Leghemoglobin green derivatives with nitrated hemes evidence production of highly reactive nitrogen species during aging of legume nodules

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 7, 2012, Pages 2660-2665

  Navascués, Joaquín ^a   Pérez Rontomé, Carmen ^a   Gay, Marina ^b   Marcos, Manuel ^c   Yang, Fei ^d,f   Walker, F Ann ^d   Desbois, Alain ^e   Abián, Joaquín ^b   Becana, Manuel ^a  

^a CSIC   (Spain)

^b INST D INVESTIGACIONS B   (Spain)

^c UNIVERSITY OF VIGO   (Spain)

^d University of Arizona   (United States)

^e SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^f MIAMI UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; APOPROTEIN; CHELATING AGENT; HEME; IRON; LEGHEMOGLOBIN; LIGAND; NITRITE; NITROUS ACID; REACTIVE NITROGEN SPECIES;

AGING PLANT; ARTICLE; IN VIVO STUDY; ISOMER; MASS SPECTROMETER; MOLECULAR WEIGHT; NITRATION; NITROSATIVE STRESS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXYGEN AFFINITY; PRIORITY JOURNAL; RAMAN SPECTROMETRY; SENESCENCE; SOYBEAN; ULTRAVIOLET SPECTROSCOPY;

FABACEAE; HEME; LEGHEMOGLOBIN; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; REACTIVE NITROGEN SPECIES; SPECTROPHOTOMETRY, ULTRAVIOLET;

GLYCINE MAX;

EID: 84857126329     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1116559109     Document Type: Article

References (56)

