Photoinduced damage of AsLOV2 domain is accompanied by increased singlet oxygen production due to flavin dissociation.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
05 03 2020
05 03 2020
Historique:
received:
13
09
2019
accepted:
13
02
2020
entrez:
7
3
2020
pubmed:
7
3
2020
medline:
7
3
2020
Statut:
epublish
Résumé
Flavin mononucleotide (FMN) belongs to the group of very efficient endogenous photosensitizers producing singlet oxygen,
Identifiants
pubmed: 32139757
doi: 10.1038/s41598-020-60861-2
pii: 10.1038/s41598-020-60861-2
pmc: PMC7058016
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4119Références
Baier, J. et al. Singlet oxygen generation by UVA light exposure of endogenous photosensitizers. Biophys. J. 91, 1452–1459, https://doi.org/10.1529/biophysj.106.082388 (2006).
doi: 10.1529/biophysj.106.082388
pubmed: 16751234
pmcid: 1518628
Westberg, M., Bregnhoj, M., Etzerodt, M. & Ogilby, P. R. Temperature Sensitive Singlet Oxygen Photosensitization by LOV-Derived Fluorescent Flavoproteins. The journal of physical chemistry. B 121, 2561–2574, https://doi.org/10.1021/acs.jpcb.7b00561 (2017).
doi: 10.1021/acs.jpcb.7b00561
pubmed: 28257211
Baron, R. et al. Multiple pathways guide oxygen diffusion into flavoenzyme active sites. Proceedings of the National Academy of Sciences of the United States of America 106, 10603–10608, https://doi.org/10.1073/pnas.0903809106 (2009).
doi: 10.1073/pnas.0903809106
pubmed: 19541622
pmcid: 2698890
Meissner, B., Schleicher, E., Weber, S. & Essen, L. O. The dodecin from Thermus thermophilus, a bifunctional cofactor storage protein. The Journal of biological chemistry 282, 33142–33154, https://doi.org/10.1074/jbc.M704951200 (2007).
doi: 10.1074/jbc.M704951200
pubmed: 17855371
Davies, M. J. Singlet oxygen-mediated damage to proteins and its consequences. Biochem. Biophys. Res. Commun. 305, 761–770, https://doi.org/10.1016/s0006-291x(03)00817-9 (2003).
doi: 10.1016/s0006-291x(03)00817-9
pubmed: 12763058
Ogilby, P. R. Singlet oxygen: there is indeed something new under the sun. Chem. Soc. Rev. 39, 3181–3209, https://doi.org/10.1039/b926014p (2010).
doi: 10.1039/b926014p
pubmed: 20571680
Schweitzer, C. & Schmidt, R. Physical mechanisms of generation and deactivation of singlet oxygen. Chem Rev 103, 1685–1757, https://doi.org/10.1021/cr010371d (2003).
doi: 10.1021/cr010371d
pubmed: 12744692
Davies, M. J. Reactive species formed on proteins exposed to singlet oxygen. Photochemical & photobiological sciences: Official journal of the European Photochemistry Association and the European Society for Photobiology 3, 17–25, https://doi.org/10.1039/b307576c (2004).
doi: 10.1039/b307576c
Mansoori, B. et al. Photodynamic therapy for cancer: role of natural products. Photodiagnosis Photodyn Ther 26, 395–404, https://doi.org/10.1016/j.pdpdt.2019.04.033 (2019).
doi: 10.1016/j.pdpdt.2019.04.033
pubmed: 31063860
McLean, M. A. et al. Mechanism of chromophore assisted laser inactivation employing fluorescent proteins. Anal. Chem. 81, 1755–1761, https://doi.org/10.1021/ac801663y (2009).
doi: 10.1021/ac801663y
pubmed: 19199572
pmcid: 2865575
Riani, Y. D., Matsuda, T., Takemoto, K. & Nagai, T. Green monomeric photosensitizing fluorescent protein for photo-inducible protein inactivation and cell ablation. BMC Biol. 16, 50, https://doi.org/10.1186/s12915-018-0514-7 (2018).
doi: 10.1186/s12915-018-0514-7
pubmed: 29712573
pmcid: 5928576
Redmond, R. W. & Kochevar, I. E. Spatially resolved cellular responses to singlet oxygen. Photochem Photobiio 82, 1178–1186, https://doi.org/10.1562/2006-04-14-IR-874 (2006).
