The anoxic plant mitochondrion as a nitrite: NO reductase

Mitochondrion

Volumn 11, Issue 4, 2011, Pages 537-543

  Gupta, Kapuganti J ^a   Igamberdiev, Abir U ^b  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Anoxia; Hemoglobin; Nitric oxide; Nitrite reduction; Plant mitochondria

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; HEMOGLOBIN; NITRIC OXIDE REDUCTASE; NITRITE;

CELL ACTIVITY; CELL FUNCTION; CELL HYPOXIA; ENZYME SYNTHESIS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PLANT CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REACTION TIME; REDOX STRESS; REVIEW; SIGNAL TRANSDUCTION; TISSUE OXYGENATION; TURNOVER TIME;

ADENOSINE TRIPHOSPHATE; CELL DEATH; CELL HYPOXIA; CYTOSOL; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; HEMOGLOBINS; MITOCHONDRIA; NAD; NADP; NITRIC OXIDE; NITRITES; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; PLANTS;

EID: 79957962052     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2011.03.005     Document Type: Review

References (71)

1. Bailey-Serres J., Voesenek L.A. Flooding stress: acclimations and genetic diversity. Ann. Rev. Plant Biol. 2008, 59:313-339.
2. Basu S., Azarova N.A., Font M.D., King S.B., Hogg N., Gladwin M.T., Shiva S., Kim-Shapiro D.B. Nitrite reductase activity of cytochrome c. J. Biol. Chem. 2008, 283:32590-32597.
3. Benamar A., Rolletschek H., Borisjuk L., Avelange-Macherel M.H., Curien G., Mostefai H.A., Andriantsitohaina R., Macherel D. Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim. Biophys. Acta 2008, 1777:1268-1275.
4. Borisjuk L., Macherel D., Benamar A., Wobus U., Rolletschek H. Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol. 2007, 176:813-823.
5. Botrel A., Magne C., Kaiser W.M. Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant Physiol. Biochem. 1996, 34:645-652.
6. Brown G.C., Borutaite V. Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic. Biol. Med. 2002, 33:1440-1450.
7. Brown G.C., Cooper C.E. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal cytochrome oxidase respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 1994, 356:295-298.
8. Brunelle J.K., Bell E.L., Quesada N.M., Vercauteren K., Tiranti V., Zeviani M., Scarpulla R.C., Chandel N.S. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab. 2005, 1:409-414.
9. Brunori M., Forte E., Arese M., Mastronicola D., Giuffrè A., Sarti P. Nitric oxide and the respiratory enzyme. Biochim. Biophys. Acta 2006, 1757:1144-1154.
10. Cassanova N., O'Brien K.M., Stahl B.T., McClure T., Poyton R.O. Yeast flavohemoglobin, a nitric oxide oxidoreductase, is located in both the cytosol and the mitochondrial matrix: effects of respiration, anoxia, and the mitochondrial genome on its intracellular level and distribution. J. Biol. Chem. 2005, 280:7645-7653.
11. Castello P.R., David P.S., McClure T., Crook Z., Poyton R.O. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab. 2006, 3:277-287.
12. Castello P.R., Woo D.K., Ball K., Wojcik J., Liu L., Poyton R.O. 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. 2008, 105:8203-8208.
13. Cooper C.E. Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector?. Trends Biochem. Sci. 2002, 27:33-39.
14. Cooper C.E., Torres J., Sharpe M.A., Wilson M.T. Nitric oxide ejects electrons from the binuclear centre of cytochrome c oxidase by reacting with oxidised copper: a general mechanism for the interaction of copper proteins with nitric oxide?. FEBS Lett. 1997, 414:281-284.
15. Coueé I., Defontaine S., Carde J.P., Pradet A. Effects of anoxia on mitochondrial biogenesis in rice shoots - modification of in organello translation characteristics. Plant Physiol. 1992, 98:411-421.
16. Dordas C., Hasinoff B.B., Igamberdiev A.U., Manac'h N., Rivoal J., Hill R.D. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J. 2003, 35:763-770.
17. Fago A., Mathews A.J., Brittain T. A role for neuroglobin: resetting the trigger level for apoptosis in neuronal and retinal cells. IUBMB Life 2008, 60:398-401.
18. Feelisch M., Fernandez B.O., Bryan N.S., Garcia-Saura M.F., Bauer S., Whitlock D.R., Ford P.C., Janero D.R., Rodriguez J., Ashrafian H. Tissue processing of nitrite in hypoxia: an intricate interplay of nitric oxide-generating and scavenging systems. J. Biol. Chem. 2008, 283:33927-33934.
