Reactive Nitrogen Species (RNS)-resistant microbes: Adaptation and medical implications

Biological Chemistry

Volumn 398, Issue 11, 2017, Pages 1193-1208

  Tharmalingam, Sujeenthar ^a   Alhasawi, Azhar ^a   Appanna, Varun P ^a   Lemire, Joe ^b   Appanna, Vasu D ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

ATP; Metabolism; Phosphotransfer; Reactive nitrogen species; RNS resistant microbes; keto acids

Indexed keywords

ANTIINFECTIVE AGENT; REACTIVE NITROGEN SPECIES;

ANIMAL; ANTIBIOTIC RESISTANCE; BACTERIUM; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; DRUG RESISTANCE, BACTERIAL; HUMANS; REACTIVE NITROGEN SPECIES;

EID: 85032467733     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2017-0152     Document Type: Review

References (112)

1. Afanas’ev, I.B. (2007). Signaling functions of free radicals superoxide & nitric oxide under physiological & pathological conditions. Mol. Biotechnol. 37, 2–4.
2. Alhasawi, A., Auger, C., Appanna, V.P., Chahma, M., and Appanna, V.D. (2014). Zinc toxicity and ATP production in Pseudomonas fluorescens. J. Appl. Microbiol. 117, 65–73.
3. Alhasawi, A., Leblanc, M., Appanna, N.D., Auger, C., and Appanna, V.D. (2015). Aspartate metabolism and pyruvate homeostasis triggered by oxidative stress in Pseudomonas fluorescens: a functional metabolomic study. Metabolomics 11, 1792–1801.
4. Alderton, W.K., Cooper, C.E., and Knowles, R.G. (2001). Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357, 593–615.
5. Andersson, E., Schain, F., Svedling, M., Claesson, H.E., and Forsell, P.K. (2006). Interaction of human 15-lipoxygenase-1 with phosphatidylinositol bisphosphates results in increased enzyme activity. Biochim. Biophys. Acta. 1761, 1498–1505.
6. Andrae, U., Singh, J., and Ziegler-Skylakakis, K. (1985). Pyruvate and related alpha-ketoacids protect mammalian cells in culture against hydrogen peroxide-induced cytotoxicity. Toxicol. Lett. 28, 93–98.
7. Anjum, M.F., Stevanin, T.M., Read, R.C., and Moir, J.W. (2002). Nitric oxide metabolism in Neisseria meningitidis. J. Bacteriol. 184, 2987–2993.
8. Appanna, V.P., Auger, C., Thomas, S.C., and Omri, A. (2014). Fumarate metabolism and ATP production in Pseudomonas fluorescens exposed to nitrosative stress. Antonie Van Leeuwenhoek 106, 431–438.
9. Appanna, V.P., Alhasawi, A.A., Auger, C., Thomas, S.C., and Appanna, V.D. (2016). Phospho-transfer networks and ATP homeostasis in response to an ineffective electron transport chain in Pseudomonas fluorescens. Arch. Biochem. Biophys. 606, 26–33.
10. Aratani, Y., Kura, F., Watanabe, H., Akagawa, H., Takano, Y., Suzuki, K., Dinauer, M.C., Maeda, N., and Koyama, H. (2002). Relative contributions of myeloperoxidase and NADPH-oxidase to the early host defense against pulmonary infections with Candida albicans and Aspergillus fumigatus. Med. Mycol. 40, 557–563.
11. Auger, C. and Appanna, V.D. (2015). A novel ATP-generating machinery to counter nitrosative stress is mediated by substrate-level phosphorylation. Biochim. Biophys. Acta. 1850, 43–50.
12. Auger, C., Lemire, J., Cecchini, D., Bignucolo, A., and Appanna, V.D. (2011). The metabolic reprogramming evoked by nitrosative stress triggers the anaerobic utilization of citrate in Pseudomonas fluorescens. PLoS One 6, e28469.
13. Auger, C., Han, S., Appanna, V.P., Thomas, S.C., Ulibarri, G., and Appanna, V.D. (2013). Metabolic reengineering invoked by microbial systems to decontaminate aluminum: implications for bioremediation technologies. Biotechnol. Adv. 31, 266–273.
