Nitric oxide: A radical molecule in quest of free radicals in proteins

Cellular and Molecular Life Sciences

Volumn 55, Issue 8-9, 1999, Pages 1054-1067

  Guittet, O ^a   Roy, B ^a   Lepoivre, M ^a  

^a CNRS   (France)

Author keywords

Nitric oxide; Nitrosotyrosine; Nitrotyrosine; Photosystem II; Prostaglandin H synthase; Radicals; Ribonucleotide reductase; Tyrosyl radicals

Indexed keywords

3 NITROTYROSINE; ARACHIDONIC ACID; FREE RADICAL; NITRIC OXIDE; PEROXIDASE; PROSTAGLANDIN SYNTHASE; PROTEIN; RIBONUCLEOTIDE REDUCTASE;

ANIMAL CELL; ARACHIDONIC ACID METABOLISM; ENZYME ACTIVITY; ENZYME INACTIVATION; IRON METABOLISM; MOUSE; NONHUMAN; PHOTOSYSTEM II; REVIEW;

EID: 0032800689     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050356     Document Type: Review

References (75)

1. 1 Beckman J. S. and Koppenol W. H. (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am. J. Physiol. 271: C1424-C1437
2. 2 Odonnell V. B., Chumley P. H., Hogg N., Bloodsworth A., Darleyusmar V. M. and Freeman B. A. (1997) Nitric oxide inhibition of lipid peroxidation: kinetics of reaction with lipid peroxyl radicals and comparison with alpha-tocopherol. Biochemistry 36; 15216-15223
3. 3 Wink D. A., Grisham M. B., Mitchell J. B. and Ford P. C. (1996) Direct and indirect effects of nitric oxide in chemical reactions relevant to biology. Methods Enzymol. 268: 12-31
4. 4 Eiserich J. P., Butler J., Vandervliet A., Cross C. E. and Halliwell B. (1995) Nitric oxide rapidly scavenges tyrosine and tryptophan radicals. Biochem. J. 310: 745-749
5. 5 Pedersen J. Z. and Finazzi-Agro A. (1993) Protein-radical enzymes. FEBS Lett. 325: 53-58
6. 6 Petrouleas V. and Diner B. A. (1990) Formation by NO of nitrosyl adducts of redox components of the photosystem II reaction center. 1. NO binds to the acceptor-side non-heme iron. Biochim. Biophys. Acta 1015: 131-140
7. 7 Lepoivre M., Fieschi F., Coves J., Thelander L. and Fontecave M. (1991) Inactivation of ribonucleotide reductase by nitric oxide. Biochem. Biophys. Res. Commun. 179: 442-448
8. 8 Gunther M. R., Hsi L. C., Curtis J. F., Gierse J. K., Marnett L. J., Eling T. E., et al. (1997) Nitric oxide trapping of the tyrosyl radical of prostaglandin H synthase-2 leads to tyrosine iminoxyl radical and nitrotyrosine formation. J. Biol. Chem. 272: 17086-17090
9. 9 Sjöberg B.-M., Reichard P., Gräslund A. and Ehrenberg A. (1977) Nature of the free radical in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 252: 536-541
10. 10 Jordan A. and Reichard P. (1998) Ribonucleotide reductases. Annu. Rev. Biochem. 67: 71-98
11. 11 Fontecave M. (1998) Ribonucleotide reductases and radical reactions. Cell. Mol. Life Sci. 54: 684-695
12. 12 Guittet O., Ducastel B., Salem J. S., Henry Y., Rubin H., Lemaire G. et al. (1998) Differential sensitivity of the tyrosyl radical of mouse ribonucleotide reductase to nitric oxide and peroxynitrite. J. Biol. Chem. 273: 22136-22144
13. 13 Roy B., Lepoivre M., Henry Y. and Fontecave M. (1995) Inhibition of ribonucleotide reductase by nitric oxide derived from thionitrites: reversible modifications of both subunits. Biochemistry 34: 5411-5418
14. 14 Eklund H., Eriksson M., Uhlin U., Nordlund P. and Logan D. (1997) Ribonucleotide reductase structural studies of a radical enzyme. Biol. Chem. 378: 821-825
15. 15 Reichard P. (1988) Interactions between deoxyribonucleotide and DNA synthesis. Annu. Rev. Biochem. 57: 349-374
16. 16 Nyholm S., Mann G. J., Johansson A. G., Bergeron R. J., Gräslund A. and Thelander L. (1993) Role of ribonucleotide reductase in inhibition of mammalian cell growth by potent iron chelators. J. Biol. Chem. 268: 26200-26205
17. 17 Babcock G. T., Espe M., Hoganson C., Lydakis-Simantiris N., McCracken J., Shi W. et al. (1997) Tyrosyl radicals in enzyme catalysis: some properties and a focus on photosynthetic water oxidation. Acta Chem. Scand. 51: 533-540
