Evidence for a transient peroxynitro acid in the reaction catalyzed by nitronate monooxygenase with propionate 3-nitronate

Biochemistry

Volumn 52, Issue 15, 2013, Pages 2694-2704

  Smitherman, Crystal ^a   Gadda, Giovanni ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORBANCE SPECTROSCOPY; ANAEROBIC REDUCTION; ENVIRONMENTAL OCCURRENCE; NEUROLOGICAL DISORDERS; PHYSIOLOGICAL SUBSTRATE; REACTION CATALYZED; STEADY-STATE KINETICS; SUCCINATE DEHYDROGENASE;

CATALYSIS; ENZYME INHIBITION; KINETICS; OXYGEN; PH EFFECTS; PHYSIOLOGY; VISCOSITY; VOLATILE FATTY ACIDS;

REACTION KINETICS;

FUMARATE HYDRATASE; NITRIC ACID DERIVATIVE; NITRONATE MONOOXYGENASE; PEROXYNITRO ACID; PROPIONATE 3 NITRONATE; SUCCINATE DEHYDROGENASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; CATALYSIS; CHEMICAL ANALYSIS; CHEMICAL REACTION; CHEMICAL STRUCTURE; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME STRUCTURE; NEUROLOGIC DISEASE; PH; PRIORITY JOURNAL; STEADY STATE;

DIOXYGENASES; HYDROGEN-ION CONCENTRATION; KINETICS; NITRO COMPOUNDS; PROPIONATES; SOLVENTS; SPECTRUM ANALYSIS; VISCOSITY; WILLIOPSIS;

FUNGI;

EID: 84876230472     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400030d     Document Type: Article

References (55)

