Reactive oxygen and oxidative stress: N-formyl kynurenine in photosystem II and non-photosynthetic proteins

Photosynthesis Research

Volumn 114, Issue 2, 2012, Pages 97-110

  Kasson, Tina M Dreaden ^a   Barry, Bridgette A ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

High light stress; N formylkynurenine; Photoinhibition; Photosynthetic oxygen evolution; Photosystem II; Post translational modification; Proteolysis; Reactive oxygen species; Synechocystis PCC. 6803; Tryptophan

Indexed keywords

BIOLOGICAL MARKER; DRUG DERIVATIVE; KYNURENINE; N' FORMYLKYNURENINE; N'-FORMYLKYNURENINE; REACTIVE OXYGEN METABOLITE; RIBULOSEBISPHOSPHATE CARBOXYLASE; TRYPTOPHAN;

ANIMAL; ANIMAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; OXIDATIVE STRESS; PHOTOSYSTEM II; PROTEIN PROCESSING; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; REVIEW; ULTRAVIOLET RADIATION;

ANIMALS; BIOLOGICAL MARKERS; KYNURENINE; MODELS, ANIMAL; MODELS, MOLECULAR; OXIDATIVE STRESS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; REACTIVE OXYGEN SPECIES; RIBULOSE-BISPHOSPHATE CARBOXYLASE; TRYPTOPHAN; ULTRAVIOLET RAYS;

SYNECHOCYSTIS;

EID: 84871610304     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-012-9784-z     Document Type: Review

References (101)

1. Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition: a historical perspective. Photosynth Res 76:343-370
2. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275-335
3. Anderson LB, Maderia M, Ouellette AJA, Putnam-Evans C, Higgins L, Krick T, MacCoss MJ, Lim H, Yates J III, Barry BA (2002) Posttranslational modifications in the CP43 subunit of photosystem II. Proc Natl Acad Sci USA 99:14676-14681
4. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483-495
5. Beinert H, Kennedy MC (1993) Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB J 7:1442-1449
6. Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272:20313-20316
7. Bricker TM, Frankel LK (2002) The structure and function of CP47 and CP43 in photosystem II. Photosynth Res 72:131-146
8. Busi MV, Maliandi MV, Valdez H, Clemente M, Zabaleta EJ, Araya A, Gomez-Casati DF (2006) Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe-S proteins and induces oxidative stress. Plant J 48:873-882
9. Caldwell CR (1993) Ultraviolet-induced photodegradation of cucumber (Cucumis sativus L.) microsomal and soluble protein tryptophanyl residues in vitro. Plant Physiol 101:947-953
10. Correia AR, Ow SY, Wright PC, Gomes CM (2009) The conserved Trp155 in human frataxin as a hotspot for oxidative stress related chemical modifications. Biochem Biophys Res Commun 390:1007-1011
11. Cossée M, Dürr A, Schmitt M, Dáhl N, Trouillas P, Allinson P, Kostrzewa M, Nivelon-Chevallier A, Gustavson K-H, Kohlschütter A, Müller U, Mandel J-L, Brice A, Koenig M, Cavalcanti F, Tammaro A, De Michele G, Filla A, Cocozza S, Labuda M, Montermini L, Poirier J, Pandolfo M (1999) Friedreich's ataxia: point mutations and clinical presentation of compound heterozygotes. Ann Neurol 45:200-206
12. Dall'Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R (2007) Different roles of α- and β- branch xanthophylls in photosystem assembly and photoprotection. J Biol Chem 282:35056-35068
13. D'Autreaux B, Toledana M (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostatis. Nat Rev Mol Cell Biol 8:813-824
14. Davies MJ (2003) Singlet oxygen-mediated damage to proteins and its consequences. Biochem Biophys Res Commun 305:761-770
15. Davies MJ, Truscott RJW (2001) Photo-oxidation of proteins and its role in cataractogenesis. J Photochem Photobiol B 63:114-125
16. Delatycki MB, Williamson R, Forrest SM (2000) Friedreich ataxia: an overview. J Med Genet 37:1-8
17. Demmig-Adams B, Cohu CM, Muller O, Adams WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113:75-88
18. Dreaden Kasson TM, Rexroth S, Barry BA (2012) Light-induced oxidative Stress, N-formylkynurenine, and oxygenic photosynthesis. PLoS One 7:e42220
19. Dreaden TM, Chen J, Rexroth S, Barry BA (2011) N-formylkynurenine as a marker of high light stress in photosynthesis. J Biol Chem 286:22632-22641
20. Ehrenshaft M, Silva SdO, Perdivara I, Bilski P, Sik RH, Chignell CF, Tomer KB, Mason RP (2009) Immunological detection of N-formylkynurenine in oxidized proteins. Free Radic Biol Med 46:1260-1266
21. Ehrenshaft M, Bonini MG, Feng L, Chignell CF, Mason RP (2010) Partial colocalization of oxidized, N-formylkynurenine-containing proteins in mitochondria and Golgi of keratinocytes. Photochem Photobiol 86:752-756
22. Fedorova M, Todorovsky T, Kuleva N, Hoffmann R (2010) Quantitative evaluation of tryptophan oxidation in actin and troponin I from skeletal muscles using a rat model of acute oxidative stress. Proteomics 10:2692-2700
23. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831-1838
24. Finkel T (2001) Signal transduction by reactive oxygen species. J Cell Biol 194:7-15
25. 5 cluster of photosystem II: implications for the identification of oxygen channels within the photosystem. Biochemistry 51:6371-6377
26. Fujimori E (1981) Blue fluorescence and crosslinking of photooxidized proteins. FEBS Lett 135:257-260
27. Galetskiy D, Lohscheider JN, Kononikhin AS, Popov IA, Nikolaev EN, Adamska I (2011) Mass spectrometric characterization of photooxidative protein modifications in Arabidopsis thaliana thylakoid membranes. Rapid Commun Mass Spectrom 25:184-190
28. Garab G, Cseh Z, Kovács L, Rajagopal S, Várkonyi Z, Wentworth M, Mustárdy L, Dér A, Ruban AV, Papp E, Holzenburg A, Horton P (2002) Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41:15121-15129
29. Gießauf A, Steiner E, Esterbauer H (1995) Early destruction of tryptophan residues of apolipoprotein B is a vitamin E independent process during copper mediated oxidation of LDL. Biochim Biophys Acta 1256:221-232
30. Gießauf A, van Wickern B, Simat T, Steinhart H, Esterbauer H (1996) Formation of N-formylkynurenine suggests the involvement of apolipoprotein B-100 centered tryptophan radicals in the initiation of LDL lipid peroxidation. FEBS Lett 389:136-140