1. Vinogradov SN, et al. (2005) Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proc Natl Acad Sci USA 102:11385-11389. (Pubitemid 41153829)
2. Gardner PR (2005) Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J Inorg Biochem 99:247-266.
3. Pesce A, et al. (2002) Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family. EMBO Rep 3:1146-1151. (Pubitemid 36105002)
4. Appleby CA, Bergersen FJ (1980) Methods for Evaluating Biological Nitrogen Fixation, ed Bergersen FJ (John Wiley, Chichester), pp 315-335.
5. Igamberdiev AU, Hill RD (2004) Nitrate, NO and haemoglobin in plant adaptation to hypoxia: An alternative to classic fermentation pathways. J Exp Bot 55:2473-2482. (Pubitemid 40025062)
6. Perazzolli M, Romero-Puertas MC, Delledonne M (2006) Modulation of nitric oxide bioactivity by plant haemoglobins. J Exp Bot 57:479-488. (Pubitemid 43164379)
7. Sturms R, DiSpirito AA, Hargrove MS (2011) Plant and cyanobacterial hemoglobins reduce nitrite to nitric oxide under anoxic conditions. Biochemistry 50:3873-3878.
8. Trevaskis B, et al. (1997) Two hemoglobin genes in Arabidopsis thaliana: The evolutionary origins of leghemoglobins. Proc Natl Acad Sci USA 94:12230-12234. (Pubitemid 27467871)
9. Bustos-Sanmamed P, et al. (2011) Regulation of nonsymbiotic and truncated hemoglobin genes of Lotus japonicus in plant organs and in response to nitric oxide and hormones. New Phytol 189:765-776.
10. Becana M, Klucas RV (1992) Oxidation and reduction of leghemoglobin in root nodules of leguminous plants. Plant Physiol 98:1217-1221.
11. Fuchsman WH, Appleby CA (1979) Separation and determination of the relative concentrations of the homogeneous components of soybean leghemoglobin by isoelectric focusing. Biochim Biophys Acta 579:314-324. (Pubitemid 9254831)
12. Whittaker RG, Moss BA, Appleby CA (1979) Determination of the blocked N-terminal of soybean leghemoglobin b. Biochem Biophys Res Commun 89:552-558. (Pubitemid 9254138)
13. Marcker A, Lund M, Jensen EØ, Marcker KA (1984) Transcription of the soybean leghemoglobin genes during nodule development. EMBO J 3:1691-1695.
14. O'Brian MR (1996) Heme synthesis in the rhizobium-legume symbiosis: A palette for bacterial and eukaryotic pigments. J Bacteriol 178:2471-2478.
15. Brown SB, Houghton JD, Wilks A (1990) Heme degradation and biosynthesis of bilins. Biosynthesis of Heme and Chlorophylls, ed Dailey HA (McGraw-Hill, New York), pp 543-575.
16. Baudouin E, Frendo P, Le Gleuher M, Puppo A (2004) A Medicago sativa haem oxygenase gene is preferentially expressed in root nodules. J Exp Bot 55:43-47. (Pubitemid 38078063)
17. Virtanen AI, Laine T (1946) Red, brown and green pigments in leguminous root nodules. Nature 157:25-26.
18. Lehtovaara P, Perttilä U (1978) Bile-pigment formation from different leghaemoglobins. Methine-bridge specificity of coupled oxidation. Biochem J 176:359-364.
19. Roponen I (1970) The effect of darkness on the leghemoglobin content and amino acid levels in the root nodules of pea plants. Physiol Plant 23:452-460.
20. Puppo A, et al. (2005) Legume nodule senescence: Roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165:683-701. (Pubitemid 40284831)
21. Becana M, Matamoros MA, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytol 188:960-976.
22. Jun H-K, Sarath G, Wagner FW (1994) Detection and purification of modified leghemoglobins from soybean root nodules. Plant Sci 100:31-40. (Pubitemid 2118672)
23. Jun H-K, et al. (1994) Characteristics of modified leghemoglobins isolated from soybean (Glycine max Merr.) root nodules. Plant Physiol 104:1231-1236. (Pubitemid 24986269)
24. Wagner FW, Sarath G (1987) Plant Senescence: Its Biochemistry and Physiology, eds Thomson WW, Nothnagel EA, Huffaker RC (Am Soc Plant Physiologists, Rockville), pp 190-197.
25. Lehtovaara P, Ellfolk N (1975) Purification and properties of Phaseolus vulgaris leghemoglobin (PhLb). Acta Chem Scand B 29:56-60.
26. 1H-NMR studies of ferric soybean leghemoglobin: Assignment of hyperfine shifted resonances of complexes with cyanide, nicotinate, pyridine and azide. Biochim Biophys Acta 625:202-220.
27. 1H NMR studies of complexes of ferric leghemoglobin with substituted pyridines and nicotinic acids. J Inorg Biochem 18:123-132.
28. 13C NMR spectroscopy: The dynamics of heme ruffling deformations. J Biol Inorg Chem 13:941-959.
29. Desbois A, Mazza G, Stetzkowski F, Lutz M (1984) Resonance Raman spectroscopy of protoheme-protein interactions in oxygen-carrying hemoproteins and in peroxidases. Biochim Biophys Acta 785:161-176.
