دورية أكاديمية
أعرض في EDS

Characterization of the active site in the thiocyanate-forming protein from Thlaspi arvense (TaTFP) using EPR spectroscopy.

التفاصيل البيبلوغرافية
العنوان: Characterization of the active site in the thiocyanate-forming protein from Thlaspi arvense (TaTFP) using EPR spectroscopy.
المؤلفون: Hashemi Haeri H; Martin Luther University Halle-Wittenberg, Institute of Chemistry, Von-Danckelmann-Platz 4, D-06120 Halle (Saale), Germany., Schneegans N; Institute of Pharmaceutical Biology, Technische Universität Braunschweig, D-38106 Braunschweig, Germany., Eisenschmidt-Bönn D; Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany., Brandt W; Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany., Wittstock U; Institute of Pharmaceutical Biology, Technische Universität Braunschweig, D-38106 Braunschweig, Germany., Hinderberger D; Martin Luther University Halle-Wittenberg, Institute of Chemistry, Von-Danckelmann-Platz 4, D-06120 Halle (Saale), Germany.
المصدر: Biological chemistry [Biol Chem] 2023 Aug 17; Vol. 405 (2), pp. 105-118. Date of Electronic Publication: 2023 Aug 17 (Print Publication: 2024).
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Walter De Gruyter Country of Publication: Germany NLM ID: 9700112 Publication Model: Electronic-Print Cited Medium: Internet ISSN: 1437-4315 (Electronic) Linking ISSN: 14316730 NLM ISO Abbreviation: Biol Chem Subsets: MEDLINE
أسماء مطبوعة: Publication: Berlin : Walter De Gruyter
Original Publication: Berlin ; New York : W. De Gruyter, c1996-
مواضيع طبية MeSH: Thiocyanates*/chemistry , Thiocyanates*/metabolism , Thlaspi*/metabolism, Catalytic Domain ; Electron Spin Resonance Spectroscopy ; Iron/metabolism ; Oxidation-Reduction
مستخلص: Glucosinolates are plant thioglucosides, which act as chemical defenses. Upon tissue damage, their myrosinase-catalyzed hydrolysis yields aglucones that rearrange to toxic isothiocyanates. Specifier proteins such as thiocyanate-forming protein from Thlaspi arvense (TaTFP) are non-heme iron proteins, which capture the aglucone to form alternative products, e.g. nitriles or thiocyanates. To resolve the electronic state of the bound iron cofactor in TaTFP, we applied continuous wave electron paramagnetic resonance (CW EPR) spectroscopy at X -and Q -band frequencies (∼9.4 and ∼34 GHz). We found characteristic features of high spin and low spin states of a d 5 electronic configuration and local rhombic symmetry during catalysis. We monitored the oxidation states of bound iron during conversion of allylglucosinolate by myrosinase and TaTFP in presence and absence of supplemented Fe 2+ . Without added Fe 2+ , most high spin features of bound Fe 3+ were preserved, while different g '-values of the low spin part indicated slight rearrangements in the coordination sphere and/or structural geometry. We also examined involvement of the redox pair Fe 3+ /Fe 2 in samples with supplemented Fe 2+ . The absence of any EPR signal related to Fe 3+ or Fe 2+ using an iron-binding deficient TaTFP variant allowed us to conclude that recorded EPR signals originated from the bound iron cofactor.
(© 2023 Walter de Gruyter GmbH, Berlin/Boston.)
