Serial crystallography captures dynamic control of sequential electron and proton transfer events in a flavoenzyme.

Arginine / metabolism Crystallography Deoxyribodipyrimidine Photo-Lyase / chemistry Electron Transport Electrons Flavin-Adenine Dinucleotide / chemistry Flavins Oxidation-Reduction Protons

Journal

Nature chemistry

ISSN: 1755-4349

Titre abrégé: Nat Chem

Pays: England

ID NLM: 101499734

Informations de publication

Date de publication:
06 2022

Historique:

received: 24 09 2020

accepted: 25 02 2022

pubmed: 9 4 2022

medline: 11 6 2022

entrez: 8 4 2022

Statut: ppublish

Résumé

Flavin coenzymes are universally found in biological redox reactions. DNA photolyases, with their flavin chromophore (FAD), utilize blue light for DNA repair and photoreduction. The latter process involves two single-electron transfers to FAD with an intermittent protonation step to prime the enzyme active for DNA repair. Here we use time-resolved serial femtosecond X-ray crystallography to describe how light-driven electron transfers trigger subsequent nanosecond-to-microsecond entanglement between FAD and its Asn/Arg-Asp redox sensor triad. We found that this key feature within the photolyase-cryptochrome family regulates FAD re-hybridization and protonation. After first electron transfer, the FAD

Identifiants

DOI: 10.1038/s41557-022-00922-3 PMID: 35393554

pubmed: 35393554

doi: 10.1038/s41557-022-00922-3

pii: 10.1038/s41557-022-00922-3

doi:

Substances chimiques

Flavins 0

Protons 0

Flavin-Adenine Dinucleotide 146-14-5

Arginine 94ZLA3W45F

Deoxyribodipyrimidine Photo-Lyase EC 4.1.99.3

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

Pagination

677-685

Informations de copyright

Références

Belevich, I., Bloch, D. A., Belevich, N., Wikström, M. & Verkhovsky, M. I. Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc. Natl Acad. Sci. USA 104, 2685–2690 (2007).

pubmed: 17293458 pmcid: 1796784 doi: 10.1073/pnas.0608794104

Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

pubmed: 9657713 doi: 10.1126/science.281.5374.237

Sun, F. et al. Crystal structure of mitochondrial respiratory membrane protein Complex II. Cell 121, 1043–1057 (2005).

pubmed: 15989954 doi: 10.1016/j.cell.2005.05.025

Alberts, B. et al. Molecular Biology of the Cell 4th edn, Ch. 14 (Garland Science, 2002).

Nicholls, D. G. & Ferguson, S. Bioenergetics 4th edn, Ch. 5 (Elsevier, 2013).

Entsch, B. & Ballou, D. P. in Encyclopedia of Biological Chemistry 2nd edn, 309-313 (Elsevier, 2013).

Wang, J., Du, X., Pan, W., Wang, X. & Wu, W. Photoactivation of the cryptochrome/photolyase superfamily. J. Photochem. Photobiol. C Photochem. Rev. 22, 84–102 (2015).

doi: 10.1016/j.jphotochemrev.2014.12.001

Kao, Y. T. et al. Ultrafast dynamics of flavins in five redox states. J. Am. Chem. Soc. 130, 13132–13139 (2008).

pubmed: 18767842 pmcid: 2637805 doi: 10.1021/ja8045469

Liu, Z. et al. Determining complete electron flow in the cofactor photoreduction of oxidized photolyase. Proc. Natl Acad. Sci. USA 110, 12966–12971 (2013).

pubmed: 23882080 pmcid: 3740875 doi: 10.1073/pnas.1311073110

Müller, P., Ignatz, E., Kiontke, S., Brettel, K. & Essen, L. O. Sub-nanosecond tryptophan radical deprotonation mediated by a protein-bound water cluster in class II DNA photolyases. Chem. Sci. 9, 1200–1212 (2018).

pubmed: 29675165 doi: 10.1039/C7SC03969G

Nohr, D. et al. Extended electron-transfer in animal cryptochromes mediated by a tetrad of aromatic amino acids. Biophys. J. 111, 301–311 (2016).

pubmed: 27463133 pmcid: 4968396 doi: 10.1016/j.bpj.2016.06.009

Aubert, C., Vos, M. H., Mathis, P., Eker, A. P. & Brettel, K. Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405, 586–590 (2000).

pubmed: 10850720 doi: 10.1038/35014644

Sancar, A. Mechanisms of DNA repair by photolyase and excision nuclease (Nobel Lecture). Angew. Chem. Int. Ed. 55, 8502–8527 (2016).