doi: 10.1562/2006-04-14-IR-874
Wojtovich, A. P. & Foster, T. H. Optogenetic control of ROS production. Redox Biol 2, 368–376, https://doi.org/10.1016/j.redox.2014.01.019 (2014).
doi: 10.1016/j.redox.2014.01.019
pubmed: 24563855
pmcid: 3926119
Westberg, M. et al. Exerting better control and specificity with singlet oxygen experiments in live mammalian cells. Methods 109, 81–91, https://doi.org/10.1016/j.ymeth.2016.07.001 (2016).
doi: 10.1016/j.ymeth.2016.07.001
pubmed: 27389303
Endres, S. et al. An optogenetic toolbox of LOV-based photosensitizers for light-driven killing of bacteria. Sci Rep 8, 15021, https://doi.org/10.1038/s41598-018-33291-4 (2018).
doi: 10.1038/s41598-018-33291-4
pubmed: 30301917
pmcid: 6177443
Hilgers, F. et al. Genetically Encoded Photosensitizers as Light-Triggered Antimicrobial Agents. Int J Mol Sci 20, 4608, https://doi.org/10.3390/ijms20184608 (2019).
doi: 10.3390/ijms20184608
pmcid: 6769541
Shirmanova, M. et al. Towards PDT with Genetically Encoded Photosensitizer KillerRed: A Comparison of Continuous and Pulsed Laser Regimens in an Animal Tumor Model. PLoS ONE 10, e0144617, https://doi.org/10.1371/journal.pone.0144617 (2015).
doi: 10.1371/journal.pone.0144617
pubmed: 26657001
pmcid: 4686120
Norman, R. A. Past and future: porphyria and porphyrins. Skinmed 4, 287–292, https://doi.org/10.1111/j.1540-9740.2005.03706.x (2005).
doi: 10.1111/j.1540-9740.2005.03706.x
pubmed: 16282750
Xiong, Y., Tian, X. & Ai, H. W. Molecular Tools to Generate Reactive Oxygen Species in Biological Systems. Bioconjug Chem 30, 1297–1303, https://doi.org/10.1021/acs.bioconjchem.9b00191 (2019).
doi: 10.1021/acs.bioconjchem.9b00191
pubmed: 30986044
Jiang, H. N., Li, Y. & Cui, Z. J. Photodynamic Physiology-Photonanomanipulations in Cellular Physiology with Protein Photosensitizers. Front Physiol 8, 191, https://doi.org/10.3389/fphys.2017.00191 (2017).
doi: 10.3389/fphys.2017.00191
pubmed: 28421000
pmcid: 5378799
Ruiz-Gonzalez, R. et al. Singlet oxygen generation by the genetically encoded tag miniSOG. J. Am. Chem. Soc. 135, 9564–9567, https://doi.org/10.1021/ja4020524 (2013).
doi: 10.1021/ja4020524
pubmed: 23781844
Rodriguez-Pulido, A. et al. Correction: Assessing the potential of photosensitizing flavoproteins as tags for correlative microscopy. Chem Commun (Camb) 52, 9300, https://doi.org/10.1039/c6cc90313d (2016).
doi: 10.1039/c6cc90313d
Westberg, M., Bregnhoj, M., Etzerodt, M. & Ogilby, P. R. No Photon Wasted: An Efficient and Selective Singlet Oxygen Photosensitizing Protein. The journal of physical chemistry. B 121, 9366–9371, https://doi.org/10.1021/acs.jpcb.7b07831 (2017).
doi: 10.1021/acs.jpcb.7b07831
pubmed: 28892628
Jimenez-Banzo, A. et al. Singlet oxygen photosensitisation by GFP mutants: oxygen accessibility to the chromophore. Photochemical & photobiological sciences: Official journal of the European Photochemistry Association and the European Society for Photobiology 9, 1336–1341, https://doi.org/10.1039/c0pp00125b (2010).
doi: 10.1039/c0pp00125b
Ragas, X., Cooper, L. P., White, J. H., Nonell, S. & Flors, C. Quantification of photosensitized singlet oxygen production by a fluorescent protein. ChemPhysChem 12, 161–165, https://doi.org/10.1002/cphc.201000919 (2011).
