Alderman, J., Inatomi, N., and Lieber, C. (1990) Role of xanthine oxidase in ethanol-induced lipid peroxidation in rats Gastroenterology 98, 203-210
103. Wright, R. M., McManaman, J. L., and Repine, J. E. (1999) Alcohol-induced breast cancer: A proposed mechanism Free Radical Biol. Med. 26, 348-354
104. Wu, D. and Cederbaum, A. I. (2003) Alcohol, oxidative stress, and free radical damage Alcohol Research & Health 27, 277-284
105. Terao, M., Kurosaki, M., Saltini, G., Demontis, S., Marini, M., Salmona, M., and Garattini, E. (2000) Cloning of the cDNAs coding for two novel molybdo-flavoproteins showing high similarity with aldehyde oxidase and xanthine oxidoreductase J. Biol. Chem. 275, 30690-30700
106. Terao, M., Kurosaki, M., Marini, M., Vanoni, M. A., Saltini, G., Bonetto, V., Bastone, A., Federico, C., Saccone, S., Fanelli, R., Salmona, M., and Garattini, E. (2001) Purification of the aldehyde oxidase homolog 1 (AOH1) protein and cloning of the AOH1 and aldehyde oxidase homolog 2 (AOH2) genes: Identification of a novel molybdo-flavoprotein gene cluster on mouse chromosome 1 J. Biol. Chem. 276, 46347-46363
107. Kurosaki, M., Terao, M., Barzago, M. M., Bastone, A., Bernardinello, D., Salmona, M., and Garattini, E. (2004) The aldehyde oxidase gene cluster in mice and rats: Aldehyde oxidase homologue 3, a novel member of the molybdo-flavoenzyme family with selective expression in the olfactory mucosa J. Biol. Chem. 279, 50482-50498
108. Maia, L. and Mira, L. (2002) Xanthine oxidase and aldehyde oxidase: A simple procedure for the simultaneous purification from rat liver Arch. Biochem. Biophys. 400, 48-53
109. 2-dependent types of rat liver xanthine dehydrogenase J. Biol. Chem. 264, 10015-10022
110. Branzoli, U. and Massey, V. (1974) Evidence for an active site persulfide residue in rabbit liver aldehyde oxidase J. Biol. Chem. 249, 4346-4349
111. Branzoli, U. and Massey, V. (1974) Preparation of aldehyde oxidase in its native and deflavo forms J. Biol. Chem. 249, 4339-4345
112. Cornish-Bowden, A. (1995) Fundamentals of enzyme kinetics, Portland Press, London.
113. Xia, Y. and Zweier, J. L. (1997) Direct measurement of nitric oxide generation from nitric oxide synthase Proc. Natl. Acad. Sci. U.S.A. 94, 12705-12710
114. Ichimori, K., Fukahori, M., Nakazawa, H., Okamoto, K., and Nishino, T. (1999) Inhibition of xanthine oxidase and xanthine dehydrogenase by nitric oxide J. Biol. Chem. 274, 7763-7768
115. Massey, V. and Edmondson, D. (1970) On the mechanism of inactivation of xanthine oxidase by cyanide J. Biol. Chem. 245, 6595-6598
116. Coughlan, M. P., Johnson, J. L., and Rajagopalan, K. V. (1980) Mechanisms of inactivation of molybdoenzymes by cyanide J. Biol. Chem. 255, 2694-2699
117. Olson, J. S., Ballou, D. P., Palmer, G., and Massey, V. (1974) The mechanism of action of xanthine oxidase J. Biol. Chem. 249, 4363-4382
118. Hunt, J. and Massey, V. (1994) Studies of the reductive half-reaction of milk xanthine dehydrogenase J. Biol. Chem. 269, 18904-18914
119. Opie, L. H. (1976) Effects of regional ischemia on metabolism of glucose and fatty acids. Relative rates of aerobic and anaerobic energy production during myocardial infarction and comparison with effects of anoxia Circ. Res. 38, 152-174
120. Cobbe, S. M. and Poole-Wilson, P. A. (1980) Tissue acidosis in myocardial hypoxia J. Mol. Cell. Cardiol. 12, 761-770
121. Momomura, S., Ingwall, J. S., Parker, J. A., Sahagian, P., Ferguson, J. J., and Grossman, W. (1985) The relationships of high energy phosphates, tissue pH, and regional blood flow to diastolic distensibility in the ischemic dog myocardium Circ. Res. 57, 822-835
122. Zweier, J. L., Wang, P., Samouilov, A., and Kuppusamy, P. (1995) Enzyme-independent formation of nitric oxide in biological tissues Nat. Med. 1, 804-809
123. Samouilov, A., Kuppusamy, P., and Zweier, J. L. (1998) Evaluation of the magnitude and rate of nitric oxide production from nitrite in biological systems Arch. Biochem. Biophys. 357, 1-7