14. Baker, P.R., Schopfer, F.J., O’Donnell, V.B., and Freeman, B.A. (2009). Convergence of nitric oxide and lipid signaling: anti-inflammatory nitro-fatty acids. Free Radic. Biol. Med. 46, 989–1003.
15. Barth, K.R., Isabella, V.M., Wright, L.F., and Clark, V.L. (2009). Resistance to peroxynitrite in Neisseria gonorrhoeae. Microbiology 155, 2532–2545.
16. Batthyany, C., Schopfer, F.J., Baker, P.R., Duran, R., Baker, L.M., Huang, Y., Cervenansky, C., Branchaud, B.P., and Freeman, B.A. (2006). Reversible post-translational modification of proteins by nitrated fatty acids in vivo. J. Biol. Chem. 281, 20450–20463.
17. Bayliak, M.M., Shmihel, H.V., Lylyk, M.P., Vytvytska, O.M., Storey, J.M., Storey, K.B., and Lushchak, V.I. (2015). Alpha-ketoglutarate attenuates toxic effects of sodium nitroprusside and hydrogen peroxide in Drosophila melanogaster. Environ. Toxicol. Pharmacol. 40, 650–659.
18. Benthin, G., Bjorkhem, I., Breuer, O., Sakinis, A., and Wennmalm, A. (1997). Transformation of subcutaneous nitric oxide into nitrate in the rat. Biochem. J. 323, 853–858.
19. Bignucolo, A., Appanna, V.P., Thomas, S.C., Auger, C., Han, S., Omri, A., and Appanna, V.D. (2013). Hydrogen peroxide stress provokes a metabolic reprogramming in Pseudomonas fluorescens: enhanced production of pyruvate. J. Biotechnol. 167, 309–315.
20. Bjorklund, G. and Chirumbolo, S. (2017). Role of oxidative stress and antioxidants in daily nutrition and human health. Nutrition 33, 311–321.
21. Bourret, T.J., Boylan, J.A., Lawrence, K.A., and Gherardini, F.C. (2011). Nitrosative damage to free and zinc-bound cysteine thiols underlies nitric oxide toxicity in wild-type Borrelia burgdorferi. Mol. Microbiol. 81, 259–273.
22. Bowman, L.A., McLean, S., Poole, R.K., and Fukuto, J.M. (2011). The diversity of microbial responses to nitric oxide and agents of nitrosative stress close cousins but not identical twins. Adv. Microb. Physiol. 59, 135–219.
23. Brune, B., Dimmeler, S., Molina y Vedia, L., and Lapetina, E.G. (1994). Nitric oxide: a signal for ADP-ribosylation of proteins. Life Sci. 54, 61–70.
24. 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. USA 101, 4308–4313.
25. Bryk, R., Griffin, P., and Nathan, C. (2000). Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407, 211–215.
26. Cadet, J. and Wagner, J.R. (2014). Oxidatively generated base damage to cellular DNA by hydroxyl radical and one-electron oxidants: similarities and differences. Arch. Biochem. Biophys. 557, 47–54.
27. Cairo, G. and Recalcati, S. (2007). Iron-regulatory proteins: molecular biology and pathophysiological implications. Expert Rev. Mol. Med. 9, 1–13.
28. Camargo, J.A. and Alonso, A. (2006). Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: A global assessment. Environ. Int. 32, 831–849.
29. Cleeter, M.W., Cooper, J.M., Darley-Usmar, V.M., Moncada, S., and Schapira, A.H. (1994). Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett. 345, 50–54.
30. Crane, B.R., Sudhamsu, J., and Patel, B.A. (2010). Bacterial nitric oxide synthases. Annu. Rev. Biochem. 79, 445–470.
31. Crawford, M.A., Henard, C.A., Tapscott, T., Porwollik, S., McClelland, M., and Vazquez-Torres, A. (2016). DksA-Dependent transcriptional regulation in Salmonella experiencing nitrosative stress. Front Microbiol. 7, 444.
32. Di Meo, S., Reed, T.T., Venditti, P., and Victor, V.M. (2016). Role of ROS and RNS sources in physiological and pathological conditions. Oxid. Med. Cell Longev. 2016, 1245049.
33. Doi, Y., Shimizu, M., Fujita, T., Nakamura, A., Takizawa, N., and Takaya, N. (2014). Achromobacter denitrificans strain YD35 pyruvate dehydrogenase controls NADH production to allow tolerance to extremely high nitrite levels. Appl. Environ. Microbiol. 80, 1910–1918. doi: 10.1128/AEM.03316-13.