doi: 10.1002/cphc.201000919
pubmed: 21226197
Westberg, M., Holmegaard, L., Pimenta, F. M., Etzerodt, M. & Ogilby, P. R. Rational design of an efficient, genetically encodable, protein-encased singlet oxygen photosensitizer. J. Am. Chem. Soc. 137, 1632–1642, https://doi.org/10.1021/ja511940j (2015).
doi: 10.1021/ja511940j
pubmed: 25575190
Shu, X. et al. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS biology 9, e1001041, https://doi.org/10.1371/journal.pbio.1001041 (2011).
doi: 10.1371/journal.pbio.1001041
pubmed: 21483721
pmcid: 3071375
Jensen, R. L., Arnbjerg, J. & Ogilby, P. R. Reaction of singlet oxygen with tryptophan in proteins: a pronounced effect of the local environment on the reaction rate. J. Am. Chem. Soc. 134, 9820–9826, https://doi.org/10.1021/ja303710m (2012).
doi: 10.1021/ja303710m
pubmed: 22594303
Torra, J. et al. Tailing miniSOG: structural bases of the complex photophysics of a flavin-binding singlet oxygen photosensitizing protein. Sci Rep 9, 2428, https://doi.org/10.1038/s41598-019-38955-3 (2019).
doi: 10.1038/s41598-019-38955-3
pubmed: 30787421
pmcid: 6382843
Zayner, J. P., Antoniou, C. & Sosnick, T. R. The amino-terminal helix modulates light-activated conformational changes in AsLOV2. J. Mol. Biol. 419, 61–74, https://doi.org/10.1016/j.jmb.2012.02.037 (2012).
doi: 10.1016/j.jmb.2012.02.037
pubmed: 22406525
pmcid: 3338903
Swartz, T. E. et al. The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin. The Journal of biological chemistry 276, 36493–36500, https://doi.org/10.1074/jbc.M103114200 (2001).
doi: 10.1074/jbc.M103114200
pubmed: 11443119
Salomon, M., Christie, J. M., Knieb, E., Lempert, U. & Briggs, W. R. Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39, 9401–9410 (2000).
doi: 10.1021/bi000585+
pubmed: 10924135
Desmond Molecular Dynamics System. Schrödinger Maestro 2019-2; Desmond Molecular Dynamics System; Schrödinger Inc. & D. E. Shaw Research; New York, NY (2019).
Bowers, K. J. et al. in Proceedings of the 2006 ACM/IEEE conference on Supercomputing - SC ‘06 (ACM Press, 2006).
Jorgensen, W. L. & Tirado-Rives, J. The OPLS [optimized potentials for liquid simulations] potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110, 1657–1666, https://doi.org/10.1021/ja00214a001 (1988).
doi: 10.1021/ja00214a001
pubmed: 27557051
Jorgensen, W. L., Maxwell, D. S. & TiradoRives, J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225–11236, https://doi.org/10.1021/Ja9621760 (1996).
doi: 10.1021/Ja9621760
Damm, W., Frontera, A., TiradoRives, J. & Jorgensen, W. L. OPLS all-atom force field for carbohydrates. J. Comput. Chem. 18, 1955–1970, 10.1002/(Sici)1096-987x(199712)18:16<1955::Aid-Jcc1>3.3.Co;2-A (1997).
McDonald, N. A. & Jorgensen, W. L. Development of an all-atom force field for heterocycles. Properties of liquid pyrrole, furan, diazoles, and oxazoles. J. Phys. Chem. B 102, 8049–8059, https://doi.org/10.1021/Jp981200o (1998).
doi: 10.1021/Jp981200o
Jorgensen, W. L. & McDonald, N. A. Development of an all-atom force field for heterocycles. Properties of liquid pyridine and diazenes. Theochem-Journal of Molecular Structure 424, 145–155, https://doi.org/10.1016/s0166-1280(97)00237-6 (1998).
doi: 10.1016/s0166-1280(97)00237-6
Rizzo, R. C. & Jorgensen, W. L. OPLS All-Atom Model for Amines: Resolution of the Amine Hydration Problem. J. Am. Chem. Soc. 121, 4827–4836, https://doi.org/10.1021/ja984106u (1999).
doi: 10.1021/ja984106u
Kaminski, G. A., Friesner, R. A., Tirado-Rives, J. & Jorgensen, W. L. Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides†. The Journal of Physical Chemistry B 105, 6474–6487, https://doi.org/10.1021/jp003919d (2001).
