دورية أكاديمية
أعرض في EDS

Unusual shift in the visible absorption spectrum of an active ctenophore photoprotein elucidated by time-dependent density functional theory.

التفاصيل البيبلوغرافية
العنوان: Unusual shift in the visible absorption spectrum of an active ctenophore photoprotein elucidated by time-dependent density functional theory.
المؤلفون: Tomilin FN; Kirensky Institute of Physics SB RAS, Federal Research Center 'Krasnoyarsk Science Center SB RAS', Akademgorodok 50/38, Krasnoyarsk, 660036, Russia.; Siberian Federal University, Svobodny 79 pr., Krasnoyarsk, 660041, Russia.; National Research Tomsk State University, Lenin Avenue 36, Tomsk, 634050, Russia., Rogova AV; Siberian Federal University, Svobodny 79 pr., Krasnoyarsk, 660041, Russia., Burakova LP; Siberian Federal University, Svobodny 79 pr., Krasnoyarsk, 660041, Russia.; Photobiology Laboratory, Institute of Biophysics SB RAS, Federal Research Center 'Krasnoyarsk Science Center SB RAS', Akademgorodok 50/50, Krasnoyarsk, 660036, Russia., Tchaikovskaya ON; National Research Tomsk State University, Lenin Avenue 36, Tomsk, 634050, Russia., Avramov PV; Kyungpook National University, 80 Daehakro, Bukgu, Daegu, 41566, South Korea., Fedorov DG; Research Center for Computational Design of Advanced Functional Materials (CD-FMat), National Institute of Advanced Industrial Science and Technology (AIST), Central 2, Umezono 1-1-1, Tsukuba, 305-8568, Japan. d.g.fedorov@aist.go.jp., Vysotski ES; Photobiology Laboratory, Institute of Biophysics SB RAS, Federal Research Center 'Krasnoyarsk Science Center SB RAS', Akademgorodok 50/50, Krasnoyarsk, 660036, Russia. eugene.vysotski@gmail.com.
المصدر: Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology [Photochem Photobiol Sci] 2021 Apr 08. Date of Electronic Publication: 2021 Apr 08.
Publication Model: Ahead of Print
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer Country of Publication: England NLM ID: 101124451 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1474-9092 (Electronic) Linking ISSN: 1474905X NLM ISO Abbreviation: Photochem Photobiol Sci Subsets: MEDLINE
أسماء مطبوعة: Publication: 2021- : [London] : Springer
Original Publication: Cambridge, UK : Royal Society of Chemistry, c2002-
مستخلص: Active hydromedusan and ctenophore Ca 2+ -regulated photoproteins form complexes consisting of apoprotein and strongly non-covalently bound 2-hydroperoxycoelenterazine (an oxygenated intermediate of coelenterazine). Whereas the absorption maximum of hydromedusan photoproteins is at 460-470 nm, ctenophore photoproteins absorb at 437 nm. Finding out a physical reason for this blue shift is the main objective of this work, and, to achieve it, the whole structure of the protein-substrate complex was optimized using a linear scaling quantum-mechanical method. Electronic excitations pertinent to the spectra of the 2-hydroperoxy adduct of coelenterazine were simulated with time-dependent density functional theory. The dihedral angle of 60° of the 6-(p-hydroxy)-phenyl group relative to the imidazopyrazinone core of 2-hydroperoxycoelenterazine molecule was found to be the key factor determining the absorption of ctenophore photoproteins at 437 nm. The residues relevant to binding of the substrate and its adopting the particular rotation were also identified.