References: Adams, J., Kelso, R., and Cooley, L. (2000). The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell. Biol. 10: 17–24, https://doi.org/10.1016/s0962-8924(99)01673-6 . (PMID: 10.1016/s0962-8924(99)01673-6)
Backenköhler, A., Eisenschmidt, D., Schneegans, N., Strieker, M., Brandt, W., and Wittstock, U. (2018). Iron is a centrally bound cofactor of specifier proteins involved in glucosinolate breakdown. PLoS One 5: e0205755, https://doi.org/10.1371/journal.pone.0205755 . (PMID: 10.1371/journal.pone.0205755)
Bolman, P.S.H., Safarik, I., Stiles, D.A., Tyerman, W.J.R., and Strausz, O.P. (1970). Electron paramagnetic resonance spectra of some sulfur-containing radicals. Can. J. Chem. 48: 3872–3876, https://doi.org/10.1139/v70-651 . (PMID: 10.1139/v70-651)
Brandt, W., Backenköhler, A., Schulze, E., Plock, A., Herberg, T., Roese, E., and Wittstock, U. (2014). Molecular models and mutational analyses of plant specifier proteins suggest active site residues and reaction mechanism. Plant Mol. Biol. 84: 173–188, https://doi.org/10.1007/s11103-013-0126-0 . (PMID: 10.1007/s11103-013-0126-0)
Burow, M., Markert, J., Gershenzon, J., and Wittstock, U. (2006). Comparative biochemical characterization of nitrile-forming proteins from plants and insects that alter myrosinase-catalysed hydrolysis of glucosinolates. FEBS J. 273: 2432–2446, https://doi.org/10.1111/j.1742-4658.2006.05252.x . (PMID: 10.1111/j.1742-4658.2006.05252.x)
Eisenschmidt-Bönn, D., Schneegans, N., Backenköhler, A., Wittstock, U., and Brandt, W. (2019). Structural diversification during glucosinolate breakdown: mechanisms of thiocyanate, epithionitrile and simple nitrile formation. Plant J. 99: 329–343, https://doi.org/10.1111/tpj.14327 . (PMID: 10.1111/tpj.14327)
Feig, A.L. and Lippard, S.J. (1994). Reactions of Non-Heme iron (III) centers with dioxygen in biology and chemistry. Chem. Rev. 94: 759–805, https://doi.org/10.1021/cr00027a011 . (PMID: 10.1021/cr00027a011)
Ferreira, C.M.H., Pinto, I.S., Soares, E.V., and Soares, H.M. (2015). (Un) suitability of the use of pH buffers in biological, biochemical and environmental studies and their interaction with metal ions – a review. RSC Adv. 5: 30989–31003, https://doi.org/10.1039/c4ra15453c . (PMID: 10.1039/c4ra15453c)
Finel, C. and Kevan, L. (1993). Effects of Fe3+ on electron spin echo signals in zeolites. J. Chem. Soc. Faraday Trans. 89: 2559–2565, https://doi.org/10.1039/ft9938902559 . (PMID: 10.1039/ft9938902559)
Gaffney, B.J., Mavrophilipos, D.V., and Doctor, K.S. (1993). Access of ligands to the ferric center in lipoxygenase-1. Biophys. J. 64: 773–783, https://doi.org/10.1016/s0006-3495(93)81438-3 . (PMID: 10.1016/s0006-3495(93)81438-3)
Gaffney, B.J. (2009). EPR of mononuclear non-Heme iron proteins. In: Berliner, L. and Hanson, G. (Eds.), High resolution EPR applications to metalloenzymes and metals in medicine, biological magnetic resonance . Springer, New York, pp. 232–268.
Gamarra, L.F., Pontuschka, W.M., Amaro, E., Costa-Filho, A.J., Brito, G.E.S., Vieira, E.D., Carneiro, S.M., Escriba, D.M., Falleiros, A.M.F., and Salvador, V.L. (2008). Kinetics of elimination and distribution in blood and liver of biocompatible ferrofluids based on Fe3O4 nanoparticles: an EPR and XRF study. Mater. Sci. Eng. 28: 519–525, https://doi.org/10.1016/j.msec.2007.06.005 . (PMID: 10.1016/j.msec.2007.06.005)
Gonçalves, L.C.P., Mansouri, H.R., Bastos, E.L., Abdellah, M., Fadiga, B.S., Sá, J., Rudroff, F., and Mihovilovic, M.D. (2019). Morpholine-based buffers activate aerobic photobiocatalysis via spin correlated ion pair formation. Catal. Sci. Technol. 9: 1365–1371, https://doi.org/10.1039/c8cy02524j . (PMID: 10.1039/c8cy02524j)
Gumz, F., Krausze, J., Eisenschmidt, D., Backenköhler, A., Barleben, L., Brandt, W., and Wittstock, U. (2015). The crystal structure of the thiocyanate-forming protein from Thlaspi arvense, a kelch protein involved in glucosinolate breakdown. Plant Mol. Biol. 89: 67–81, https://doi.org/10.1007/s11103-015-0351-9 . (PMID: 10.1007/s11103-015-0351-9)
Habib, A., Tabata, M., and Wu, Y.G. (2005). Formation of gold nanoparticles by good’s buffers. Bull. Chem. Soc. Jpn. 78: 262–269, https://doi.org/10.1246/bcsj.78.262 . (PMID: 10.1246/bcsj.78.262)
Hasegawa, H. and Nakamura, K. (2010). Tryptophan hydroxylase and serotonin synthesis regulation. In: Müller, C.P. and Jacobs, B.L. (Eds.), Handbook of behavioral neuroscience . Elsevier, pp. 183–202.