1. Gadda, G. and Francis, K. (2010) Nitronate monooxygenase, a model for anionic flavin semiquinone intermediates in oxidative catalysis Arch. Biochem. Biophys. 493, 53-61
2. Mijatovic, S. and Gadda, G. (2008) Oxidation of alkyl nitronates catalyzed by 2-nitropropane dioxygenase from Hansenula mrakii Arch. Biochem. Biophys. 473, 61-68
3. Francis, K., Russell, B., and Gadda, G. (2005) Involvement of a flavosemiquinone in the enzymatic oxidation of nitroalkanes catalyzed by 2-nitropropane dioxygenase J. Biol. Chem. 280, 5195-5204
4. Francis, K. and Gadda, G. (2006) Probing the chemical steps of nitroalkane oxidation catalyzed by 2-nitropropane dioxygenase with solvent viscosity, pH, and substrate kinetic isotope effects Biochemistry 45, 13889-13898
5. Francis, K. and Gadda, G. (2008) The nonoxidative conversion of nitroethane to ethylnitronate in Neurospora crassa 2-nitropropane dioxygenase is catalyzed by histidine 196 Biochemistry 47, 9136-9144
6. Francis, K. and Gadda, G. (2009) Inflated kinetic isotope effects in the branched mechanism of Neurospora crassa 2-nitropropane dioxygenase Biochemistry 48, 2403-2410
7. Francis, K., Nishino, S. F., Spain, J. C., and Gadda, G. (2012) A novel activity for fungal nitronate monooxygenase: detoxification of the metabolic inhibitor propionate-3-nitronate Arch. Biochem. Biophys. 521, 84-89
8. Ha, J. Y., Min, J. Y., Lee, S. K., Kim, H. S., Kim do, J., Kim, K. H., Lee, H. H., Kim, H. K., Yoon, H. J., and Suh, S. W. (2006) Crystal structure of 2-nitropropane dioxygenase complexed with FMN and substrate. Identification of the catalytic base J. Biol. Chem. 281, 18660-18667
9. Alston, T. A., Mela, L., and Bright, H. J. (1977) 3-Nitropropionate, the toxic substance of Indigofera, is a suicide inactivator of succinate dehydrogenase Proc. Natl. Acad. Sci. U. S. A. 74, 3767-3771
10. Coles, C. J., Edmondson, D. E., and Singer, T. P. (1979) Inactivation of succinate dehydrogenase by 3-nitropropionate J. Biol. Chem. 254, 5161-5167
11. Huang, L. S., Sun, G., Cobessi, D., Wang, A. C., Shen, J. T., Tung, E. Y., Anderson, V. E., and Berry, E. A. (2006) 3-nitropropionic acid is a suicide inhibitor of mitochondrial respiration that, upon oxidation by complex II, forms a covalent adduct with a catalytic base arginine in the active site of the enzyme J. Biol. Chem. 281, 5965-5972
12. Porter, D. J. and Bright, H. J. (1980) 3-Carbanionic substrate analogues bind very tightly to fumarase and aspartase J. Biol. Chem. 255, 4772-4780
13. Scallet, A. C., Nony, P. L., Rountree, R. L., and Binienda, Z. K. (2001) Biomarkers of 3-nitropropionic acid (3-NPA)-induced mitochondrial dysfunction as indicators of neuroprotection Ann. N.Y. Acad. Sci. 939, 381-392
14. Ludolph, A. C., He, F., Spencer, P. S., Hammerstad, J., and Sabri, M. (1991) 3-Nitropropionic acid-exogenous animal neurotoxin and possible human striatal toxin Can. J. Neurol. Sci. 18, 492-498
15. Pang, Z. and Geddes, J. W. (1997) Mechanisms of cell death induced by the mitochondrial toxin 3-nitropropionic acid: acute excitotoxic necrosis and delayed apoptosis J. Neurosci. 17, 3064-3073
16. Burdock, G. A., Carabin, I. G., and Soni, M. G. (2001) Safety assessment of B-nitropropionic acid: a monograph in support of an acceptable daily intake in humans Food Chem. 75, 1-27
17. Ming, L. (1995) Moldy sugarcane poisoning - a case report with a brief review J. Toxicol. Clin. Toxicol. 33, 363-367
18. Hamilton, B. F., Gould, D. H., and Gustine, D. L. (2000) History of 3-nitropropionic acid, in Mitochondrial Inhibitors and Neurodegenerative Disorders Comptemporary Neuroscience, Humana Press, Totowa, NJ.
19. Mathews, F. P. (1940) The toxicity of red-stemmed peavine (Astragalus emoryanus) for cattle, sheep, and goats J. Am. Vet. Med. Assoc. 97, 125-134
20. Liu, X., Luo, X., and Hu, W. (1992) Studies on the epidemiology and etiology of moldy sugarcane poisoning in China Biomed. Environ. Sci. 5, 161-177
21. Beal, M. F., Brouillet, E., Jenkins, B. G., Ferrante, R. J., Kowall, N. W., Miller, J. M., Storey, E., Srivastava, R., Rosen, B. R., and Hyman, B. T. (1993) Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid J. Neurosci. 13, 4181-4192
22. Guyot, M. C., Hantraye, P., Dolan, R., Palfi, S., Maziere, M., and Brouillet, E. (1997) Quantifiable bradykinesia, gait abnormalities and Huntington's disease-like striatal lesions in rats chronically treated with 3-nitropropionic acid Neuroscience 79, 45-56
23. Tsang, T. M., Haselden, J. N., and Holmes, E. (2009) Metabonomic characterization of the 3-nitropropionic acid rat model of Huntington's disease Neurochem. Res. 34, 1261-1271
24. Francis, K. and Gadda, G. (2009) Kinetic evidence for an anion binding pocket in the active site of nitronate monooxygenase Bioorg. Chem. 37, 167-172
25. Bush, M. T., Touster, O., and Brockman, J. E. (1951) The production of beta-nitropropionic acid by a strain of Aspergillus flavus J. Biol. Chem. 188, 685-693
26. Lewis, R. J. (1996) Sax's Dangerous Properties of Industrial Materials, 9 th ed., Van Nostrand Reinhold, New York.