References: Haddock, S. H. D., Moline, M. A., & Case, J. F. (2010). Bioluminescence in the sea. Annual Review of Marine Science, 2, 443–493. (PMID: 2114167210.1146/annurev-marine-120308-081028)
Widder, E. A. (2010). Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science, 328, 704–708. (PMID: 2044817610.1126/science.1174269)
Shimomura, O. (2006). Bioluminescence: chemical principles and methods. . World Scientific Publishing Co. (PMID: 10.1142/6102)
Markova, S. V., & Vysotski, E. S. (2015). Coelenterazine-dependent luciferases. Biochemistry (Mosc), 80, 714–732. (PMID: 10.1134/S0006297915060073)
Vysotski, E. S., Markova, S. V., & Frank, L. A. (2006). Calcium-regulated photoproteins of marine coelenterates. Molecular Biology, 40, 404–417. (PMID: 10.1134/S0026893306030022)
Shimomura, O., & Johnson, F. H. (1972). Structure of the light-emitting moiety of aequorin. Biochemistry, 11, 1602–1608. (PMID: 440215610.1021/bi00759a009)
Cormier, M. J., Hori, K., Karkhanis, Y. D., Anderson, J. M., Wampler, J. E., Morin, J. G., & Hastings, J. W. (1973). Evidence for similar biochemical requirements for bioluminescence among the coelenterates. Journal of Cellular Physiology, 81, 291–297. (PMID: 414439710.1002/jcp.1040810218)
Vysotski, E. S., & Lee, J. (2004). Ca 2+ -regulated photoproteins: structural insight into the bioluminescence mechanism. Accounts of Chemical Research, 37, 405–415. (PMID: 1519605010.1021/ar0400037)
Shimomura, O., & Johnson, F. H. (1975). Regeneration of the photoprotein aequorin. Nature, 256, 236–238. (PMID: 23935123935110.1038/256236a0)
Eremeeva, E. V., Natashin, P. V., Song, L., Zhou, Y., van Berkel, W. J., Liu, Z. J., & Vysotski, E. S. (2013). Oxygen activation of apoobelin-coelenterazine complex. ChemBioChem, 14, 739–745. (PMID: 234948312349483110.1002/cbic.201300002)
Bonora, M., Giorgi, C., Bononi, A., Marchi, S., Patergnani, S., Rimessi, A., Rizzuto, R., & Pinton, P. (2013). Subcellular calcium measurements in mammalian cells using jellyfish photoprotein aequorin-based probes. Nature Protocols, 8, 2105–2118. (PMID: 2411378410.1038/nprot.2013.127)
Alonso, M. T., Rodríguez-Prados, M., Navas-Navarro, P., Rojo-Ruiz, J., & García-Sancho, J. (2017). Using aequorin probes to measure Ca 2+ in intracellular organelles. Cell Calcium, 64, 3–11. (PMID: 2821402310.1016/j.ceca.2017.01.006)
Prasher, D., McCann, R. O., & Cormier, M. J. (1985). Cloning and expression of the cDNA coding for aequorin, a bioluminescent calcium-binding protein. Biochemical and Biophysical Research Communications, 126, 1259–1268. (PMID: 257964710.1016/0006-291X(85)90321-3)
Inouye, S., Noguchi, M., Sakaki, Y., Takagi, Y., Miyata, T., Iwanaga, S., Miyata, T., & Tsuji, F. I. (1985). Cloning and sequence analysis of cDNA for the luminescent protein aequorin. Proceedings of the National Academy of Sciences of the United States of America, 82, 3154–3158. (PMID: 385881339773310.1073/pnas.82.10.3154)
Prasher, D. C., McCann, R. O., Longiaru, M., & Cormier, M. J. (1987). Sequence comparisons of complementary DNAs encoding aequorin isotypes. Biochemistry, 26, 1326–1332. (PMID: 288277710.1021/bi00379a019)
Inouye, S., & Tsuji, F. I. (1993). Cloning and sequence analysis of cDNA for the Ca 2+ -activated photoprotein, clytin. FEBS Letters, 315, 343–346. (PMID: 842292810.1016/0014-5793(93)81191-2)
Inouye, S. (2008). Cloning, expression, purification and characterization of an isotype of clytin, a calcium-binding photoprotein from the luminous hydromedusa Clytia gregarium. Journal of Biochemistry, 143, 711–717. (PMID: 1829671510.1093/jb/mvn024)
Markova, S. V., Burakova, L. P., Frank, L. A., Golz, S., Korostileva, K. A., & Vysotski, E. S. (2010). Green-fluorescent protein from the bioluminescent jellyfish Clytia gregaria: cDNA cloning, expression, and characterization of novel recombinant protein. Photochemical and Photobiological Sciences, 9, 757–765. (PMID: 2044295310.1039/c0pp00023j)
Fourrage, C., Swann, K., Garcia, J. R. G., Campbell, A. K., & Houliston, E. (2014). An endogenous green fluorescent protein photoprotein pair in Clytia hemisphaerica eggs shows co-targeting to mitochondria and efficient bioluminescence energy transfer. Open Biology, 4, 130206. (PMID: 24718596404311010.1098/rsob.130206)
Fagan, T. F., Ohmiya, Y., Blinks, J. R., Inouye, S., & Tsuji, F. I. (1993). Cloning, expression and sequence analysis of cDNA for the Ca 2+ -binding photoprotein, mitrocomin. FEBS Letters, 333, 301–305. (PMID: 822419810.1016/0014-5793(93)80675-K)
Burakova, L. P., Natashin, P. V., Markova, S. V., Eremeeva, E. V., Malikova, N. P., Cheng, C., Liu, Z. J., & Vysotski, E. S. (2016). Mitrocomin from the jellyfish Mitrocoma cellularia with deleted C-terminal tyrosine reveals a higher bioluminescence activity compared to wild type photoprotein. Journal of Photochemistry and Photobiology B: Biology, 162, 286–297. (PMID: 10.1016/j.jphotobiol.2016.06.054)
Illarionov, B. A., Markova, S. V., Bondar, V. S., Vysotski, E. S., & Gitelson, J. I. (1992). Cloning and expression of cDNA for the Ca 2+ -activated photoprotein obelin from the hydroid polyp Obelia longissima. Doklady Akademii Nauk, 326, 911–913.