18. 18 Nordlund P., Sjöberg B.-M. and Eklund H. (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345: 593-598
19. 19 Kauppi B., Nielsen B. A., Ramaswamy S., Larsen I. K., Thelander M., Thelander L. et al. (1996) The three-dimensional structure of mammalian ribonucleotide reductase protein R2 reveals a more-accessible iron-radical site than Escherichia coli R2. J. Mol. Biol. 262: 706-720
20. 20 Ormo M., Regnström K., Wang Z. G., Que L., Sahlin M. and Sjöberg B. M. (1995) Residues important for radical stability in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 270: 6570-6576
21. 21 Sahlin M., Petersson L., Gräslund A., Ehrenberg A., Sjöberg B.-M. and Thelander L. (1987) Magnetic interaction between the tyrosyl free radical and the antiferromagnetically coupled iron center in ribonucleotide reductase. Biochemistry 26: 5541-5548
22. 22 Cooper C. E., Lynagh G. R., Hoyes K. P., Hider R. C., Cammack R. and Porter J. B. (1996) The relationship of intracellular iron chelation to the inhibition and regeneration of human ribonucleotide reductase. J. Biol. Chem. 271: 20291-20299
23. 23 Uhlin U. and Eklund H. (1994) Structure of ribonucleotide reductase protein R1. Nature 370: 533-539
24. 24 Mao S. S., Holler T. P., Yu G. X., Bollinger J.-M., Booker S., Johnston M. I. et al. (1992) A model for the role of multiple cysteine residues involved in ribonucleotide reduction: amazing and still confusing. Biochemistry 31: 9733-9743
25. 25 Persson A. L., Eriksson M., Katterle B., Potsch S., Sahlin M. and Sjöberg B. M. (1997) A new mechanism-based radical intermediate in a mutant R1 protein affecting the catalytically essential Glu(441) in Escherichia coli ribonucleotide reductase. J. Biol. Chem. 272: 31533-31541
26. 26 Eriksson M., Uhlin U., Ramaswamy S., Ekberg M., Regnström K., Sjöberg B. M. et al. (1997) Binding of allosteric effectors to ribonucleotide reductase protein R1: reduction of active-site cysteines promotes substrate binding. Structure 5: 1077-1092
27. 27 Logan D. T., Su X. D., Aberg A., Regnström K., Hajdu J., Eklund H. and Nordlund P. (1996) Crystal structure of reduced protein R2 of ribonucleotide reductase: the structural basis for oxygen activation at a dinuclear iron site. Structure 4: 1053-1064
28. 28 Janzen E. G., Wilcox A. L. and Manoharan V. (1993) Reactions of nitric oxide with phenolic antioxidants and phenoxy radicals. J. Org. Chem. 58: 3597-3599
29. 29 Wilcox A. L. and Janzen E. G. (1993) Nitric oxide reactions with antioxidants in model systems: sterically hindered phenols and α-tocopherol in sodium dodecyl sulfate (SDS) micelles. J. Chem. Soc. Chem. Commun. 18: 1377-1379
30. 30 Haskin C. J., Ravi N., Lynch J. B., Munck E. and Que L. (1995) Reaction of NO with the reduced R2 protein of ribonucleotide reductase from Escherichia coli. Biochemistry 34: 11090-11098
31. 31 Han J. Y., Gräslund A., Thelander L. and Sykes A. G. (1997) Kinetic studies on the reduction of the R2 subunit of mouse ribonucleotide reductase with hydroxyurea, hydrazine, phenylhydrazine and hydroxylamine. J. Biol. Inorg. Chem. 2: 287-294
32. 32 Davydov R., Sahlin M., Kuprin S., Gräslund A. and Ehrenberg A. (1996) Effect of the tyrosyl radical on the reduction and structure of the Escherichia coli ribonucleotide reductase protein R2 diferric site as probed by EPR on the mixed-valent state. Biochemistry 35: 5571-5576
33. 33 Davydov R. M., Davydov A., Ingemarson R., Thelander L., Ehrenberg A. and Gräslund A. (1997) EPR study of the mixed-valent diiron sites in mouse and herpes simplex virus ribonucleotide reductases: effect of the tyrosyl radical on structure and reactivity of the diferric center. Biochemistry 36: 9093-9100