34. Doi, Y. and Takaya, N. (2015). A novel A3 group aconitase tolerates oxidation and nitric oxide. J. Biol. Chem. 290, 1412–1421.
35. Everts, B., Amiel, E., van der Windt, G.J., Freitas, T.C., Chott, R., Yarasheski, K.E., Pearce, E.L., and Pearce, E.J. (2012). Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells. Blood 120, 1422–1431.
36. Flannagan, R.S., Heit, B., and Heinrichs, D.E. (2015). Antimicrobial mechanisms of macrophages and the immune evasion strategies of Staphylococcus aureus. Pathogens 4, 826–868.
37. Forstermann, U. and Sessa, W.C. (2012). Nitric oxide synthases: regulation and function. Eur. Heart J. 33, 829–837, 837a–837d.
38. Friedman, A. and Friedman, J. (2009). New biomaterials for the sustained release of nitric oxide: past, present and future. Expert Opin. Drug Deliv. 6, 1113–1122.
39. Gardner, A.M., Helmick, R.A., and Gardner, P.R. (2002). Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol. Chem. 277, 8172–8177.
40. Gladwin, M.T., Crawford, J.H., and Patel, R.P. (2004). The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radic. Biol. Med. 36, 707–717.
41. Gomes, C.M., Giuffre, A., Forte, E., Vicente, J.B., Saraiva, L.M., Brunori, M., and Teixeira, M. (2002). A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin. J. Biol. Chem. 277, 25273–25276.
42. Green, J., Rolfe, M.D., and Smith, L.J. (2014). Transcriptional regulation of bacterial virulence gene expression by molecular oxygen and nitric oxide. Virulence 5, 794–809.
43. Greenacre, S.A. and Ischiropoulos, H. (2001). Tyrosine nitration: localisation, quantification, consequences for protein function and signal transduction. Free Radic. Res. 34, 541–581.
44. Hamel, R., Appanna, V.D., Viswanatha, T., and Puiseux-Dao, S. (2004). Overexpression of isocitrate lyase is an important strategy in the survival of Pseudomonas fluorescens exposed to aluminum. Biochem. Biophys. Res. Commun. 317, 1189–1194. doi: 10.1016/j.bbrc.2004.03.157.
45. Han, S., Lemire, J., Appanna, V.P., Auger, C., Castonguay, Z., Appanna, V.D. (2013). How aluminum, an intracellular ROS generator promotes hepatic and neurological diseases: the metabolic tale. Cell Biol. Toxicol. 29, 75–84.
46. Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E., and Stamler, J.S. (2005). Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150–166.
47. Hill, B.G., Dranka, B.P., Bailey, S.M., Lancaster, J.R., Jr., and Darley-Usmar, V.M. (2010). What part of NO don’t you understand? Some answers to the cardinal questions in nitric oxide biology. J. Biol. Chem. 285, 19699–19704.
48. Hopper, R.A. and Garthwaite, J. (2006). Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J. Neurosci. 26, 11513–11521.
49. Horan, S., Bourges, I., and Meunier, B. (2006). Transcriptional response to nitrosative stress in Saccharomyces cerevisiae. Yeast 23, 519–535.
50. Hromatka, B.S., Noble, S.M., and Johnson, A.D. (2005). Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol. Biol. Cell 16, 4814–4826.
51. Hutchings, M.I., Mandhana, N., and Spiro, S. (2002). The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species. J. Bacteriol. 184, 4640–4643.
52. Jain, K., Siddam, A., Marathi, A., Roy, U., Falck, J.R., and Balazy, M. (2008). The mechanism of oleic acid nitration by *NO(2). Free Radic. Biol. Med. 45, 269–283.
53. Johansson, A., Moller, C., Fogh, J., and Harper, P. (2003). Biochemical characterization of porphobilinogen deaminase-deficient mice during phenobarbital induction of heme synthesis and the effect of enzyme replacement. Mol. Med. 9, 193–199.
54. Khan, B.V., Harrison, D.G., Olbrych, M.T., Alexander, R.W., and Medford, R.M. (1996). Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. Proc. Natl. Acad. Sci. USA 93, 9114–9119.