Illarionov, B. A., Bondar, V. S., Illarionova, V. A., & Vysotski, E. S. (1995). Sequence of the cDNA encoding the Ca 2+ -activated photoprotein obelin from the hydroid polyp Obelia longissima. Gene, 153, 273–274. (PMID: 787560010.1016/0378-1119(94)00797-V)
Markova, S. V., Vysotski, E. S., Blinks, J. R., Burakova, L. P., Wang, B. C., & Lee, J. (2002). Obelin from the bioluminescent marine hydroid Obelia geniculata: cloning, expression, and comparison of some properties with those of other Ca 2+ -regulated photoproteins. Biochemistry, 41, 2227–2236. (PMID: 1184121410.1021/bi0117910)
Ohmiya, Y., & Hirano, T. (1996). Shining the light: the mechanism of the bioluminescence reaction of calcium-binding photoproteins. Chemistry & Biology, 3, 337–347. (PMID: 10.1016/S1074-5521(96)90116-7)
Kawasaki, H., Nakayama, S., & Kretsinger, R. H. (1998). Classification and evolution of EF-hand proteins. BioMetals, 11, 277–295. (PMID: 1019149410.1023/A:1009282307967)
Head, J. F., Inouye, S., Teranishi, K., & Shimomura, O. (2000). The crystal structure of the photoprotein aequorin at 2.3 Å resolution. Nature, 18, 372–376. (PMID: 10.1038/35012659)
Liu, Z. J., Vysotski, E. S., Chen, C. J., Rose, J. P., Lee, J., & Wang, B. C. (2000). Structure of the Ca 2+ -regulated photoprotein obelin at 1.7 Å resolution determined directly from its sulfur substructure. Protein Science, 9, 2085–2093. (PMID: 11152120214449910.1110/ps.9.11.2085)
Liu, Z. J., Vysotski, E. S., Deng, L., Lee, J., Rose, J. P., & Wang, B. C. (2003). Atomic resolution structure of obelin: soaking with calcium enhances electron density of the second oxygen atom substituted at the C2-position of coelenterazine. Biochemical and Biophysical Research Communications, 311, 433–439. (PMID: 1459243210.1016/j.bbrc.2003.09.231)
Titushin, M. S., Feng, Y., Stepanyuk, G. A., Li, Y., Markova, S. V., Golz, S., Wang, B. C., Lee, J., Wang, J., Vysotski, E. S., & Liu, Z. J. (2010). NMR-derived topology of a GFP-photoprotein energy transfer complex. Journal of Biological Chemistry, 285, 40891–40900. (PMID: 10.1074/jbc.M110.133843)
Deng, L., Markova, S. V., Vysotski, E. S., Liu, Z. J., Lee, J., Rose, J., & Wang, B. C. (2004). Crystal structure of a Ca 2+ -discharged photoprotein: implications for mechanisms of the calcium trigger and bioluminescence. Journal of Biological Chemistry, 279, 33647–33652. (PMID: 10.1074/jbc.M402427200)
Liu, Z. J., Stepanyuk, G. A., Vysotski, E. S., Lee, J., Markova, S. V., Malikova, N. P., & Wang, B. C. (2006). Crystal structure of obelin after Ca 2+ -triggered bioluminescence suggests neutral coelenteramide as the primary excited state. Proceedings of the National Academy of Sciences of the United States of America, 103, 2570–2575. (PMID: 16467137141383410.1073/pnas.0511142103)
Deng, L., Vysotski, E. S., Markova, S. V., Liu, Z. J., Lee, J., Rose, J., & Wang, B. C. (2005). All three Ca 2+ -binding loops of photoproteins bind calcium ions: the crystal structures of calcium-loaded apo-aequorin and apo-obelin. Protein Science, 14, 663–675. (PMID: 15689515227929310.1110/ps.041142905)
Nelson, M. R., & Chazin, W. J. (1998). Structures of EF-hand Ca 2+ -binding proteins: diversity in the organization, packing and response to Ca 2+ binding. BioMetals, 11, 297–318. (PMID: 1019149510.1023/A:1009253808876)
Eremeeva, E. V., & Vysotski, E. S. (2019). Exploring bioluminescence function of the Ca 2+ -regulated photoproteins with site-directed mutagenesis. Photochemistry and Photobiology, 95, 8–23. (PMID: 2985504110.1111/php.12945)
Vysotski, E. S., & Lee, J. (2007). Bioluminescent mechanism of Ca 2+ -regulated photoproteins from three-dimensional structures. In V. R. Viviani & Y. Ohmiya (Eds.), Luciferases and fluorescent proteins: principles and advances in biotechnology and bioimaging. (pp. 19–41). Transworld Research Network.