27. Nielsen, A. T. (1969) Nitronic acids and esters, in The Chemistry of the Nitro and Nitroso Groups (Feuer, H., Ed.), pp 349-486, Interscience Publishers, New York.
28. Lide, D. R. (2000) Handbook of Chemistry and Physics, 6 th ed., CRC Press, Boca Raton, FL.
29. Segel, I. H. (1975) Enzyme Kinetics, Wiley, New York.
30. Kuo, C. F. and Fridovich, I. (1986) Free-radical chain oxidation of 2-nitropropane initiated and propagated by superoxide Biochem. J. 237, 505-510
31. Massey, V. and Palmer, G. (1966) On the existence of spectrally distinct classes of flavoprotein semiquinones. A new method for the quantitative production of flavoprotein semiquinones Biochemistry 5, 3181-3189
32. Ghanem, M., Fan, F., Francis, K., and Gadda, G. (2003) Spectroscopic and kinetic properties of recombinant choline oxidase from Arthrobacter globiformis Biochemistry 42, 15179-15188
33. Job, V., Marcone, G. L., Pilone, M. S., and Pollegioni, L. (2002) Glycine oxidase from Bacillus subtilis. Characterization of a new flavoprotein J. Biol. Chem. 277, 6985-6993
34. Gadda, G., Wels, G., Pollegioni, L., Zucchelli, S., Ambrosius, D., Pilone, M. S., and Ghisla, S. (1997) Characterization of cholesterol oxidase from Streptomyces hygroscopicus and Brevibacterium sterolicum Eur. J. Biochem. 250, 369-376
35. Dougherty, R. C. (1998) Temperature and pressure dependence of hydrogen bond strength: A perturbation molecular orbital approach J. Chem. Phys. 109, 7372-7378
36. Jaenicke, R. (1990) Protein structure and function at low temperatures Philos. Trans. R. Soc. London, B 326, 535-551; discussion: 551-553
37. Cordier, F. and Grzesiek, S. (2002) Temperature-dependence of protein hydrogen bond properties as studied by high-resolution NMR J. Mol. Biol. 317, 739-752
38. Takahashi, K., Numata, N., Kinoshita, N., Utoguchi, N., Mayumi, T., and Mizuno, N. (2004) Characterization of the influence of nitric oxide donors on intestinal absorption of macromolecules Int. J. Pharm. 286, 89-97
39. Kelm, M., Dahmann, R., Wink, D., and Feelisch, M. (1997) The nitric oxide/superoxide assay. Insights into the biological chemistry of the NO/O-2. interaction J. Biol. Chem. 272, 9922-9932
40. Bamdad, F., Wu, J., and Chen, L. (2011) Effects of enzymatic hydrolysis on molecular structure and antioxidant activity of barley hordein J. Cereal Sci. 54, 20-28
41. Evans, J. P., Niemevz, F., Buldain, G., and de Montellano, P. O. (2008) Isoporphyrin intermediate in heme oxygenase catalysis. Oxidation of alpha-meso-phenylheme J. Biol. Chem. 283, 19530-19539
42. Fielden, E. M., Roberts, P. B., Bray, R. C., Lowe, D. J., Mautner, G. N., Rotilio, G., and Calabrese, L. (1974) Mechanism of action of superoxide dismutase from pulse radiolysis and electron paramagnetic resonance. Evidence that only half the active sites function in catalysis Biochem. J. 139, 49-60
43. Maehly, A. C. and Chance, B. (1954) The assay of catalases and peroxidases Methods Biochem. Anal. 1, 357-424
44. Hasinoff, B. B. (1984) Kinetics of carbonic anhydrase catalysis in solvents of increased viscosity: a partially diffusion-controlled reaction Arch. Biochem. Biophys. 233, 676-681
45. Quinn, D. M. (1987) Acetylcholinesterase: Enzyme structure, reaction dynamics, and virtual transition states Chem. Rev. 87, 955-979
46. Waterson, R. M. and Hill, R. L. (1972) Enoyl coenzyme A hydratase (crotonase). Catalytic properties of crotonase and its possible regulatory role in fatty acid oxidation J. Biol. Chem. 247, 5258-5265
47. Sweet, W. L. and Blanchard, J. S. (1990) Fumarase: viscosity dependence of the kinetic parameters Arch. Biochem. Biophys. 277, 196-202
48. Blacklow, S. C., Raines, R. T., Lim, W. A., Zamore, P. D., and Knowles, J. R. (1988) Triosephosphate isomerase catalysis is diffusion controlled. Appendix: Analysis of triose phosphate equilibria in aqueous solution by 31P NMR Biochemistry 27, 1158-1167
49. Christensen, H., Martin, M. T., and Waley, S. G. (1990) Beta-lactamases as fully efficient enzymes. Determination of all the rate constants in the acyl-enzyme mechanism Biochem. J. 266, 853-861
50. Brouwer, A. C. and Kirsch, J. F. (1982) Investigation of diffusion-limited rates of chymotrypsin reactions by viscosity variation Biochemistry 21, 1302-1307
51. Wilcox, P. E. (1970) Chymotrypsinogens-chymotrypsins Methods Enzymol. 19, 64-108
52. Gadda, G., Powell, N. L., and Menon, P. (2004) The trimethylammonium headgroup of choline is a major determinant for substrate binding and specificity in choline oxidase Arch. Biochem. Biophys. 430, 264-273
53. Quaye, O., Lountos, G. T., Fan, F., Orville, A. M., and Gadda, G. (2008) Role of Glu312 in binding and positioning of the substrate for the hydride transfer reaction in choline oxidase Biochemistry 47, 243-256
54. Little, H. N. (1951) Oxidation of nitroethane by extracts from Neurospora J. Biol. Chem. 193, 347-358
55. Nishino, S. F., Shin, K. A., Payne, R. B., and Spain, J. C. (2010) Growth of bacteria on 3-nitropropionic acid as a sole source of carbon, nitrogen, and energy Appl. Environ. Microbiol. 76, 3590-3598