34. 34 Lepoivre M., Chenais B., Yapo A., Lemaire G., Thelander L. and Tenu J.-P. (1990) Alterations of ribonucleotide reductase activity following induction of the nitrite-generating pathway in adenocarcinoma cells. J. Biol. Chem. 265: 14143-14149
35. 35 Kwon N. S., Stuehr D. J. and Nathan C. F. (1991) Inhibition of tumor cell ribonucleotide reductase by macrophage-derived nitric oxide. J. Exp. Med. 174: 761-767
36. 36 Eriksson S., Gräslund A., Skog S., Thelander L. and Tribukait B. (1984) Cell-cyde-dependent regulation of mammalian ribonucleotide reductase: the S phase-correlated increase in subunit M2 is regulated by de novo protein synthesis. J. Biol. Chem. 259: 11695-11700
37. 37 Kotake Y., Tanigawa T., Tanigawa M., Ueno I., Allen D. R. and Lai C. S. (1996) Continuous monitoring of cellular nitric oxide generation by spin trapping with an iron-dithiocarbamate complex. Biochim. Biophys. Acta 1289: 362-368
38. 38 Laurent M., Lepoivre M. and Tenu J. P. (1996) Kinetic modelling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochem. J. 314: 109-113
39. 39 Brown G. C., Bolanos J. P., Heales S. J. R. and Clark J. B. (1995) Nitric oxide produced by activated astrocytes rapidly and reversibly inhibits cellular respiration. Neurosci. Lett. 193: 201-204
40. 40 Lepoivre M., Flaman J. M., Bobe P., Lemaire G. and Henry Y. (1994) Quenching of the tyrosyl free radical of ribonucleotide reductase by nitric oxide - relationship to cytostasis induced in tumor cells by cytotoxic macrophages. J. Biol. Chem. 269: 21891-21897
41. 41 Wang Z., Wang M. and Carr B. I. (1998) The inhibitory effect of interleukin 1β on rat hepatocyte DNA synthesis is mediated by nitric oxide. Hepatology 28: 430-435
42. 42 Melkova Z. and Esteban M. (1995) Inhibition of vaccinia virus DNA replication by inducible expression of nitric oxide synthase. J. Immunol. 155: 5711-5718
43. 43 Lepoivre M., Flaman J.-M. and Henry Y. (1992) Early loss of the tyrosyl radical in ribonucleotide reductase of adenocarcinoma cells producing nitric oxide. J. Biol. Chem. 267: 22994-23000
44. 44 Fan H. Z., Villegas C. and Wright J. A. (1996) A link between ferritin gene expression and ribonucleotide reductase R2 protein, as demonstrated by retroviral vector mediated stable expression of R2 cDNA. FEBS Lett. 382: 145-148
45. 45 Hibbs J. B. Jr., Taintor R. R. and Vavrin Z. (1984) Iron depletion: possible cause of tumor cell toxicity induced by activated macrophages. Biochem Biophys. Res. Commun. 123: 716-723
46. 46 Drapier J.-C. and Bouton C. (1996) Modulation by nitric oxide of metalloprotein regulatory activities. Bioessays 18: 549-556
47. 47 Babcock G. T., Barry B. A., Debus R. J., Hoganson C. W., Atamian M., McIntosh L. et al. (1989) Water oxidation in photosystem II: from radical chemistry to multielectron chemistry. Biochemistry 28: 9557-9565
48. 48 Hoganson C. W. and Babcock G. T. (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953-1956
49. 49 Tommos C., Hoganson C. W., Valentin M. D., Lydakis-Simantiris N., Dorlet P., Westphal K. et al. (1998) Manganese and tyrosyl radical function in photosynthetic oxygen evolution. Curr. Opin. Chem. Biol. 2: 244-252
50. 50 Barry B. and Babcock G. T. (1987) Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. USA 84: 7099-7103
51. 51 Razeghifard M. R., Klughammer C. and Pace R. J. (1997) Electron paramagnetic resonance kinetic studies of the S states in spinach thylakoids. Biochemistry 36: 86-92
52. 52 Debus R. J. (1988) Site-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. USA 85: 427-430
53. u of photosystem II. J. Am. Chem. Soc. 119: 4787-4788
54. 54 Szalai V. A. and Brudvig G. W. (1996) Reversible binding of nitric oxide to tyrosyl radicals in photosystem II: nitric oxide quenches formation of the S3 EPR signal species in acetate-inhibited photosystem II. Biochemistry 35: 15080-15087
55. 2 + -deficient photosystem II. Biochemistry 28: 8984-8989
