First evidence for an LDL- and HDL-associated nitratase activity that denitrates albumin-bound nitrotyrosine-Physiological consequences (original) (raw)
Abstract
In the systemic circulation, LDL occurs in the form of a weakly nitrated LDL-albumin complex (LAC). The question here is whether LAC (or HDL) is able to denitrate the albumin-bound 3-NO 2 -tyrosine (3NT). Nitrated albumin was incubated in the presence of lipoprotein fraction (LPF) to be tested, with or without Ca 21 . After precipitation and centrifugation, supernatants (SNs) and protein pellets (PP) were collected. HCl proteolysis was carried out with deuterated 3NT as an internal standard, and amino acids were derivatized for GC-MS analysis, whereas SNs were used for NO 2 2 /NO 3 2 -fluorimetric assays. A loss of 3NT, higher with albumin-low LDL than with albumin-rich LDL or HDL, was found in PP only in the presence of Ca 21 . c-Tocopherol loading of LPF inhibited 3NT loss. 3NT loss was found for the first time to be stoichiometrically equivalent to NO 3 2 , proving that the 3NT loss must be ascribed to a 3NT-denitrating nitratase activity. 3NT loss and NO 3 2 production that clearly cannot be attributed to PON-1 were impaired by D-penicillamine and phenylacetate, inhibitor, and substrate of PON-1, respectively, leading to speculate on the active site. Finally, nitratase activity and albumin contribute to beneficially convert peroxynitrite (ONOO 2 ) into nonbioactive NO 3 2 . But, in inflammatory conditions, xanthine oxidoreductase is expressed leading to detrimentally reduce O 2 and NO 3 2 into O 2 2 and NO that may interact, reconstituting the ONOO 2 pool. The real consequence of nitratase activity and the physiological significance of nitration/denitration processes remain to be explored.
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References (40)
- Knowles, R. G., and Moncada, S. (1994) Nitric oxide synthases in mammals. Biochem. J. 298, 249-258.
- Moncada, S., and Higgs, A (1993) The L-arginine-nitric oxide pathway. Engl. J. Med. 329, 2002-2012.
- Huie, R. E., and Padmaja, S. (1993) The reaction of NO with superox- ide.
- Free Radic. Res. Commun. 18, 195-199.
- Beckman, J. S., Chen, J., Ischiropoulos, H., and Crow J. P. (1994) Oxi- dative chemistry of peroxynitrite. Methods Enzymol. 233, 229-240.
- Ohshima, H., Friesen, M., Brouet, I., and Bartsch, H. (1990) Nitrotyro- sine as a new marker for endogenous nitrosation and nitration of pro- tein. Food Chem. Toxicol. 28, 647-652.
- Shaklai, N., Garlick, R. L., and Bunn, H. F. (1984) Nonenzymatic gly- cosylation of human serum albumin alters its conformation and func- tion. J. Biol. Chem. 259, 3812-3817.
- Coussons, P. J., Jacoby, J., McKay, A., Kelly, S. M., Price, N. C., and Hunt, J. V. (1997) Glucose modification of human serum albumin: a structural study. Free Radic. Biol. Med. 22, 1217-1227.
- Peters, T. (1996) All About Albumin: Biochemistry, Genetics, and Medi- cal Applications. Academic Press, New York.
- Jiao, K., Mandapati, S., Skipper, P. L., Tannenbaum, S. R., and Wish- nok, J. S. (2001) Site-selective nitration of tyrosine in human serum albumin by peroxynitrite. Anal. Biochem. 293, 43-52.
- Torres-Rasgado, E., Fouret, G., Carbonneau, M. A., and Le ´ger, C. L. (2007) Peroxynitrite mild nitration of albumin and LDL-albumin com- plex naturally present in plasma and tyrosine nitration rate-albumin impairs LDL nitration. Free Radic. Res. 41, 367-375.