55. Kinkel, T.L., Ramos-Montanez, S., Pando, J.M., Tadeo, D.V., Strom, E.N., Libby, S.J., and Fang, F.C. (2016). An essential role for bacterial nitric oxide synthase in Staphylococcus aureus electron transfer and colonization. Nat. Microbiol. 2, 16224.
56. Klatt, P. and Lamas, S. (2000). Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem. 267, 4928–4944.
57. Korkmaz, A., Yaren, H., Topal, T., and Oter, S. (2006). Molecular targets against mustard toxicity: implication of cell surface receptors, peroxynitrite production, and PARP activation. Arch. Toxicol. 80, 662–670.
58. Laver, J.R., Stevanin, T.M., Messenger, S.L., Lunn, A.D., Lee, M.E., Moir, J.W., Poole, R.K., and Read, R.C. (2010). Bacterial nitric oxide detoxification prevents host cell S-nitrosothiol formation: a novel mechanism of bacterial pathogenesis. FASEB. J. 24, 286–295.
59. Lee, J.H., Yang, E.S., and Park, J.W. (2003). Inactivation of NADP + -dependent isocitrate dehydrogenase by peroxynitrite. Implications for cytotoxicity and alcohol-induced liver injury. J. Biol. Chem. 278, 51360–51371.
60. Lemire, J., Mailloux, R., Puiseux‐Dao, S., Appanna, V.D. (2009). Aluminum-induced defective mitochondrial metabolism perturbs cytoskeletal dynamics in human astrocytoma cells. J. Neurosci. Res. 87, 1474–1483.
61. 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.
62. Liu, V.W. and Huang, P.L. (2008). Cardiovascular roles of nitric oxide: a review of insights from nitric oxide synthase gene disrupted mice. Cardiovasc. Res. 77, 19–29.
63. Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J., and Stamler, J.S. (2001). A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490–494.
64. Liu, X.B., Hill, P., and Haile, D.J. (2002). Role of the ferroportin iron-responsive element in iron and nitric oxide dependent gene regulation. Blood Cells Mol. Dis. 29, 315–326.
65. Mahnke, A., Meier, R.J., Schatz, V., Hofmann, J., Castiglione, K., Schleicher, U., Wolfbeis, O.S., Bogdan, C., and Jantsch, J. (2014). Hypoxia in Leishmania major skin lesions impairs the NO-dependent leishmanicidal activity of macrophages. J. Invest. Dermatol. 134, 2339–2346.
66. Mailloux, R.J., Bériault, R., Lemire, J., Singh, R., Chénier, D.R., Hamel, R.D., Appanna, V.D. (2007). The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PLoS One 2, e690.
67. Mailloux, R.J., Puiseux-Dao, S., Appanna, V.D. (2009). α-ketoglutarate abrogates the nuclear localization of HIF-1α in aluminum-exposed hepatocytes. Biochimie 91, 408–415.
68. Martinez, M.C., and Andriantsitohaina, R. (2009). Reactive nitrogen species: molecular mechanisms and potential significance in health and disease. Antioxid. Redox Signal 11, 669–702.
69. McBride, A.G., Borutaite, V., and Brown, G.C. (1999). Superoxide dismutase and hydrogen peroxide cause rapid nitric oxide breakdown, peroxynitrite production and subsequent cell death. Biochim. Biophys. Acta. 1454, 275–288.
70. Middaugh, J., Hamel, R., Jean-Baptiste, G., Beriault, R., Chenier, D., and Appanna, V.D. (2005). Aluminum triggers decreased aconitase activity via Fe-S cluster disruption and the overexpression of isocitrate dehydrogenase and isocitrate lyase: a metabolic network mediating cellular survival. J. Biol. Chem. 280, 3159–3165.
71. Missall, T.A., Lodge, J.K., and McEwen, J.E. (2004). Mechanisms of resistance to oxidative and nitrosative stress: implications for fungal survival in mammalian hosts. Eukaryot. Cell 3, 835–846.
72. Mukhopadhyay, P., Zheng, M., Bedzyk, L.A., LaRossa, R.A., and Storz, G. (2004). Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc. Natl. Acad. Sci. USA 101, 745–750.
73. Muller, B., Kleschyov, A.L., Alencar, J.L., Vanin, A., and Stoclet, J.C. (2002). Nitric oxide transport and storage in the cardiovascular system. Ann. N Y Acad. Sci. 962, 131–139.