19. Gardner P.R. Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J. Inorg. Biochem. 2005, 99:247-266.
20. Gardner A.M., Cook M.R., Gardner P.R. Nitric oxide dioxygenase function of human cytoglobin with cellular reductants and in rat hepatocytes. J. Biol. Chem. 2010, 285:23850-23857.
21. Gladwin M.T., Shiva S. The ligand binding battle at cytochrome c oxidase: how NO regulates oxygen gradients in tissue. Circ. Res. 2009, 104:1136-1138.
22. Goshima N., Mukai T., Suemori M., Takahashi M., Caboche M., Morikawa H. Emission of nitrous oxide (N2O) from transgenic tobacco expressing antisense NiR mRNA. Plant J. 1999, 19:75-80.
23. Gupta K.J. Protein S-nitrosylation in plants: photorespiratory metabolism and NO signaling. Sci. Signal. 2011, 4:jc1.
24. Gupta K.J., Kaiser W.M. Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol. 2010, 51:576-584.
25. Gupta K.J., Stoimenova M., Kaiser W.M. In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J. Exp. Bot. 2005, 56:2601-2609.
26. Gupta K.J., Igamberdiev A.U., Kaiser W.M. New insights into the mitochondrial nitric oxide production pathways. Plant Signal. Behav. 2010, 29:999-1001.
27. Hagen T., Taylor C.T., Lam F., Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 2003, 302:1975-1978.
28. Hebelstrup K.H., Østergaard-Jensen E., Hill R.D. Bioimaging techniques for subcellular localization of plant hemoglobins and measurement of hemoglobin-dependent nitric oxide scavenging in planta. Meth. Enzymol. 2008, 437:595-604.
29. Horchani F., Prevot M., Boscari A., Evangelisti E., Meilhoc E., Bruand C., Raymond P., Boncompagni E., Aschi-Smiti S., Puppo A., Brouquisse R. Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol. 2011, 155:1023-1036.
30. Huang X., von Rad U., Durner J. Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 2002, 215:914-923.
31. Igamberdiev A.U., Hill R.D. Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J. Exp. Bot. 2004, 55:2473-2482.
32. Igamberdiev A.U., Hill R.D. Plant mitochondrial function during anaerobiosis. Ann. Bot. 2009, 103:259-268.
33. Igamberdiev A.U., Bykova N.V., Lea P.J., Gardeström P. The role of photorespiration in redox and energy balance of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxylase. Physiol. Plant. 2001, 111:427-438.
34. Igamberdiev A.U., Bykova N.V., Hill R.D. Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. Planta 2006, 223:1033-1040.
35. Igamberdiev A.U., Bykova N.V., Shah J.K., Hill R.D. Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol. Plant. 2010, 138:393-404.
36. Jancura D., Antalik M., Berka V., Palmer G., Fabian M. Filling the catalytic site of cytochrome c oxidase with electrons. Reduced CuB facilitates internal electron transfer to heme a3. J. Biol. Chem. 2006, 281:20003-20010.
37. Kozlov A.V., Staniek K., Nohl H. Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett. 1999, 454:127-130.
38. Kurtz D.M. Flavo-diiron enzymes: nitric oxide or dioxygen reductases?. Dalton Trans. 2007, 37:4115-4121.
39. Laus M.N., Soccio M., Trono D., Cattivelli L., Pastore D. Plant inner membrane anion channel (PIMAC) function in plant mitochondria. Plant Cell Physiol. 2008, 49:1039-1055.
40. Libourel I.G.L., van Bodegom P.M., Fricker M.D., Ratcliffe R.G. Nitrite reduces cytoplasmic acidosis under anoxia. Plant Physiol. 2006, 142:1710-1717.
41. Liu L., Zeng M., Hausladen A., Heitman J., Stamler J.S. Protection from nitrosative stress by yeast flavohemoglobin. Proc. Natl Acad. Sci. U. S. A. 2000, 97:4672-4676.
42. Mason M.G., Nicholls P., Wilson M.T., Cooper C.E. Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proc. Natl Acad. Sci. U. S. A. 2006, 103:708-713.
43. Millar A.H., Trend A.E., Heazlewood J.L. Changes in the mitochondrial proteome during the anoxia to air transition in rice focus around cytochrome-containing respiratory complexes. J. Biol. Chem. 2004, 279:39471-39478.
44. Millar A.H., Eubel H., Jänsch L., Kruft V., Heazlewood J.L., Braun H.P. Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol. Biol. 2004, 56:77-90.
45. Modolo L.V., Augusto O., Almeida I.M., Magalhaes J.R., Salgado I. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett. 2005, 579:3814-3820.