- Irie, Y., Saeki, M., Kamisaki, Y., Martin, E., and Murad, F. (2003). His- tone H1.2 is a substrate for denitrase, an activity that reduces nitrotyro- sine immunoreactivity in proteins. Proc. Natl. Acad. Sci. USA 100, 5634-5639.
- Aulak, K. S., Koeck, T., Crabb, J. W., and Stuehr, D. J. (2004). Dynam- ics of protein nitration in cells and mitochondria. Am. J. Physiol. Heart Circ. Physiol. 286, H30-H38.
- Kuo, W. N., Kanadia, R. N., Shanbhag, V. P., and Toro, R. (1999) Denitration of peroxynitrite-treated proteins by 'protein nitratases' from rat brain and heart. Mol. Cell. Biochem. 201, 11-16.
- Carbonneau, M. A., Cartron E., Le ´ger, C. L., Senglat, C., and Descomps, B. (2002) New insight on the relationship between LDL composition, associated proteins, oxidative resistance and preparation procedure. Free Radic. Res. 36, 127-142.
- Cartron, E., Carbonneau, M. A., Fouret, G., Descomps, B., and Le ´ger, C. L. (2001) Specific antioxidant activity of caffeoyl derivatives and other natural phenolic compounds: LDL protection against oxidation and decrease in the proinflammatory lysophophatidylcholine production. J. Nat. Prod. 64, 480-486.
- Sokolovsky, M., Riordan, J. F., and Vallee, B. L. (1966) Tetranitro- methane. A reagent for the nitration of tyrosyl residues in proteins. Bio- chemistry 5, 3582-3589.
- Crowley, J. R., Yarasheski, K., Leeuwenburg, C., Turk, J., and Heineck- eby, J. W. (1998) Isotope dilution mass spectrometric quantification of 3-nitrotyrosine in proteins and tissues is facilitated by reduction to 3- aminotyrosine. Anal. Biochem. 259, 127-135.
- Ohshima, H., Celan, I., Chazotte, L., Pignateli, B., and Mower, H. F. (1999) Analysis of 3-nitrotyrosine in biological fluids and protein hydrolyzates by high-performance liquid chromatography using a postseparation, on-line reduction column and electrochemical detec- tion: results with various nitrating agents. Nitric Oxide 3, 132- 141.
- Steinbrecher, U. P., Zhang, H., and Lougheed, M. (1990) Role of oxida- tively modified LDL in atherosclerosis. Free Radic. Biol. Med. 9, 155- 168.
- Steinberg, D. (1997) Low density lipoprotein oxidation and its patholog- ical significance. J. Biol. Chem. 272, 20963-20966.
- Auge ´, N., Nikolova-Karakashian, M., Carpentier, S., Parthasarathy, S., Ne `gre-Salvayre, A., Salvayre, R., Merrill, A. H., Jr., and Levade, T. (1999) Role of sphingosine 1-phophate in the mitogenesis induced by oxidized low density lipoprotein in smooth muscle cells via activation of sphingomyelinase, ceramidase, and shipngosine kinase. J. Biol. Chem. 274, 31533-31538.
- Parthasarathy, S., and Rankin, S. M. (1992) Role of oxidized low-den- sity lipoprotein in atherogenesis. Prog. Lipid. Res. 31, 127-143.
- Darley, U. V. M., Hogg, N., O'Leary, V. J., Wilson, M. T., and Mon- cada, S. (1992) The simultaneous generation of superoxide and nitric oxide can initiate lipid peroxidation in human low-density lipoprotein. Free Radic. Res. Commun. 17, 9-20.
- Patel, R. P., Diezfalusy, U., Dzeletovic, S., Wilson, M. T., and Darley, U. V. M. (1996) Formation of oxysterols during oxidation of low- density lipoprotein by peroxynitrite, myoglobin, and copper. J. Lipid Res. 37, 2361-2371.