74. Murad, F. (2006). Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development. N. Engl. J. Med. 355, 2003–2011.
75. 2 in vitro and in vivo and reduce menadione-induced DNA injury and cytotoxicity. Am. J. Physiol. 268, C227–236.
76. Nathan, C. (2003). Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J. Clin. Invest. 111, 769–778.
77. Nittler, M.P., Hocking-Murray, D., Foo, C.K., and Sil, A. (2005). Identification of Histoplasma capsulatum transcripts induced in response to reactive nitrogen species. Mol. Biol. Cell 16, 4792–4813.
78. Ohshima, H., Sawa, T., and Akaike, T. (2006). 8-nitroguanine, a product of nitrative DNA damage caused by reactive nitrogen species: formation, occurrence, and implications in inflammation and carcinogenesis. Antioxid. Redox Signal 8, 1033–1045.
79. Parente, A.F., Naves, P.E., Pigosso, L.L., Casaletti, L., McEwen, J.G., Parente-Rocha, J.A., and Soares, C.M. (2015). The response of Paracoccidioides spp. to nitrosative stress. Microbes. Infect. 17, 575–585.
80. Parker, H., Albrett, A.M., Kettle, A.J., and Winterbourn, C.C. (2012). Myeloperoxidase associated with neutrophil extracellular traps is active and mediates bacterial killing in the presence of hydrogen peroxide. J. Leukoc. Biol. 91, 369–376.
81. Peluffo, G., and Radi, R. (2007). Biochemistry of protein tyrosine nitration in cardiovascular pathology. Cardiovasc. Res. 75, 291–302.
82. Pham-Huy, L.A., He, H., and Pham-Huy, C. (2008). Free radicals, antioxidants in disease and health. Int. J. Biomed. Sci. 4, 89–96.
83. Phaniendra, A., Jestadi, D.B., and Periyasamy, L. (2015). Free radicals: properties, sources, targets, and their implication in various diseases. Indian J. Clin. Biochem. 30, 11–26.
84. Poole, R.K. (2005). Nitric oxide and nitrosative stress tolerance in bacteria. Biochem. Soc. Trans. 33, 176–180.
85. Poole, R.K., and Hughes, M.N. (2000). New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36, 775–783.
86. Qu, W., Zhou, Y., Shao, C., Sun, Y., Zhang, Q., Chen, C., and Jia, J. (2009). Helicobacter pylori proteins response to nitric oxide stress. J. Microbiol. 47, 486–493.
87. Radi, R. (2013). Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc. Chem. Res. 46, 550–559.
88. Richardson, A.R., Dunman, P.M., and Fang, F.C. (2006). The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Mol. Microbiol. 61, 927–939.
89. Richardson, A.R., Libby, S.J., and Fang, F.C. (2008). A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science 319, 1672–1676.
90. Rogstam, A., Larsson, J.T., Kjelgaard, P., and von Wachenfeldt, C. (2007). Mechanisms of adaptation to nitrosative stress in Bacillus subtilis. J. Bacteriol. 189, 3063–3071.
91. Sandoo, A., van Zanten, J.J., Metsios, G.S., Carroll, D., and Kitas, G.D. (2010). The endothelium and its role in regulating vascular tone. Open Cardiovasc. Med. J. 4, 302–312.
92. Santos, R.M., Lourenco, C.F., Ledo, A., Barbosa, R.M., and Laranjinha, J. (2012). Nitric oxide inactivation mechanisms in the brain: role in bioenergetics and neurodegeneration. Int. J. Cell Biol. 2012, 391914.
93. Sawa, T., Zaki, M.H., Okamoto, T., Akuta, T., Tokutomi, Y., Kim-Mitsuyama, S., Ihara, H., Kobayashi, A., Yamamoto, M., Fujii, S., et al. (2007). Protein S-guanylation by the biological signal 8-nitroguanosine 3′,5′-cyclic monophosphate. Nat. Chem. Biol. 3, 727–735.
94. Schleicher, U., Paduch, K., Debus, A., Obermeyer, S., Konig, T., Kling, J.C., Ribechini, E., Dudziak, D., Mougiakakos, D., Murray, P.J., et al. (2016). TNF-mediated restriction of arginase 1 expression in myeloid cells triggers type 2 NO synthase activity at the site of infection. Cell Rep. 15, 1062–1075.