doi: 10.1021/jp003919d
Watkins, E. K. & Jorgensen, W. L. Perfluoroalkanes: Conformational Analysis and Liquid-State Properties from ab Initio and Monte Carlo Calculations. The Journal of Physical Chemistry A 105, 4118–4125, https://doi.org/10.1021/jp004071w (2001).
doi: 10.1021/jp004071w
Berendsen, H. J. C., Grigera, J. R. & Straatsma, T. P. The Missing Term in Effective Pair Potentials. J. Phys. Chem.-Us 91, 6269–6271, https://doi.org/10.1021/J100308a038 (1987).
doi: 10.1021/J100308a038
Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14(33-38), 27–38 (1996).
Chovancova, E. et al. CAVER 3.0: a tool for the analysis of transport pathways in dynamic protein structures. PLoS Comput. Biol. 8, e1002708, https://doi.org/10.1371/journal.pcbi.1002708 (2012).
doi: 10.1371/journal.pcbi.1002708
pubmed: 23093919
pmcid: 3475669
Dassault Systemes BIOVIA; Discovery Studio Client; San Diego, USA. Dassault Systemes BIOVIA; Discovery Studio 2019 Client; San Diego, USA (2019).
Gil, A. A. et al. Femtosecond to Millisecond Dynamics of Light Induced Allostery in the Avena sativa LOV Domain. The journal of physical chemistry. B 121, 1010–1019, https://doi.org/10.1021/acs.jpcb.7b00088 (2017).
doi: 10.1021/acs.jpcb.7b00088
pubmed: 28068090
pmcid: 5327423
Durr, H., Salomon, M. & Rudiger, W. Chromophore exchange in the LOV2 domain of the plant photoreceptor phototropin1 from oat. Biochemistry 44, 3050–3055, https://doi.org/10.1021/bi0478897 (2005).
doi: 10.1021/bi0478897
pubmed: 15723549
Song, S. H. et al. Modulating LOV domain photodynamics with a residue alteration outside the chromophore binding site. Biochemistry 50, 2411–2423, https://doi.org/10.1021/bi200198x (2011).
doi: 10.1021/bi200198x
pubmed: 21323358
pmcid: 3068209
Fukunaga, Y., Katsuragi, Y., Izumi, T. & Sakiyama, F. Fluorescence characteristics of kynurenine and N’-formylkynurenine. Their use as reporters of the environment of tryptophan 62 in hen egg-white lysozyme. Journal of biochemistry 92, 129–141, https://doi.org/10.1093/oxfordjournals.jbchem.a133909 (1982).
doi: 10.1093/oxfordjournals.jbchem.a133909
pubmed: 7118867
Lobley, A., Whitmore, L. & Wallace, B. A. DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18, 211–212 (2002).
doi: 10.1093/bioinformatics/18.1.211
pubmed: 11836237
Sreerama, N. & Woody, R. W. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252–260, https://doi.org/10.1006/abio.2000.4880 (2000).
doi: 10.1006/abio.2000.4880
pubmed: 11112271
Micsonai, A. et al. BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra. Nucleic Acids Res. 46, W315–W322, https://doi.org/10.1093/nar/gky497 (2018).
doi: 10.1093/nar/gky497
pubmed: 29893907
pmcid: 6031044
Tomasková, N., Varinska, L. & Sedlak, E. Rate of oxidative modification of cytochrome c by hydrogen peroxide is modulated by Hofmeister anions. General Physiology and Biophysics 29, 255–265, https://doi.org/10.4149/gpb_2010_03_255 (2010).
doi: 10.4149/gpb_2010_03_255
pubmed: 20817949
Zayner, J. P. & Sosnick, T. R. Factors that control the chemistry of the LOV domain photocycle. PLoS ONE 9, e87074, https://doi.org/10.1371/journal.pone.0087074 (2014).
doi: 10.1371/journal.pone.0087074
pubmed: 24475227
pmcid: 3903614
Leferink, N. G. et al. Identification of a gatekeeper residue that prevents dehydrogenases from acting as oxidases. The Journal of biological chemistry 284, 4392–4397, https://doi.org/10.1074/jbc.M808202200 (2009).
doi: 10.1074/jbc.M808202200
pubmed: 19088070
Yagi, K., Ohishi, N., Nishimoto, K., Choi, J. D. & Song, P. S. Effect of hydrogen bonding on electronic spectra and reactivity of flavins. Biochemistry 19, 1553–1557, https://doi.org/10.1021/bi00549a003 (1980).
