Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells

Plant and Cell Physiology

Volumn 47, Issue 6, 2006, Pages 689-697

  Saito, Syuhei ^a   Yamamoto Katou, Ayako ^a,b   Yoshioka, Hirofumi ^a   Doke, Noriyuki ^a   Kawakita, Kazuhito ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Defense responses; INF1 elicitin; Nitrotyrosine; Peroxynitrite; Tobacco BY 2 cells; Urate

Indexed keywords

3 MORPHOLINO SYDNONIMINE; 3 NITROTYROSINE; 3-MORPHOLINO-SYDNONIMINE; 3-NITROTYROSINE; ALGAL PROTEIN; AMINOPHENYL FLUORESCEIN; ANILINE DERIVATIVE; ANTIIDIOTYPIC ANTIBODY; CYCLIC GMP; DRUG DERIVATIVE; FLUORESCEIN DERIVATIVE; FUNGAL PROTEIN; INF1 PROTEIN, PHYTOPHTHORA INFESTANS; MOLSIDOMINE; NITRIC OXIDE; PEROXYNITROUS ACID; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TYROSINE; URIC ACID;

ARTICLE; CELL CULTURE; CHEMISTRY; DRUG EFFECT; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PHYTOPHTHORA; TOBACCO;

ALGAL PROTEINS; ANILINE COMPOUNDS; ANTIBODIES, ANTI-IDIOTYPIC; CELLS, CULTURED; CYCLIC GMP; FLUORESCEINS; FUNGAL PROTEINS; MOLSIDOMINE; NITRIC OXIDE; PEROXYNITROUS ACID; PHYTOPHTHORA; REACTIVE OXYGEN SPECIES; SUPEROXIDES; TOBACCO; TYROSINE; URIC ACID;

NICOTIANA TABACUM; PHYTOPHTHORA INFESTANS;

EID: 33745367692     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcj038     Document Type: Article

References (65)