95. Stern, A.M., Liu, B., Bakken, L.R., Shapleigh, J.P., and Zhu, J. (2013). A novel protein protects bacterial iron-dependent metabolism from nitric oxide. J. Bacteriol. 195, 4702–4708.
96. Storm, J., Sethia, S., Blackburn, G.J., Chokkathukalam, A., Watson, D.G., Breitling, R., Coombs, G.H., and Muller, S. (2014). Phosphoenolpyruvate carboxylase identified as a key enzyme in erythrocytic Plasmodium falciparum carbon metabolism. PLoS Pathog. 10, e1003876.
97. Szabo, C., Ischiropoulos, H., and Radi, R. (2007). Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6, 662–680.
98. Thomson, L. (2015). 3-nitrotyrosine modified proteins in atherosclerosis. Dis. Markers 2015, 708282.
99. Thomas, C., Mackey, M.M., Diaz, A.A., and Cox, D.P. (2009). Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation. Redox Rep. 14, 102–108.
100. Tillmann, A., Gow, N.A., and Brown, A.J. (2011). Nitric oxide and nitrosative stress tolerance in yeast. Biochem. Soc. Trans. 39, 219–223.
101. Ullmann, B.D., Myers, H., Chiranand, W., Lazzell, A.L., Zhao, Q., Vega, L.A., Lopez-Ribot, J.L., Gardner, P.R., and Gustin, M.C. (2004). Inducible defense mechanism against nitric oxide in Candida albicans. Eukaryot. Cell 3, 715–723.
102. Uppu, R.M. and Pryor, W.A. (1996). Carbon dioxide catalysis of the reaction of peroxynitrite with ethyl acetoacetate: an example of aliphatic nitration by peroxynitrite. Biochem. Biophys Res. Commun. 229, 764–769.
103. Villacorta, L., Zhang, J., Garcia-Barrio, M.T., Chen, X.L., Freeman, B.A., Chen, Y.E., and Cui, T. (2007). Nitro-linoleic acid inhibits vascular smooth muscle cell proliferation via the Keap1/Nrf2 signaling pathway. Am. J. Physiol. Heart Circ. Physiol. 293, H770–776.
104. Virag, L. and Szabo, C. (2002). The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 54, 375–429.
105. Wanstall, J.C., Homer, K.L., and Doggrell, S.A. (2005). Evidence for, and importance of, cGMP-independent mechanisms with NO and NO donors on blood vessels and platelets. Curr. Vasc. Pharmacol. 3, 41–53.
106. Weidinger, A. and Kozlov, A.V. (2015). Biological activities of reactive oxygen and nitrogen species: oxidative stress versus signal transduction. Biomolecules 5, 472–484.
107. White, P.J., Charbonneau, A., Cooney, G.J., and Marette, A. (2010). Nitrosative modifications of protein and lipid signaling molecules by reactive nitrogen species. Am. J. Physiol. Endocrinol. Metab. 299, E868–878.
108. Wright, M.M., Kim, J., Hock, T.D., Leitinger, N., Freeman, B.A., and Agarwal, A. (2009). Human haem oxygenase-1 induction by nitro-linoleic acid is mediated by cAMP, AP-1 and E-box response element interactions. Biochem. J. 422, 353–361.
109. Yermilov, V., Rubio, J., and Ohshima, H. (1995). Formation of 8-nitroguanine in DNA treated with peroxynitrite in vitro and its rapid removal from DNA by depurination. FEBS Lett. 376, 207–210.
110. Zhao, J. (2007). Interplay among nitric oxide and reactive oxygen species: a complex network determining cell survival or death. Plant Signal. Behav. 2, 544–547.
111. Zhou, S., Narukami, T., Nameki, M., Ozawa, T., Kamimura, Y., Hoshino, T., and Takaya, N. (2012). Heme-biosynthetic porphobilinogen deaminase protects Aspergillus nidulans from nitrosative stress. Appl. Environ. Microbiol. 78, 103–109.
112. Zmijewski, J.W., Landar, A., Watanabe, N., Dickinson, D.A., Noguchi, N., and Darley-Usmar, V.M. (2005). Cell signalling by oxidized lipids and the role of reactive oxygen species in the endothelium. Biochem. Soc. Trans. 33, 1385–1389.