doi: 10.1021/bi00549a003
pubmed: 7378363
Halavaty, A. S. & Moffat, K. N- and C-terminal flanking regions modulate light-induced signal transduction in the LOV2 domain of the blue light sensor phototropin 1 from Avena sativa. Biochemistry 46, 14001–14009, https://doi.org/10.1021/bi701543e (2007).
doi: 10.1021/bi701543e
pubmed: 18001137
Pietra, F. Molecular dynamics simulation of dioxygen pathways through mini singlet oxygen generator (miniSOG), a genetically encoded marker and killer protein. Chem. Biodivers. 11, 1883–1891, https://doi.org/10.1002/cbdv.201400125 (2014).
doi: 10.1002/cbdv.201400125
pubmed: 25491332
Alia, A., Mohanty, P. & Matysik, J. Effect of proline on the production of singlet oxygen. Amino Acids 21, 195–200, https://doi.org/10.1007/s007260170026 (2001).
doi: 10.1007/s007260170026
pubmed: 11665815
Matysik, J., Alia, A., Bhalu, B. & Mohanty, P. Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Current Science 82, 525–532 (2002).
Signorelli, S., Arellano, J. B., Melo, T. B., Borsani, O. & Monza, J. Proline does not quench singlet oxygen: evidence to reconsider its protective role in plants. Plant physiology and biochemistry: PPB 64, 80–83, https://doi.org/10.1016/j.plaphy.2012.12.017 (2013).
doi: 10.1016/j.plaphy.2012.12.017
pubmed: 23384940
Pimenta, F. M., Jensen, R. L., Breitenbach, T., Etzerodt, M. & Ogilby, P. R. Oxygen-dependent photochemistry and photophysics of “miniSOG,” a protein-encased flavin. Photochemistry and Photobiology 89, 1116–1126, https://doi.org/10.1111/php.12111 (2013).
doi: 10.1111/php.12111
pubmed: 23869989
Barnett, M. E., Baran, T. M., Foster, T. H. & Wojtovich, A. P. Quantification of light-induced miniSOG superoxide production using the selective marker, 2-hydroxyethidium. Free radical biology &. medicine 116, 134–140, https://doi.org/10.1016/j.freeradbiomed.2018.01.014 (2018).
doi: 10.1016/j.freeradbiomed.2018.01.014
Winterbourn, C. C. Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278–286, https://doi.org/10.1038/nchembio.85 (2008).
doi: 10.1038/nchembio.85
pubmed: 18421291
Di Mascio, P. et al. Singlet Molecular Oxygen Reactions with Nucleic Acids, Lipids, and Proteins. Chem Rev 119, 2043–2086, https://doi.org/10.1021/acs.chemrev.8b00554 (2019).
doi: 10.1021/acs.chemrev.8b00554
pubmed: 30721030
Kim, J. et al. Oxidative modification of cytochrome c by singlet oxygen. Free radical biology & medicine 44, 1700–1711, https://doi.org/10.1016/j.freeradbiomed.2007.12.031 (2008).
doi: 10.1016/j.freeradbiomed.2007.12.031
Marques, E. F., Medeiros, M. H. G. & Di Mascio, P. Lysozyme oxidation by singlet molecular oxygen: Peptide characterization using [(18) O]-labeling oxygen and nLC-MS/MS. Journal of mass spectrometry: JMS 52, 739–751, https://doi.org/10.1002/jms.3983 (2017).
doi: 10.1002/jms.3983
pubmed: 28801970
Kiselar, J. G., Maleknia, S. D., Sullivan, M., Downard, K. M. & Chance, M. R. Hydroxyl radical probe of protein surfaces using synchrotron X-ray radiolysis and mass spectrometry. International journal of radiation biology 78, 101–114, https://doi.org/10.1080/09553000110094805 (2002).
doi: 10.1080/09553000110094805
pubmed: 11779360
Jensen, R. L., Arnbjerg, J. & Ogilby, P. R. Temperature effects on the solvent-dependent deactivation of singlet oxygen. J. Am. Chem. Soc. 132, 8098–8105, https://doi.org/10.1021/ja101753n (2010).
doi: 10.1021/ja101753n
pubmed: 20491478