1. Alamillo, J.M. and García-Olmedo, F. (2001) Effects of urate, a natural scavenger of peroxynitrite-mediated toxicity, in the response of Arabidopsis thaliana to the bacterial pathogen Pseudomonas syringae. Plant J. 25: 529-540.
2. Apostol, I., Heinstein, P.F. and Low, P.S. (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiol. 90: 106-116.
3. Balavoine, G.G.A. and Geletii, Y.V. (1999) Peroxynitrite scavenging by different antioxidants. Part I: convenient assay. Nitric Oxide: Biol. Chem. 3: 40-54.
4. Beckman, J.S., Beckman, T.W., Chen, J., Marshall, P.A. and Freeman, B.A. (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl Acad. Sci. USA 87: 1620-1624.
5. Bethke, P.C., Badger, M.R. and Jones, R.L. (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16: 332-341.
6. Bradford, M.M. (1976) A rapid and sensitive method for the quantiation of microgram quantities of protein utilizing the principle of protein - dye binding. Anal. Biochem. 72: 248-254.
7. Bradley, D.J., Kjellbom, P. and Lamb, C.J. (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21-30.
8. Cobbs, C.S., Samanta, M., Harkins, L.E., Gillespie, G.Y., Merrick, B.A. and MacMillan-Crow, L.A. (2001) Evidence for peroxynitrite-mediated modifications to p53 in human gliomas: possible functional consequences. Arch. Biochem. Biophys. 15: 167-172.
9. Cooney, R.V., Harwood, P.J., Custer, L.J. and Franke, A.A. (1994) Light-mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environ. Health Perspect. 102: 460-462.
10. Daiber, A., Bachschmid, M., Beckman, J.S., Munzel, T. and Ullrich, V. (2004) The impact of metal catalysis on protein tyrosine nitration by peroxynitrite. Biochem. Biophys. Res. Commun. 317: 873-881.
11. Delledonne, M., Zeier, J., Marocco, A. and Lamb, C. (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585-588.
12. Delledonne, M., Zeier, J., Marocco, A. and Lamb, C. (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl Acad. Sci. USA 98: 13454-13459.
13. Desikan, R., A.-H.-Mackerness, S., Hancock, J.T. and Neill, S.J. (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127: 159-172.
14. Desikan, R., Griffiths, R., Hancock, J. and Neill, S. (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 99: 16314-16318.
15. Doke, N. (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 23: 345-357.
16. Dumer, J., Wendehenne, D. and Klessig, D.F. (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl Acad. Sci. USA 95: 10328-10333.
17. Foissner, I., Wendehenne, D., Langebartels, C. and Durner, J. (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J. 23: 817-824.
18. Giasson, B.I., Duda, J.E., Murray, I.V.J., Chen, Q., Souza, J.M., Hurtig, H.I., Ischiropoulos, H., Trojanowski, J.Q. and Lee, V.M.-Y. (2000) Oxidative damage linked to neurodegeneration by selective α-synuclein nitration in synucleinopathy lesions. Science 290: 985-989.
19. Guo, F.-Q. and Crawford, N.M. (2005) Arabidopsis nitric oxide synthase 1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17: 3436-3450.
20. Guo, F.-Q., Okamoto, M. and Crawford, N.M. (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302: 100-103.
21. Hanazawa, T., Kharitonov, S.A. and Barnes, P.J. (2000) Increased nitrotyrosine in exhaled breath condensate of patients with asthma. Amer. J. Respir. Crit. Care Med. 162: 1273-1276.
22. Hensley, K., Maidt, M.L., Yu, Z., Sang, H., Markesbery, W.R. and Floyd, R.A. (1998) Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J. Neurosci. 18: 8126-8132.
23. Imada, I., Sato, E.F., Miyamoto, M., Ichimori, Y., Minamiyama, Y., Konaka, R. and Inoue, M. (1999) Analysis of reactive oxygen species generated by neutrophils using a chemiluminescence probe L-012. Anal. Biochem. 271: 53-58.
24. Kaiser, W.M., Weiner, H., Kandlbinder, A., Tsai, C.-B., Rockel, P., Sonoda, M. and Planchet, E. (2002) Modulation of nitrate reductase: some new insights, an unusual case and a potentially important side reaction. J. Exp. Bot. 53: 875-882.
25. Kamoun, S., van West, P., de Jong, A.J., de Groot, K.E., Vleeshouwers, V.G.A.A. and Govers, F. (1997) A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol. Plant-Microbe Interact. 10: 13-20.
26. Kozak, A.J., Liu, F., Funovics, P., Jacoby, A., Kubant, R. and Malinski T. (2005) Role of peroxynitrite in the process of vascular tone regulation by nitric oxide and prostanoids - a nanotechnological approach. Prostaglandins Leukot. Essent. Fatty Acids 72: 105-113.
27. Leon, J., Lawton, M.A. and Raskin, I. (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108: 1673-1678.
28. -, in solid argon. J. Amer. Chem. Soc. 123: 9848-9854.
29. Lindermayr, C., Saalbach, G. and Durner, J. (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 137: 921-930.
30. MacMillan-Crow, L.A., Crow, J.P., Kerby, J.D., Beckman, J.S. and Thompson, J.A. (1996) Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl Acad. Sci. USA 93: 11853-11858.
31. Martin-Romero, F.J., Gutíerrez-Martin, Y., Henao, F. and Gutíerrez-Merino, C. (2004) Fluorescence measurements of steady state peroxynitrite production upon SIN-1 decomposition: NADH versus dihydrodichlorofluorescein and dihydrorhodamine 123: J. Fluoresc. 14: 17-23.
32. Morse, M., Pironcheva, G. and Gehring, C. (2004) AtPNP-A is a systemically mobile natriuretic peptide immunoanalogue with a role in Arabidopsis thaliana cell volume regulation. FEBS Lett. 556: 99-103.