46. Møller I.M. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52:561-591.
47. Moreau M., Lee G.I., Wang Y., Crane B.R., Klessig D.F. AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase. J. Biol. Chem. 2008, 283:32957-32967.
48. Müller E., Albers B., Janiesch P. Influence of NO3 and NH4 nutrition on fermentation, nitrate reductase activity and adenylate energy charge of roots of Carex pseudocyperus L. and Carex sylvatica Huds. exposed to anaerobic nutrient solutions. Plant Soil 1994, 166:221-230.
49. Mur L.A., Carver T.L., Prats E. NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J. Exp. Bot. 2006, 57:489-505.
50. Palmieri M.C., Lindermayr C., Bauwe H., Steinhauser C., Durner J. Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol. 2010, 152:1514-1528.
51. Pearce L.L., Kanai A.J., Birder L.A., Pitt B.R., Peterson J. The catabolic fate of nitric oxide: the nitric oxide oxidase and peroxynitrite reductase activities of cytochrome oxidase. J. Biol. Chem. 2002, 277:13556-13562.
52. Planchet E., Gupta K.J., Sonoda M., Kaiser W.M. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J. 2005, 41:732-743.
53. Poyton R.O., Ball K.A., Castello P.R. Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol. Metab. 2009, 20:332-340.
54. Rasmusson A.G., Geisler D.A., Møller I.M. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 2008, 8:47-60.
55. Roberts J.K.M., Andrade F.H., Anderson I.C. Further evidence that cytoplasmic acidosis is a determinant of flooding intolerance in plants. Plant Physiol. 1985, 77:492-494.
56. Rolletschek H., Borisjuk L., Koschorreck M., Wobus U., Weber H. Legume embryos develop in a hypoxic environment. J. Exp. Bot. 2002, 53:1099-1107.
57. Shiva S. Mitochondria as metabolizers and targets of nitrite. Nitric Oxide 2010, 22:64-74.
58. Smagghe B.J., Trent J.T., Hargrove M.S. NO dioxygenase activity in hemoglobins is ubiquitous in vitro, but limited by reduction in vivo. PLoS ONE 2008, 3:e2039.
59. Stoimenova M., Igamberdiev A.U., Gupta K.J., Hill R.D. Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 2007, 226:465-474.
60. Sugiura M., Georgescu M.N., Takahashi M. A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant Cell Physiol. 2007, 48:1022-1035.
61. Tielens A.G.M., Rotte C., van Hellemond J.J., Martin W. Mitochondria as we don't know them. Trends Biochem. Sci. 2002, 27:564-572.
62. Tischner R., Planchet E., Kaiser W.M. Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett. 2004, 576:151-155.
63. Trimmer B.A., Aprille J.R., Dudzinski D.M., Lagace C.J., Lewis S.M., Michel T., Qazi S., Zayas R.M. Nitric oxide and the control of firefly flashing. Science 2001, 292:2486-2488.
64. Tschiersch H., Borisjuk L., Rutten T., Rolletschek H. Gradients of seed photosynthesis and its role for oxygen balancing. BioSystems 2011, 103:302-308.
65. Unitt D.C., Hollis V.S., Palacios-Callender M., Frakich N., Moncada S. Inactivation of nitric oxide by cytochrome c oxidase under steady-state oxygen conditions. Biochim. Biophys. Acta Bioenerg. 2010, 1797:371-377.
66. Vartapetian B.B., Polyakova L.I. Protective effect of exogenous nitrate on the mitochondrial ultrastructure of Oryza sativa coleoptiles under strict anoxia. Protoplasma 1999, 206:163-167.
67. Vartapetian B.B., Andreeva I.N., Generozova I.P., Polyakova L.I., Maslova I.P., Dolgikh Y.I., Stepanova A.Y. Functional electron microscopy in studies of plant response and adaptation to anaerobic stress. Ann. Bot. 2003, 91:155-172.
68. Vartapetian B.B., Andreeva I.N., Generozova I.P., Polyakova L.I., Maslova I.P., Dolgikh Y.I., Stepanova A.Y. Functional electron microscopy in studies of plant response and adaptation to anaerobic stress. Ann. Bot. 2003, 91:155-172.
69. Walters C.L., Taylor A.M. The reduction of nitrite by skeletal muscle mitochondria. Biochim. Biophys. Acta 1965, 96:522-524.
70. Wang R., Xing X., Crawford N. Nitrite acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiol. 2007, 145:1735-1745.
71. Zhao X.-J., Sampath V., Caughey W.S. Cytochrome c oxidase catalysis of the reduction of nitric oxide to nitrous oxide. Biochem. Biophys. Res. Commun. 1995, 212:1054-1060.