30. Lin-Vien D, Colthup NB, Fateley WG, Grasselli JG (1991) The Handbook of Infrared and Raman Characteristic Frequencies of Organic Molecules (Academic Press, San Diego), pp 179-190.
31. Hu S, Smith KM, Spiro TG (1996) Assignment of protoheme resonance Raman spectrum by heme labeling in myoglobin. J Am Chem Soc 118:12638-12646. (Pubitemid 27041986)
32. Picaud T, Le Moigne C, Loock B, Momenteau M, Desbois A (2003) Nonplanar distortions of bis-base low-spin iron(II)-porphyrinates: Absorption and resonance Raman investigations of cross-trans-linked iron(II)-basket-handle porphyrin complexes. J Am Chem Soc 125:11616-11625. (Pubitemid 37210110)
33. Bondoc LL, Timkovich R (1989) Structural characterization of nitrimyoglobin. J Biol Chem 264:6134-6145. (Pubitemid 19106682)
34. Otsuka M, et al. (2010) Covalent modifications of hemoglobin by nitrite anion: Formation kinetics and properties of nitrihemoglobin. Chem Res Toxicol 23:1786-1795.
35. Yi J, Thomas LM, Musayev FN, Safo MK, Richter-Addo GB (2011) Crystallographic trapping of heme loss intermediates during the nitrite-induced degradation of human hemoglobin. Biochemistry 50:8323-8332.
36. Olah GA, Narang SC, Olah JA, Lammertsma K (1982) Recent aspects of nitration: New preparative methods and mechanistic studies (a review). Proc Natl Acad Sci USA 79: 4487-4494.
37. Brennan ML, et al. (2002) A tale of two controversies: Defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J Biol Chem 277:17415-17427.
38. Nicolis S, Monzani E, Roncone R, Gianelli L, Casella L (2004) Metmyoglobin-catalyzed exogenous and endogenous tyrosine nitration by nitrite and hydrogen peroxide. Chemistry 10:2281-2290.
39. Bartesaghi S, et al. (2004) Reactions of desferrioxamine with peroxynitrite-derived carbonate and nitrogen dioxide radicals. Free Radic Biol Med 36:471-483. (Pubitemid 38224519)
40. Baysal E, Monteiro HP, Sullivan SG, Stern A (1990) Desferrioxamine protects human red blood cells from hemin-induced hemolysis. Free Radic Biol Med 9:5-10.
41. Nicolis S, et al. (2006) Easy oxidation and nitration of human myoglobin by nitrite and hydrogen peroxide. Chemistry 12:749-757. (Pubitemid 43099281)
42. Wojciechowski G, de Montellano PR (2007) Radical energies and the regiochemistry of addition to heme groups. Methylperoxy and nitrite radical additions to the heme of horseradish peroxidase. J Am Chem Soc 129:1663-1672.
43. 2: Formation of heme-protein cross-links and dimeric species. Biochim Biophys Acta 1251:17-22.
44. Hargrove MS, et al. (1997) Characterization of recombinant soybean leghemoglobin a and apolar distal histidine mutants. J Mol Biol 266:1032-1042. (Pubitemid 27122607)
45. - reaction. Proc Natl Acad Sci USA 99:12691-12696.
46. Sakamoto A, et al. (2004) Three distinct Arabidopsis hemoglobins exhibit peroxidase-like activity and differentially mediate nitrite-dependent protein nitration. FEBS Lett 572:27-32. (Pubitemid 39092508)
47. Herold S, Puppo A (2005) Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: A possible role in functioning nodules? J Biol Inorg Chem 10:935-945. (Pubitemid 41682556)
48. Lee KK, Shearman LL, Erickson BK, Klucas RV (1995) Ferric leghemoglobin in plant-attached leguminous nodules. Plant Physiol 109:261-267.
49. Mathieu C, Moreau S, Frendo P, Puppo A, Davies MJ (1998) Direct detection of radicals in intact soybean nodules: Presence of nitric oxide-leghemoglobin complexes. Free Radic Biol Med 24:1242-1249. (Pubitemid 28246739)
50. 2 fixation by nitrate. I. Nitrate effects on nitrate-reductase activities of bacteroids and nodule cytosol. Planta 180:40-45.
51. Meakin GE, et al. (2007) The contribution of bacteroidal nitrate and nitrite reduction to the formation of nitrosylleghaemoglobin complexes in soybean root nodules. Microbiology 153:411-419.
52. Horchani F, et al. (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 155:1023-1036.
53. Pladys D, Barthe P, Rigaud J (1988) Changes in intracellular pH in French-bean nodules induced by senescence and nitrate treatment. Plant Sci 56:99-106.
54. Casanovas A, Carrascal M, Abián J, López-Tejero MD, Llobera M (2009) Discovery of lipoprotein lipase pI isoforms and contributions to their characterization. J Proteomics 72:1031-1039.
55. Ascoli F, Fanelli MR, Antonini E (1981) Preparation and properties of apohemoglobin and reconstituted hemoglobins. Methods Enzymol 76:72-87.
56. DeLano WL (2002) The PyMol User's Manual (DeLano Scientific, Palo Alto, CA).