Burakova, L. P., & Vysotski, E. S. (2019). Recombinant Ca 2+ -regulated photoproteins of ctenophores: current knowledge and application prospects. Applied Microbiology and Biotechnology, 103, 5929–5946. (PMID: 3117220410.1007/s00253-019-09939-0)
Ward, W. W., & Seliger, H. H. (1976). Action spectrum and quantum yield for the photoinactivation of mnemiopsin, a bioluminescent photoprotein from the ctenophores Mnemiopsis sp. Photochemistry and Photobiology, 23, 351–363. (PMID: 697910.1111/j.1751-1097.1976.tb07260.x6979)
Anctil, M., & Shimomura, O. (1984). Mechanism of photoinactivation and reactivation in the bioluminescence system of the ctenophore Mnemiopsis. Biochemistry, 221, 269–272. (PMID: 10.1042/bj2210269)
Aghamaali, M. R., Jafarian, V., Sariri, R., Molakarimi, M., Rasti, B., Taghdir, M., Sajedi, R. H., & Hosseinkhani, S. (2011). Cloning, sequencing, expression and structural investigation of mnemiopsin from Mnemiopsis leidyi: an attempt toward understanding Ca 2+ -regulated photoproteins. Protein Journal, 30, 566–574. (PMID: 10.1007/s10930-011-9363-8)
Markova, S. V., Burakova, L. P., Golz, S., Malikova, N. P., Frank, L. A., & Vysotski, E. S. (2012). The light-sensitive photoprotein berovin from the bioluminescent ctenophore Beroe abyssicola: a novel type of Ca 2+ -regulated photoprotein. FEBS Journal, 279, 856–870. (PMID: 10.1111/j.1742-4658.2012.08476.x)
Powers, M. L., McDermott, A. G., Shaner, N., & Haddock, S. H. (2013). Expression and characterization of the calcium-activated photoprotein from the ctenophore Bathocyroe fosteri: insights into light-sensitive photoproteins. Biochemical and Biophysical Research Communications, 431, 360–366. (PMID: 2326218110.1016/j.bbrc.2012.12.026)
Stepanyuk, G. A., Liu, Z. J., Burakova, L. P., Lee, J., Rose, J., Vysotski, E. S., & Wang, B. C. (2013). Spatial structure of the novel light-sensitive photoprotein berovin from the ctenophore Beroe abyssicola in the Ca 2+ -loaded apoprotein conformation state. Biochimica et Biophysica Acta, 1834, 2139–2146. (PMID: 2389174610.1016/j.bbapap.2013.07.006)
Burakova, L. P., Natashin, P. V., Malikova, N. P., Niu, F., Pu, M., Vysotski, E. S., & Liu, Z. J. (2016). All Ca 2+ -binding loops of light-sensitive ctenophore photoprotein berovin bind magnesium ions: the spatial structure of Mg 2+ -loaded apo-berovin. Journal of Photochemistry and Photobiology B: Biology, 154, 57–66. (PMID: 10.1016/j.jphotobiol.2015.11.012)
Molakarimi, M., Gorman, M. A., Mohseni, A., Pashandi, Z., Taghdir, M., Naderi-Manesh, H., Sajedi, R. H., & Parker, M. W. (2019). Reaction mechanism of the bioluminescent protein mnemiopsin1 revealed by X-ray crystallography and QM/MM simulations. Journal of Biological Chemistry, 294, 20–27. (PMID: 10.1074/jbc.RA118.006053)
Burakova, L. P., Stepanyuk, G. A., Eremeeva, E. V., & Vysotski, E. S. (2016). Role of certain amino acid residues of the coelenterazine binding cavity in bioluminescence of light-sensitive Ca 2+ -regulated photoprotein berovin. Photochemical and Photobiological Sciences, 15, 691–704. (PMID: 2711754410.1039/C6PP00050A)