33. Moulian, N., Truffault, F., Gaudry-Talarmain, Y.M., Serraf A. and Berrin-Aknin, S. (2001) In vivo and in vitro apoptosis of human thymocytes are associated with nitrotyrosine formation. Immunobiology 97: 3521-3530.
34. Noritake, T., Kawakita, K. and Doke, N. (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol. 37: 113-116.
35. Padmaja, S. and Huie, R.E. (1993) The reaction of nitric oxide with organic peroxylo radicals. Biochem. Biophys. Res. Commun. 195: 539-544.
36. Peng, M. and Kuc, J. (1992) Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf discs. Phytopathology 82: 696-699.
37. Perazzolli, M., Dominici, P., Romero-Puertas, M.C., Zago, E., Zeier, J., Sonoda, M., Lamb, C. and Delledonne, M. (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16: 2785-2794.
38. + fluxes in Zea mays roots. Mol. Cell. Biol. 2: 53-57.
39. Planchet, E., Gupta, K.J., Sonoda, M. and Kaiser, W.M. (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J. 41: 732-743.
40. Planchet, E., Sonoda, M., Zeier, J. and Kaiser, W.M. (2006) Nitric oxide (NO) as an intermediate in the cryptogein-induced hypersensitive response - a critical re-evaluation. Plant Cell Environ. 29: 59-69.
41. Pryor, W.A., Jin, X. and Squadrito, G.L. (1996) Insensitivity of the rate of decomposition of peroxynitrite in viscosity; evidence against free radical formation. J. Amer. Chem. Soc. 118: 3125-3128.
42. Reiter, C.D., Teng, R.-J. and Beckman, J.S. (2000) Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J. Biol. Chem. 275: 32460-32466.
43. Rubbo, H., Denicola, A. and Radi, R. (1994a) Peroxynitrite inactivates thiol-containing enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration. Arch. Biochem. Biophys. 308: 96-102.
44. Rubbo, H., Radi, R., Trujillo, M., Telleri, R., Kalyanaraman, B., Barnes, S., Kirk, M. and Freeman, B.A. (1994b) Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. J. Biol. Chem. 269: 26066-26075.
45. Salgo, M.G., Bermúdez, E., Squadrito, G.L. and Pryor, W.A. (1995) DNA damage and oxidation of thiols peroxynitrite causes in rat thymocytes. Arch. Biochem. Biophys. 322: 500-505.
46. Sandoval, M., Zhang, X.-J., Liu, X., Mannick, E.E., Clark, D.A. and Miller, M.J.S. (1997) Peroxynitrite-induced apoptosis in T84 and raw 264.7 cells: attenuation by L-ascorbic acid. Free Radic. Biol. Med. 22: 489-495.
47. Sasabe, M., Takeuchi, K., Kamoun, S., Ichinose, Y., Govers, F., Toyoda, K., Shiraishi, T. and Yamada, T. (2000) Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. Eur. J. Biochem. 267: 5005-5013.
48. Schlossmann, J., Feil, R. and Hofmann, F. (2003) Signaling through NO and cGMP-dependent protein kinases. Trends Mol. Med. 35: 21-27.
49. Setsukinai, K.-I., Urano, Y., Kakinuma, K., Majima, H.J. and Nagano, T. (2003) Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278: 3170-3175.
50. Shimoda, Y., Nagata, M., Suzuki, A., Abe, M., Sato, S., Kato, T., Tabata, S., Higashi, S. and Uchiumi, T. (2005) Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol. 46: 99-107.
51. Stamler, J.S. (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78: 931-936.
52. Stöhr, C., Strube, F., Marx, G., Ullrich, W.R. and Peter, R. (2001) A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212: 835-841.
53. Symons, M.C.R. (2000) cis- and trans-conformations for peroxynitrite anions. J. Inorg. Biochem. 78: 299-301.
54. Tada, Y., Mori, T., Shinogi, T., Yao, N., Takahashi, S., et al. (2004) Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defense response of Oat. Mol. Plant-Microbe Interact. 17: 245-253.
55. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA 99: 517-522.
56. Wang, J.W. and Wu, J.Y. (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol. 46: 923-930.
57. Yamamoto, A., Katou, S., Yoshioka, H., Doke, N. and Kawakita, K. (2003) Nitrate reductase, a nitric oxide-producing enzyme: induction by pathogen signals. J. Gen. Plant Pathol. 69: 218-229.
58. Yamamoto, A., Katou, S., Yoshioka, H., Doke, N. and Kawakita, K. (2004) Involvement of nitric oxide generation in hypersensitive cell death induced by elicitin in tobacco cell suspension culture. J. Gen. Plant Pathol. 70: 85-92.
59. Yamasaki, H. (2005) The NO world for plants: achieving balance in an open system. Plant Cell Environ. 28: 78-84.
60. Yamasaki, H. and Sakihama, Y. (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett. 468: 89-92.
61. 2 accumulation and resistance to Phytophthora infestans. Plant Cell 15: 706-718.
62. Zeidler, D., Zähringer, U., Gerber, I., Dubery, I., Hartung, T., Bors, W., Hutzler, P. and Durner, J. (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc. Natl Acad. Sci. USA 1001: 15811-15816.
63. Zhang, P., Wang, Y.-Z., Kagan, E. and Bonner, J.C. (2000) Peroxynitrite targets the epidermal growth factor receptor, Raf-1, and MEK independently to activate MAPK. J. Biol. Chem. 275: 22479-22486.
64. Zhang, X., Kim, W.-S., Hatcher, N., Potgieter, K., Moroz, L.L., Gillette, R. and Sweedler, J.V. (2002) Interfering with nitric oxide measurements. J. Biol. Chem. 277: 48472-48478.
65. Zhu, S., Basiouny, K.F., Crow, J.P. and Matalon, S. (2000) Carbon dioxide enhances nitration of surfactant protein A by activated alveolar macrophages. Amer. J. Physiol. Lung Cell Mol. Physiol. 278: 1025-1031.