124. Zweier, J. L., Samouilov, A., and Kuppusamy, P. (1999) Non-enzymatic nitric oxide synthesis in biological systems Biochim. Biophys. Acta 1411, 250-262
125. Gorenflo, M., Zheng, C., Poge, A., Bettendorf, M., Werle, E., and Fiehn, W. (2001) Metabolites of the L-arginine-NO pathway in patients with left-to-right shunt Clin. Lab. 47, 441-447
126. Rodriguez, J., Maloney, R. E., Rassaf, T., Bryan, N. S., and Feelisch, M. (2003) Chemical nature of nitric oxide storage forms in rat vascular tissue Proc. Natl. Acad. Sci. U.S.A. 100, 336-341
127. Bryan, N. S., Rassaf, T., Maloney, R. E., Rodriguez, C. M., Saijo, F., Rodriguez, J. J., and Feelisch, M. (2004) Cellular targets and mechanisms of nitros(yl)ation: An insight into their nature and kinetics in vivo Proc. Natl. Acad. Sci. U.S.A. 101, 4308-4313
128. Shiva, S. and Gladwin, M. T. (2009) Shining a light on tissue NO stores: Near infrared release of NO from nitrite and nitrosylated hemes J. Mol. Cell. Cardiol. 46, 1-3
129. Kim, J. H., Ryan, M. G., Knaut, H., and Hille, R. (1996) The reductive half-reaction of xanthine oxidase: The involvement of prototropic equilibria in the course of the catalytic sequence J. Biol. Chem. 271, 6771-6780
130. Xia, M., Dempski, R., and Hille, R. (1999) The reductive half-reaction of xanthine oxidase: Reaction with aldehyde substrates and identification of the catalytically labile oxygen J. Biol. Chem. 274, 3323-3330
131. Koppenol, W. H. (1998) The basic chemistry of nitrogen monoxide and peroxynitrite Free Radical Biol. Med. 25, 385-391
132. Klug, D., Rabani, J., and Fridovich, I. (1972) A direct demonstration of the catalytic action of superoxide dismutase through the use of pulse radioiysis J. Biol. Chem. 247, 4839-4842
133. Fridovich, I. (1982) Measuring the activity of superoxide dismutases: An embarrassment of riches. In Superoxide dismuatase (Oberley, L. W., Ed.) Vol. 1, pp 69-88, CRC Press, Bora Raton, FL.
134. Ward, J. P. T. (2008) Oxygen sensors in context Biochim. Biophys. Acta 1777, 1-14
135. Williamson, J. R., Steenbergen, C., Rich, T., Deleeuw, G., Barlow, C., and Chance, B. (1977) The nature of ischemic injury in cardiac tissue. In Pathophysiology and Therapeutics of Myocardial Ischemia, pp 193-225, Spectrum Publications Inc., New York.
136. Kobayashi, K. and Neely, J. R. (1983) Effects of ischemia and reperfusion on pyruvate dehydrogenase activity in isolated rat hearts J. Mol. Cell. Cardiol. 15, 359-367
137. Williamson, J. R. (1996) Glycolytic control mechanisms. II. Kinetics of intermediate changes during the aerobic-anoxic transitions in perfused rat heart J. Biol. Chem. 241, 5026-5036
138. 2+], and NADH with dysfunction after global ischemia in intact hearts Am. J. Physiol. 280, H280-H293
139. Lartigue-Mattei, C., Chabard, J. L., Bargnoux, H., Petit, J., Berger, J. A., Ristori, J. M., Bussiere, J. L., Catilina, P., and Catilina, M. J. (1990) Plasma and blood assay of xanthine and hypoxanthine by gas chromatography-mass spectrometry: Physiological variations in humans J. Chromatogr. 529, 93-101
140. Himmel, H. M., Sadony, V., and Ravens, U. (1991) Quantitation of hypoxanthine in plasma from patients with ischemic heart disease: Adaption of a high-performance liquid chromatographic method J. Chromatogr. 568, 105-115
141. Quinlan, G. J., Lamb, N. J., Tilley, R., Evans, T. W., and Gutteridge, J. M. (1997) Plasma hypoxanthine levels in ARDS: Implications for oxidative stress, morbidity, and mortality Am. J. Respir. Crit. Care Med. 155, 479-484
142. Pesonen, E. J., Linder, N., Raivio, K. O., Sarnesto, A., Lapatto, R., Hockerstedt, K., Makisalo, H., and Andersson, S. (1998) Circulating xanthine oxidase and neutrophil activation during human liver transplantation Gastroenterology 114, 1009-1015