31. Gracanin M, Hawkins CL, Pattison DI, Davies MJ (2009) Singlet-oxygen-mediated amino acid and protein oxidation: formation of tryptophan peroxides and decomposition products. Free Radic Biol Med 47:92-102
32. Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725-749
33. Grossman AR, Bhaya D, Apt KE, Kehoe DM (1995) Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu Rev Genet 29:231-288
34. Gruszka J, Pawlak A, Kruk J (2008) Tocochromanols, plastoquinol, and other biological prenyllipids as singlet oxygen quenchers-determination of singlet oxygen quenching rate constants and oxidation products. Free Radic Biol Med 45:920-928
35. Guptasarma P, Balasubramanian D, Matsugo S, Saito I (1992) Hydroxyl radical mediated damage to proteins, with special reference to the crystallins. Biochemistry 31:4296-4303
36. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334-342
37. Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706:68-80
38. Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Ann Rev Biochemistry 76:223-241
39. Helland R, Fjellbirkeland A, Karlsen OA, Ve T, Lillehaug JR, Jensen HB (2008) An oxidized tryptophan facilitates copper binding in Methylococcus capsulatus-secreted protein MopE. J Biol Chem 283:13897-13904
40. Herman C, Prakash S, Lu CZ, Matouschek A, Gross CA (2003) Lack of a robust unfoldase activity confers a unique level of substrate specificity to the universal AAA protease FtsH. Mol Cell 11:659-669
41. Hideg E, Spetea C, Vass I (1994) Singlet oxygen and free radical production during acceptor-induced and donor-side photoinhibition: studies with spin-trapping EPR spectroscopy. Biochim Biophys Acta 1186:143-152
42. 2 addition. Photosynth Res 38:417-423
43. Huang HV, Bond MW, Hunkapiller MW, Hood LE (1983) Cleavage at tryptophanyl residues with dimethylsulfoxide hydrochloric acid and cyanogen bromide. Methods Enzymol 91:318-324
44. Huesgen PF, Schuhmann H, Adamska I (2006) Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett 580:6929-6932
45. Hunzinger C, Wozny W, Schwall GP, Poznanović S, Stegmann W, Zengerling H, Schoepf R, Groebe K, Cahill MA, Osiewacz HD, Jägemann N, Bloch M, Dencher NA, Krause F, Schrattenholz A (2006) Comparative profiling of the mammalian mitochondrial proteome: multiple aconitase-2 isoforms including N-formylkynurenine modifications as part of a protein biomarker signature for reactive oxidative species. J Proteome Res 5:625-633
46. Inoue M, Sato EF, Nishikawa M, Park A-M, Kira Y, Imada I, Utsumi K (2003) Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr Med Chem 10:2495-2505
47. Inoue S, Ejima K, Iwai E, Hayashi H, Appel J, Tyystjarvi E, Murata N, Nishiyama N (2011) Protection by alpha-tocopherol of the repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803. Biochim Biophys Acta 807:236-241
48. Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211-231
49. α-diformylkynurenine. Arch Biochem Biophys 186:84-88
50. Janes SM, Mu D, Wemmer D, Smith AJ, Kaur S, Maltby D, Burlingame AL, Klinman JP (1990) A new redox cofactor in eukaryotic enzymes: 6-hydroxydopa at the active site of bovine serum amine oxidase. Science 248:981-987
51. Ji JA, Zhang BY, Cheng W, Wang YJ (2009) Methionine, tryptophan, and histidine oxidation in a model protein, PTH: mechanisms and stabilization. J Pharm Sci 98:4485-4500
52. Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci USA 100:98-103
53. Karlsen OA, Berven FS, Stafford GP, Larsen O, Murrell JC, Jensen HB, Fjellbirkeland A (2003) The surface-associated and secreted MopE protein of Methylococcus capsulatus (Bath) responds to changes in the concentration of copper in the growth medium. Appl Environ Microbiol 69:2386-2388
54. Keren N, Krieger-Liszkay A (2011) Photoinhibition: molecular mechanisms and physiological significance. Physiol Plant 142:1-5
55. Kim CH, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9:435-439
56. Koeck T, Stuehr DJ, Aulak KS (2005) Mitochondria and regulated tyrosine nitration. Biochem Soc Trans 33:1399-1403
57. Komenda J, Barker M, Kuviková S, de Vries R, Mullineaux CW, Tichy M, Nixon PJ (2006) The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp. PCC 6803. J Biol Chem 281:1145-1151
58. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551-564
59. Kruk J, Strzalka K, Leblanc RM (1992) Monolayer study of plastoquinones, α-tocopherol quinone, their hydroquinone forms and their interaction with monogalatosyldiacylglycerol. Charge-transfer complexes in a mixed monolayer. Biochim Biophys Acta 1112:19-26
60. Kühlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367:614-621
61. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040-1044
62. Lynch SM, Frei B (1993) Mechanisms of copper-dependent and iron-dependent oxidative modification of human low density lipoprotein. J Lipid Res 34:1745-1753
63. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300-309
64. Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127-1133
65. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Ann Rev Plant Biol 57:521-565
66. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742-749
67. Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56:357-363
68. Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1-16
69. Nyström T (2005) Role of oxidative carbonylation in protein quality control and senescence. EMBO J 24:1311-1317
70. Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32 kilodalton polypeptides in chloroplast membranes. J Cell Biol 99:481-485
71. Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494-8499
72. Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta 1787:1151-1160
73. Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817:218-231
74. Previero A, Coletti-Previero M-A, Jollès P (1967) Localization of non-essential tryptophan residues for biological activity of lysozyme. J Mol Biol 24:261-268
75. Rexroth S, Poetsch A, Rogner M, Hamann A, Werner A, Osiewacz HD, Schafer ER, Seelert H, Dencher NA (2012) Reactive oxygen species target specific tryptophan site in the mitochondrial ATP synthase. Biochim Biophys Acta 1817:381-387
76. Rhee K-H, Morris EP, Barber J, Kühlbrandt W (1998) Three-dimensional structure of the plant photosystem II reaction center at 8 Å resolution. Nature 396:283-286
77. Rinalducci S, Pedersen JZ, Zolla L (2004) Formation of radicals from singlet oxygen produced during photoinhibition of isolated light-harvesting proteins of photosystem II. Biochim Biophys Acta 1608:63-73
78. Rinalducci S, Campostrini N, Antonioli P, Righetti PG, Roepstorff P, Zolla L (2005) Formation of truncated proteins and high-molecular-mass aggregates upon soft illumination of photosynthetic proteins. J Proteome Res 4:2327-2337
79. Roose JL, Wegener KM, Pakrasi HB (2007) The extrinsic proteins of photosystem II. Photosynth Res 92:369-387
80. Santabarbara S, Neverov KV, Garlaschi FM, Zucchelli G, Jennings RC (2001) Involvement of uncoupled antenna chlorophylls in photoinhibition in thylakoids. FEBS Lett 491:109-113
81. Shi L-X, Schröder WP (2004) The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim Biophys Acta 1608:75-96
82. Simat T, Meyer K, Steinhart H (1994) Synthesis and analysis of oxidation of carbonyl condensation compounds of tryptophan. J Chromatogr A 661:93-99
83. Stadtman ER (1990) Covalent modification reactions are marking steps in protein turnover. Biochemistry 29:6323-6331
84. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL (1989) Beyond cholesterol. Modifications of low density lipoprotein that increase its atherogenicity. New Engl J Med 320:915-924
85. Steinbrecher UP, Parthasarathy S, Leake DS, Witztum JL, Steinberg D (1984) Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc Natl Acad Sci USA 81:3883-3887
86. Taylor SW, Fahy E, Murray J, Capaldi RA, Ghosh SS (2003) Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins. J Biol Chem 278:19587-19590
87. Telfer A (2005) Too much light? How β-carotene protects the photosystem II reaction centre. Photochem Photobiol Sci 4:950-956
88. Thomas C, Mackey MM, Diaz AA, Cox DP (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
89. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55-60
90. Vásquez-Vivar J, Kalyanaraman B, Kennedy MC (2000) Mitochondrial aconitase is a source of hydroxyl radical - an electron spin resonance investigation. J Biol Chem 275:14064-14069
91. A species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89:1408-1412
92. Wagner D, Przybyla D, Camp ROD, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183-1185
93. Walrant P, Santus R (1974) Ultraviolet and N-formylkynurenine-sensitized photoactivation of bovine carbonic anhydrase: and internal photodynamic effect. Photochem Photobiol 20:455-460
94. Yamamoto Y, Akasaka T (1995) Degradation of antenna chlorophyll-binding protein CP43 during photoinhibition of Photosystem II. Biochemistry 34:9038-9045
95. Yang D-H, Paulsen H, Andersson B (2000) The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis. FEBS Lett 466:385-388
96. 2 evolving complex. Coord Chem Rev 252:296-305
97. Zhao H, Sagert J, Hwang DS, Waite JH (2009) Glycosylated hydroxytryptophan in a mussel adhesive protein from Perna viridis. J Biol Chem 284:23344-23352
98. Zigler JS, Goosey JD (1981) Photosensitized oxidation in the ocular lens: evidence for photosensitizers endogenous to the human lens. Photochem Photobiol 33:869-874
99. Zigler JS, Jernigan HM, Garland D, Reddy VN (1985) The effects of "oxygen radicals" generated in the medium on lenses in organ culture: inhibition of damage by chelated iron. Arch Biochem Biophys 241:163-172
100. Zolla L, Rinalducci S (2002) Involvement of active oxygen species in degradation of light-harvesting proteins under light stresses. Biochemistry 41:14391-14402
101. Zouni A, Witt H-T, Kern J, Fromme P, Krauß N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739-743