56. 56 Boussac A., Zimmermann J.-L., Rutherford A. W. and Lavergne J. (1990) Histidine oxidation in the oxygen-evolving photosystem-II enzyme. Nature 341: 303-306
57. 57 Hallahan B. J., Nugent J. H. A., Warden J. T. and Evans M. C. W. (1992) Investigation of the origin of the 'S3' EPR signal from the oxygen-evolving complex of photosystem 2: the role of tyrosine Z. Biochemistry 31: 4562-4573
58. 58 Gilchrist M. L. Jr., Ball J. A., Randall D. W. and Britt R. D. (1995) Proximity of the manganese cluster of photosystem II to the redox-active tyrosine YZ. Proc. Natl. Acad. Sci. USA 92: 9545-9549
59. · of photosystem II to form an iminoxyl radical. Biochemistry 36: 1411-1417
60. 60 Smith W. L., Garavito R. M. and DeWitt D. L. (1996) Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J. Biol. Chem. 271: 33157-33160
61. 61 Karthein R., Dietz R., Nastainczyk W. and Ruf H. H. (1988) Higher oxidation states of prostaglandin H synthase: EPR study of a transient tyrosyl radical in the enzyme during the peroxidase reaction. Eur. J. Biochem. 171: 313-320
62. 62 Tsai A., Hsi L. C., Kulmacz R. J., Palmer G. and Smith W. L. (1994) Characterization of the tyrosyl radicals in ovine prostaglandin H synthase-1 by isotope replacement and site-directed mutagenesis. J. Biol. Chem. 269: 5085-5091
63. 63 DeGray J. A., Lassmann G., Curtis J. F., Kennedy T. A., Marnett L. J., Eling T. E. et al. (1992) Spectral analysis of the protein-derived tyrosyl radicals from prostaglandin H synthase. J. Biol. Chem. 267: 23583-23588
64. 64 Lassmann G., Odenwaller R., Curtis J. F., DeGray J. A., Mason R. P., Marnett L. J. et al. (1991) Electron spin resonance investigation of tyrosyl radicals of prostaglandin H synthase: relation to enzyme catalysis. J. Biol. Chem. 266: 20045-20055
65. 65 Tsai A., Kulmacz R. J. and Palmer G. (1995) Spectroscopic evidence for reaction of prostaglandin H synthase-1 tyrosyl radical with arachidonic acid. J. Biol. Chem. 270: 10503-10508
66. 66 Tsai A., Palmer G., Xiao G., Swinney D. C. and Kulmacz R. J. (1998) Structural characterization of arachidonyl radicals formed by prostaglandin H synthase-2 and prostaglandin H synthase-1 reconstituted with mangano protoporphyrin IX. J. Biol. Chem. 273: 3888-3894
67. 67 Shimokawa T., Kulmacz R. J., DeWitt D. L. and Smith W. L. (1990) Tyrosine 385 of prostaglandin endoperoxide synthase is required for cyclooxygenase catalysis. J. Biol. Chem. 265: 20073-20076
68. 2. Eur. J. Biochem. 171: 321-328
69. 69 Goodwin D. C., Gunther M. R., Hsi L. C., Crews B. C., Eling T. E., Mason R. P. et al. (1998) Nitric oxide trapping of tyrosyl radicals generated during prostaglandin endoperoxide synthase turnover: detection of the radical derivative of tyrosine 385. J. Biol. Chem. 273: 8903-8909
70. 70 Hajjar D. P., Lander H. M., Pearce S. F., A., Upmacis R. K. and Pomerantz K. B. (1995) Nitric oxide enhance-sprostaglandin-H synthase-1 activity by a heme-independent mechanism: evidence implicating nitrosothiols. J. Am. Chem. Soc. 117: 3340-3346
71. 71 Tsai A. L., Wei C., and Kulmacz R. J. (1994) Interaction between nitric oxide and prostaglandin H synthase. Arch. Biochem. Biophys. 313: 367-372
72. 72 Maccarrone M., Putti S. and Finazzi Agro A. (1997) Nitric oxide donors activate the cyclo-oxygenase and peroxidase activities of prostaglandin H synthase. FEBS Lett. 410: 470-476
73. 73 Leeuwenburgh C., Rusmussen J. E., Hsu F. F., Mueller D. M., Pennathur S. and Heinecke J. W. (1997) Mass spectrometric quantification of markers for protein oxidation by tyrosyl radical, copper, and hydroxyl radical in low density lipoprotein isolated from human atherosclerotic plaques. J. Biol. Chem. 272: 3520-3526
74. 74 Hausladen A. and Stamler J. S. (1998) Nitric oxide in plant immunity. Proc. Natl. Acad. Sci. USA 95: 10345-10347
75. · in water-splitling. Biochemistry 36: 12062-12070