doi: 10.1002/anie.201601524

Zhong, D. Electron transfer mechanisms of DNA repair by photolyase. Annu. Rev. Phys. Chem. 66, 691–715 (2015).

pubmed: 25830375 doi: 10.1146/annurev-physchem-040513-103631

Zhao, X. et al. Reaction mechanism of (6-4) photolyase. J. Biol. Chem. 272, 32580–32590 (1997).

pubmed: 9405473 doi: 10.1074/jbc.272.51.32580

Zhang, M., Wang, L. & Zhong, D. Photolyase: dynamics and electron-transfer mechanisms of DNA repair. Arch. Biochem. Biophys. 632, 158–174 (2017).

pubmed: 28802828 pmcid: 5650541 doi: 10.1016/j.abb.2017.08.007

Chaves, I. et al. The cryptochromes: blue light photoreceptors in plants and animals. Annu. Rev. Plant Biol. 62, 335–364 (2011).

pubmed: 21526969 doi: 10.1146/annurev-arplant-042110-103759

Sancar, A. & Zhong, D. It is chemistry but not your grandfather’s chemistry. Biochemistry 56, 1–2 (2017).

pubmed: 28068777 doi: 10.1021/acs.biochem.6b01262

Brettel, K. & Byrdin, M. Reaction mechanisms of DNA photolyase. Curr. Opin. Struct. Biol. 20, 693–701 (2010).

pubmed: 20705454 doi: 10.1016/j.sbi.2010.07.003

Müller, F. Flavin radicals: chemistry and biochemistry. Free Radic. Biol. Med. 3, 215–230 (1987).

pubmed: 3311900 doi: 10.1016/0891-5849(87)90009-8

Balland, V., Byrdin, M., Eker, A. P. M., Ahmad, M. & Brettel, K. What makes the difference between a cryptochrome and DNA photolyase? A spectroelectrochemical comparison of the flavin redox transitions. J. Am. Chem. Soc. 131, 426–427 (2009).

pubmed: 19140781 doi: 10.1021/ja806540j

Park, H., Kim, S., Sancar, A. & Deisenhofer, J. Crystal structure of DNA photolyase from Escherichia coli. Science 268, 1866–1872 (1995).

pubmed: 7604260 doi: 10.1126/science.7604260

Kiontke, S. et al. Crystal structures of an archaeal class II DNA photolyase and its complex with UV-damaged duplex DNA. EMBO J. 30, 4437–4449 (2011).

pubmed: 21892138 pmcid: 3230371 doi: 10.1038/emboj.2011.313

Mees, A. et al. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 306, 1789–1793 (2004).

pubmed: 15576622 doi: 10.1126/science.1101598

Kort, R., Komori, H., Adachi, S. I., Miki, K. & Eker, A. DNA apophotolyase from Anacystis nidulans: 1.8-Å structure, 8-HDF reconstitution and X-ray-induced FAD reduction. Acta Crystallogr. D Biol. Crystallogr. 60, 1205–1213 (2004).

pubmed: 15213381 doi: 10.1107/S0907444904009321

Chapman, H. N. et al. Femtosecond X-ray protein nanocrystallography. Nature 470, 73–78 (2011).

pubmed: 21293373 pmcid: 3429598 doi: 10.1038/nature09750

Neutze, R. & Moffat, K. Time-resolved structural studies at synchrotrons and X-ray free electron lasers: opportunities and challenges. Curr. Opin. Struct. Biol. 22, 651–659 (2012).

pubmed: 23021004 pmcid: 3520507 doi: 10.1016/j.sbi.2012.08.006

Spence, J. C. H. XFELs for structure and dynamics in biology. IUCrJ 4, 322–339 (2017).

pubmed: 28875020 pmcid: 5571796 doi: 10.1107/S2052252517005760

Coquelle, N. et al. Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography. Nat. Chem. 10, 31–37 (2018).

pubmed: 29256511 doi: 10.1038/nchem.2853

Nango, E. et al. A three-dimensional movie of structural changes in bacteriorhodopsin. Science 354, 1552–1557 (2016).

pubmed: 28008064 doi: 10.1126/science.aah3497

Nogly, P. et al. Retinal isomerization in bacteriorhodopsin ÿcaptured by a femtosecond X-ray laser. Science 361, eaat0094 (2018).

pubmed: 29903883 doi: 10.1126/science.aat0094

Tenboer, J. et al. Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein. Science 346, 1242–1246 (2014).