- Shafiee, M., Carbonneau, M. A., Urban, N., Descomps, B., and Le ´ger, C. L. (2003) Grape and grape speed extract capacities at protecting LDL against oxidation generated by Cu 21 , AAPH or SIN-1 and at decreasing superoxide THP-1 cell production. A comparison to other extracts or compounds. Free Radic. Res. 37, 573-584.
- Hogg, N., Darley, U. V. M., Wilson, M. T., and Moncada, S. (1999) The oxidation of a-tocopherol in human low-density lipoprotein by the simultaneous generation of superoxide and nitric oxide. FEBS Lett. 326, 199-203.
- Leeuwenburgh, C., Hardy, M. M., Hazen, S. L., Wagner, P., Ohishi, S., Steinbrecher, U. P., and Heinecke, J. W. (1997) Reactive nitrogen inter- mediates promote low-density lipoprotein oxidation in human athero- sclerotic intima. J. Biol. Chem. 272, 1433-1436.
- Graham, A., Hogg, N., Kalyanaraman, B., O'Leary, V., Darley, U. V. M., and Moncada, S. (1993) Peroxynitrite modification of low-density lipoprotein leads to recognition by the macrophage scavenger receptor. FEBS Lett. 330, 181-185.
- Dabbagh, A., and Frei, B. (1995) Human suction blister interstitial fluid prevents metals ions-dependant oxidation of low-density lipo- protein by macrophages and in cell-free systems. J. Clin. Invest. 96, 1958-1966.
- Jakubowski, H. (2000) Calcium-dependent human serum homocysteine thiolactone hydrolase. J. Biol. Chem. 275, 3957-3962.
- Kamisaki, Y., Wada, K., Bian, K, Balabanli, B., Davis, K., Martin, E., Behbod, F., Lee, Y.-C., and Murad, F. (1998) An activity in rat tissues that modifies nitrotyrosine-containing proteins. Proc. Natl. Acad. Sci. USA 95, 11584-11589.
- Gruijthuijsen, Y. K., Grieshuber, I., Stocklinger, A, Tischler, U., Fehrenbach, T., Weller, M. G., Vogel, L., Vieths, S., Po ¨schl, U., and Duschl, A. (2006) Nitration enhances the allergenic potential of pro- teins. Int. Arch. Allergy Immunol. 141, 265-275.
- Predescu, D., Pedrescu, S., and Malik, A. B. (2002) Transport of nitrated albumin across continuous vascular endothelium. Proc. Natl. Acad. Sci. USA 99, 13932-13937.
- Ohara, Y., Peterson, T. E., and Harrison, D. G. (1993) Hypercholestero- lemia increases endothelial superoxide anion production. J. Clin. Invest. 91, 2546-2551.
- Godber, B. L. J., Doel, J. J., Goult, T. A., Eisenthal, R., and Harrison, R. (2001) Suicide inactivation of xanthine oxidoreductase during reduc- tion of inorganic nitrite to nitric oxide. Biochem. J. 358, 325-333.
- Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., and Blake, D. R. (1998) Xanthine oxidoreductase catalyses the reduc- tion of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Lett. 427, 225-228.
- Lee, C., Liu, X., and Zweier, J. L. (2000) Regulation of xanthine oxi- dase by nitric oxide and peroxynitrite. J. Biol. Chem. 275, 9369-9376.
- Christen, S., Woodall, A. A., Shigenaga, M. K., Southwell-Keely, P. T., Duncan, M. W., and Ames, B. N. (1997) c-Tocopherol traps mutagenic electrophilies such as NOx and complements a-tocopherol: physiologi- cal implications. Proc. Natl. Acad. Sci. USA 94, 3217-3222.
- Kong, S.-K., Yim, M. B., Stadtman, E. R., and Chock, P. B. (1996). Peroxynitrite disables the tyrosine phosphorylation regulatory mecha- nism: lymphocyte-specific tyrosine kinase fails to phosphorylate nitrated cdc2(6-20)NH 2 peptide. Proc. Natl. Acad. Sci. USA 93, 3377-3382.