143. Kojima, H., Nakatsubo, N., Kikuchi, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y., and Nagano, T. (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: Diaminofluoresceins Anal. Chem. 70, 2446-2453
144. Ye, X., Rubakhin, S. S., and Sweedler, J. V. (2008) Detection of nitric oxide in single cells Analyst 133, 423-433
145. 4 in aqueous solution J. Am. Chem. Soc. 92, 5821-5828
146. Lee, K. Y., Kuchynka, D. J., and Kochi, J. K. (1990) Redox equilibria of the nitrosonium cation and of its nonbonded complexes Inorg. Chem. 29, 4196-4204
147. Ignarro, L. J., Fukuto, J. M., Griscavage, J. M., Rogers, N. E., and Byrns, R. E. (1993) Oxidation of nitric oxide in aqueous solution to nitrite but not nitrate: Comparison with enzymatically formed nitric oxide from l -arginine Proc. Natl. Acad. Sci. U.S.A. 90, 8103-8107
148. 2 in wäβriger Lösung Ber. Bunsen-Ges. 74, 488-492
149. Ford, P. C. and Lorkovic, I. M. (2002) Mechanistic aspects of the reactions of nitric oxide with transition-metal complexes Chem. Rev. 102, 993-1018
150. Roy, S., Khanna, S., Bickerstaff, A. A., Subramanian, S. V., Atalay, M., Bierl, M., Pendyala, S., Levy, D., Sharma, N., Venojarvi, M., Strauch, A., Orosz, C. G., and Sen, C. K. (2003) Oxygen sensing by primary cardiac fibroblasts: A key role of p21(Waf1/Cip1/Sdi1) Circ. Res. 92, 264-271
151. Okamoto, K., Matsumoto, K., Hille, R., Eger, B. T., Pai, E. F., and Nishino, T. (2004) The crystal structure of xanthine oxidoreductase during catalysis: Implications for reaction mechanism and enzyme inhibition Proc. Natl. Acad. Sci. U.S.A. 101, 7931-7936
152. Pauff, J. M., Zhang, J., Bell, C. E., and Hille, R. (2008) Substrate orientation in xanthine oxidase: Crystal structure of enzyme in reaction with 2-hydroxy-6-methylpurine J. Biol. Chem. 283, 4818-4824
153. Burgrnayer, S. J. N. and Stlefel, E. I. (1985) Molybdenum enzymes, cofactors, and model systems: The chemical uniqueness of molybdenum J. Chem. Educ. 62, 943-953
154. Harlan, E. E., Berg, J. M., and Holm, R. H. (1986) Thermodynamic fitness of molybdenum(IV,VI) complexes for oxygen atom transfer reactions, including those with enzymatic substrates J. Am. Chem. Soc. 108, 6992-7000
155. Stiefel, E. I. (1973) Proposed molecular mechanism for the action of molybdenum in enzymes: Coupled proton and electron transfer Proc. Natl. Acad. Sci. U.S.A. 70, 988-992
156. Rajapakshe, A., Snyder, R. A., Astashkin, A. V., Bernardson, P., Evans, D. J., Young, C. G., Evans, D. H., and Enemark, J. H. (2009) Insights into the nature of Mo(V) species in solution: Modeling catalytic cycles for molybdenum enzymes Inorg. Chim. Acta 362, 4603-4608
157. Ghosh, S., Dey, A., Sun, Y., Scholes, C. P., and Solomon, E. I. (2009) Spectroscopic and computational studies of nitrite reductase: Proton induced electron transfer and backbonding contributions to reactivity J. Am. Chem. Soc. 131, 277-288
158. George, G. N. and Bray, R. C. (1988) Studies by electron paramagnetic resonance spectroscopy of xanthine oxidase enriched with molybdenum-95 and with molybdenum-97 Biochemistry 27, 3603-3609
159. Wilson, G. L., Greenwood, R. J., Pilbrow, J. R., Spence, J. T., and Wedd, A. G. (1991) Molybdenum(V) sites in xanthine oxidase and relevant analogue complexes: Comparison of molybdenum-95 and sulfur-33 hyperfine coupling J. Am. Chem. Soc. 113, 6803-6812
160. Doonan, C. J., Rubie, N. D., Peariso, K., Harris, H. H., Knottenbelt, S. Z., George, G. N., Young, C. C., and Kirk, M. L. (2008) Electronic structure description of the cis-MoOS unit in models for molybdenum hydroxylases J. Am. Chem. Soc. 130, 55-65
161. Hille, R. (2002) Molybdenum and tungsten in biology Trends Biochem. Sci. 27, 360-367
162. Schwarz, G., Mendel, R. R., and Ribbe, M. W. (2009) Molybdenum cofactors, enzymes and pathways Nature 460, 839-847
163. Hille, R. and Mendel, R. (2011) Molybdenum in living systems Coord. Chem. Rev. 255, 991-992
164. Mendel, R. and Kruse, T. (2012) Cell biology of molybdenum in plants and humans Biochim. Biophys. Acta 1823, 1568-1579