pubmed: 25477465 pmcid: 4361027 doi: 10.1126/science.1259357

Skopintsev, P. et al. Femtosecond-to-millisecond structural changes in a light-driven sodium pump. Nature 583, 314–318 (2020).

pubmed: 32499654 doi: 10.1038/s41586-020-2307-8

Kupitz, C. et al. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513, 261–265 (2014).

pubmed: 25043005 pmcid: 4821544 doi: 10.1038/nature13453

Pande, K. et al. Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein. Science 352, 725–729 (2016).

pubmed: 27151871 pmcid: 5291079 doi: 10.1126/science.aad5081

Schmidt, M. Time-resolved macromolecular crystallography at pulsed X-ray sources. Int. J. Mol. Sci. 20, 1401 (2019).

pmcid: 6470897 doi: 10.3390/ijms20061401

Rould, M. A. & Carter, C. W. Isomorphous difference methods. Methods Enzymol. 374, 145–163 (2003).

pubmed: 14696372 doi: 10.1016/S0076-6879(03)74007-5

Nakai, S., Yoneda, F. & Yamabe, T. Theoretical study on the lowest-frequency mode of the flavin ring. Theor. Chem. Acc. 103, 109–116 (1999).

doi: 10.1007/s002140050521

Fox, K. M. & Karplus, P. A. Old yellow enzyme at 2 Å resolution: overall structure, ligand binding and comparison with related flavoproteins. Structure 2, 1089–1105 (1994).

pubmed: 7881908 doi: 10.1016/S0969-2126(94)00111-1

Lennon, B. W., Williams, C. H. & Ludwig, M. L. Crystal structure of reduced thioredoxin reductase from Escherichia coli: structural flexibility in the isoalloxazine ring of the flavin adenine dinucleotide cofactor. Protein Sci. 8, 2366–2379 (2008).

doi: 10.1110/ps.8.11.2366

White, T. A., Johnson, W. H., Whitman, C. P. & Tanner, J. J. Structural basis for the inactivation of Thermus thermophilus proline dehydrogenase by N-propargylglycine. Biochemistry 47, 5573–5580 (2008).

pubmed: 18426222 doi: 10.1021/bi800055w

Draper, R. D. & Ingraham, L. L. A potentiometric study of the flavin semiquinone equilibrium. Arch. Biochem. Biophys. 125, 802–808 (1968).

pubmed: 5671043 doi: 10.1016/0003-9861(68)90517-1

Ludwig, M. L., Schopfer, L. M., Metzger, A. L., Pattridge, K. A. & Massey, V. Structure and oxidation-reduction behavior of 1-deaza-FMN flavodoxins: modulation of redox potentials in flavodoxins. Biochemistry 29, 10364–10375 (1990).

pubmed: 2261478 doi: 10.1021/bi00497a011

Wijaya, I. M. M., Domratcheva, T., Iwata, T., Getzoff, E. D. & Kandori, H. Single hydrogen bond donation from flavin N5 to proximal asparagine ensures FAD reduction in DNA photolyase. J. Am. Chem. Soc. 138, 4368–4376 (2016).

pubmed: 27002596 doi: 10.1021/jacs.5b10533

Iwata, T., Zhang, Y., Hitomi, K., Getzoff, E. D. & Kandori, H. Key dynamics of conserved asparagine in a cryptochrome/photolyase family protein by Fourier transform infrared spectroscopy. Biochemistry 49, 8882–8891 (2010).

pubmed: 20828134 doi: 10.1021/bi1009979

Walsh, J. D. & Miller, A. F. Flavin reduction potential tuning by substitution and bending. J. Mol. Struct. THEOCHEM 623, 185–195 (2003).

doi: 10.1016/S0166-1280(02)00719-4

Domratcheva, T. Neutral histidine and photoinduced electron transfer in DNA photolyases. J. Am. Chem. Soc. 133, 18172–18182 (2011).

pubmed: 21970417 doi: 10.1021/ja203964d

Dereka, B. et al. Direct observation of a photochemical alkyne-allene reaction and of a twisted and rehybridized intramolecular charge-transfer state in a donor-acceptor dyad. J. Am. Chem. Soc. 139, 16885–16893 (2017).

pubmed: 29068229 doi: 10.1021/jacs.7b09591

Kao, Y.-T. et al. Ultrafast dynamics and anionic active states of the flavin cofactor in cryptochrome and photolyase. J. Am. Chem. Soc. 130, 7695–7701 (2008).

pubmed: 18500802 pmcid: 2661107 doi: 10.1021/ja801152h

Damiani, M. J., Nostedt, J. J. & O’Neill, M. A. Impact of the N5-proximal Asn on the thermodynamic and kinetic stability of the semiquinone radical in photolyase. J. Biol. Chem. 286, 4382–4391 (2011).