Molakarimi, M., Mohseni, A., Taghdir, M., Pashandi, Z., Gorman, M. A., Parker, M. W., Naderi-Manesh, H., & Sajedi, R. H. (2017). QM/MM simulations provide insight into the mechanism of bioluminescence triggering in ctenophore photoproteins. PLoS ONE, 12, e0182317. (PMID: 28777808554420510.1371/journal.pone.0182317)
Eremeeva, E. V., Markova, S. V., Frank, L. A., Visser, A. J., van Berkel, W. J., & Vysotski, E. S. (2013). Bioluminescent and spectroscopic properties of His-Trp-Tyr triad mutants of obelin and aequorin. Photochemical and Photobiological Sciences, 12, 1016–1024. (PMID: 2352524110.1039/c3pp00002h)
Marenich, A. V., Cramer, C. J., & Truhlar, D. G. (2009). Universal solution model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. The Journal of Physical Chemistry B, 113, 6378–6396. (PMID: 1936625910.1021/jp810292n)
Schmidt, M. W., Baldridge, K. K., Boatz, J. A., et al. (1993). General atomic and molecular electronic structure system. Journal of Computational Chemistry, 14, 1347–1363. (PMID: 10.1002/jcc.540141112)
Barca, G. M. J., Bertoni, C., Carrington, L., et al. (2020). Recent developments in the general atomic and molecular electronic structure system. The Journal of Chemical Physics, 152, 154102. (PMID: 3232125910.1063/5.0005188)
Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40. (PMID: 18215316224590110.1186/1471-2105-9-40)
Roy, A., Kucukural, A., & Zhang, Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols, 5, 725–738. (PMID: 20360767284917410.1038/nprot.2010.5)
Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER suite: protein structure and function prediction. Nature Methods, 12, 7–8. (PMID: 25549265442866810.1038/nmeth.3213)
Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30, 2785–2791. (PMID: 19399780276063810.1002/jcc.21256)
Fedorov, D. G., & Kitaura, K. (2004). The importance of three-body terms in the fragment molecular orbital method. The Journal of Chemical Physics, 120, 6832–6840. (PMID: 1526758210.1063/1.1687334)
Fedorov, D. G. (2017). The fragment molecular orbital method: theoretical development, implementation in GAMESS, and applications. WIREs Computational Molecular Science, 7, e1322. (PMID: 10.1002/wcms.1322)
Gaus, M., Goez, A., & Elstner, M. (2013). Parametrization and benchmark of DFTB3 for organic molecules. Journal of Chemical Theory and Computation, 9, 338–354. (PMID: 2658903710.1021/ct300849w)
Peach, M. J. G., Benfield, P., Helgaker, T., & Tozer, D. J. (2008). Excitation energies in density functional theory: an evaluation and a diagnostic test. The Journal of Chemical Physics, 128, 044118. (PMID: 1824794110.1063/1.2831900)
Nishimoto, Y., & Fedorov, D. G. (2016). The fragment molecular orbital method combined with density-functional tight-binding and the polarizable continuum model. Physical Chemistry Chemical Physics, 18, 22047–22061. (PMID: 2721566310.1039/C6CP02186G)
Fedorov, D. G. (2019). Solvent screening in zwitterions analyzed with the fragment molecular orbital method. Journal of Chemical Theory and Computation, 15, 5404–5416. (PMID: 3146127710.1021/acs.jctc.9b00715)
معلومات مُعتمدة: 0721-2020-0033 Russian Ministry of Science and Education
تواريخ الأحداث: Date Created: 20210409 Latest Revision: 20240222
رمز التحديث: 20240223
DOI: 10.1007/s43630-021-00039-5
PMID: 33834429
قاعدة البيانات: MEDLINE
الوصف
تدمد:1474-9092
DOI:10.1007/s43630-021-00039-5