pubmed: 21131361 doi: 10.1074/jbc.M110.194696

Berndt, A. et al. A novel photoreaction mechanism for the circadian blue light photoreceptor Drosophila cryptochrome. J. Biol. Chem. 282, 13011–13021 (2007).

pubmed: 17298948 doi: 10.1074/jbc.M608872200

Mowat, C. G. et al. Kinetic and crystallographic analysis of the key active site acid base arginine in a soluble fumarate reductase. Biochemistry 40, 12292–12298 (2001).

pubmed: 11591148 doi: 10.1021/bi011360h

Senger, M. et al. How [FeFe]-hydrogenase facilitates bidirectional proton transfer. J. Am. Chem. Soc. 141, 17394–17403 (2019).

pubmed: 31580662 pmcid: 6823627 doi: 10.1021/jacs.9b09225

Stevens, D. R. & Hammes-Schiffer, S. Examining the mechanism of phosphite dehydrogenase with quantum mechanical/molecular mechanical free energy simulations. Biochemistry 59, 943–954 (2020).

pubmed: 32031785 doi: 10.1021/acs.biochem.9b01089

Van Der Kamp, M. W., Perruccio, F. & Mulholland, A. J. High-level QM/MM modelling predicts an arginine as the acid in the condensation reaction catalysed by citrate synthase. Chem. Commun. 2008, 1874–1876 (2008).

doi: 10.1039/b800496j

Keenholtz, R. A. et al. Arginine as a general acid catalyst in serine recombinase-mediated DNA cleavage. J. Biol. Chem. 288, 29206–29214 (2013).

pubmed: 23970547 pmcid: 3790019 doi: 10.1074/jbc.M113.508028

Paddock, M. L. et al. ENDOR spectroscopy reveals light induced movement of the H-bond from Ser-L223 upon forming the semiquinone (QB

pubmed: 17590017 doi: 10.1021/bi7005256

Sugahara, M. et al. Grease matrix as a versatile carrier of proteins for serial crystallography. Nat. Methods 12, 61–63 (2014).

pubmed: 25384243 doi: 10.1038/nmeth.3172

Yabashi, M., Tanaka, H. & Ishikawa, T. Overview of the SACLA facility. J. Synchrotron Rad. 22, 477–484 (2015).

doi: 10.1107/S1600577515004658

Nakane, T. et al. Data processing pipeline for serial femtosecond crystallography at SACLA. J. Appl. Crystallogr. 49, 1035–1041 (2016).

pubmed: 27275146 pmcid: 4886989 doi: 10.1107/S1600576716005720

White, T. A. et al. CrystFEL: a software suite for snapshot serial crystallography. J. Appl. Crystallogr. 45, 335–341 (2012).

doi: 10.1107/S0021889812002312

Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D. Biol. Crystallogr. 67, 235–242 (2011).

pubmed: 21460441 pmcid: 3069738 doi: 10.1107/S0907444910045749

Genick, U. K. et al. Structure of a protein photocycle intermediate by millisecond time-resolved crystallography. Science 275, 1471–1475 (1997).

pubmed: 9045611 doi: 10.1126/science.275.5305.1471

Carrillo, M. et al. High-resolution crystal structures of transient intermediates in the phytochrome photocycle. Structure 29, 743–754 (2021).

pubmed: 33756101 pmcid: 8405169 doi: 10.1016/j.str.2021.03.004

Claesson, E. et al. The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser. eLife 9, e53514 (2020).

pubmed: 32228856 pmcid: 7164956 doi: 10.7554/eLife.53514

Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352–367 (2012).

pubmed: 22505256 pmcid: 3322595 doi: 10.1107/S0907444912001308

Von Stetten, D. et al. In crystallo optical spectroscopy (icOS) as a complementary tool on the macromolecular crystallography beamlines of the ESRF. Acta Crystallogr. D Biol. Crystallogr. 71, 15–26 (2015).

doi: 10.1107/S139900471401517X

Chandran, D. & Sauro, H. M. Hierarchical modeling for synthetic biology. ACS Synth. Biol. 1, 353–364 (2012).

pubmed: 23651289 doi: 10.1021/sb300033q

Müller, F., Mayhew, S. G. & Massey, V. On the effect of temperature on the absorption spectra of free and protein-bound flavines. Biochemistry 12, 4654–4662 (1973).

pubmed: 4149349 doi: 10.1021/bi00747a017