Hinderberger, D., Ebner, S., Mayr, S., Jaun, B., Reiher, M., Goenrich, M., Thauer, R.K., and Harmer, J. (2008). Coordination and binding geometry of methyl-coenzyme M in the red1m state of methyl-coenzyme M reductase. J. Biol. Inorg. Chem. 13: 1275–1289, https://doi.org/10.1007/s00775-008-0417-0 . (PMID: 10.1007/s00775-008-0417-0)
Hinderberger, D., Piskorski, R.P., Goenrich, M., Thauer, R.K., Schweiger, A., Harmer, J., and Jaun, B. (2006). A nickel-alkyl bond in an inactivated state of the enzyme catalyzing methane formation. Angew. Chem. Int. Ed. 45: 3602–3607, https://doi.org/10.1002/anie.200600366 . (PMID: 10.1002/anie.200600366)
Hunold, J., Eisermann, J., Brehm, M., and Hinderberger, D. (2020). Characterization of aqueous lower polarity solvation shells around amphiphilic TEMPO radicals in water. J. Phys. Chem. B 124: 8601–8609, https://doi.org/10.1021/acs.jpcb.0c04863 . (PMID: 10.1021/acs.jpcb.0c04863)
Kappl, R., Eltis, L.D., Caspersen, M.B., Christensen, H.E.M., and Hüttermann, J. (2007). Site-specific oxidation of the (Fe4S4) cubanes in high-potential iron sulfur proteins as probed by EPR and orientation-selective proton ENDOR spectroscopy: Ectothiorhodospira halophila I versus Rhodocyclus tenuis. Appl. Magn. Reson. 31: 483–507, https://doi.org/10.1007/bf03166598 . (PMID: 10.1007/bf03166598)
Kappl, R., Bracic, G., and Hüttermann, J. (2009). Probing structural and electronic parameters in randomly oriented metalloproteins by orientation-selective ENDOR spectroscopy. In: Berliner, L., and Hanson, G. (Eds.), High resolution EPR applications to metalloenzymes and metals in medicine, biological magnetic resonance . Springer, New York, pp. 63–103.
Kostka, K.L., Fox, B.G., Hendrich, M.P., Collins, T.J., Rickard, C.E.F., Wright, J., and Munck, E. (1993). High-valent transition metal chemistry. Mössbauer and EPR studies of high-spin (S = 2) iron (1V) and intermediate-spin (S = 3/2) iron (II1) complexes with a macrocyclic Tetraamido-N ligand. J. Am. Chem. Soc. 115: 6746–6757, https://doi.org/10.1021/ja00068a035 . (PMID: 10.1021/ja00068a035)
Kuchernig, J.C., Backenköhler, A., Lübbecke, M., Burow, M., and Wittstock, U. (2011). A thiocyanate-forming protein generates multiple products upon allylglucosinolate breakdown in Thlaspi arvense. Phytochemistry 72: 1699–1709, https://doi.org/10.1016/j.phytochem.2011.06.013 . (PMID: 10.1016/j.phytochem.2011.06.013)
Kuchernig, J.C., Burow, M., and Wittstock, U. (2012). Evolution of specifier proteins in glucosinolate-containing plants. BMC Evol. Biol. 12: 127, https://doi.org/10.1186/1471-2148-12-127 . (PMID: 10.1186/1471-2148-12-127)
Labute, P. (2008). The generalized Born/volume integral implicit solvent model: estimation of the free energy of hydration using London dispersion instead of atomic surface area. J. Comput. Chem. 29: 1693–1698, https://doi.org/10.1002/jcc.20933 . (PMID: 10.1002/jcc.20933)
Lassmann, G., Kolberg, M., Bleifuss, G., Gräslund, A., Sjöberg, B.M., and Lubitz, W. (2003). Protein thiyl radicals in disordered systems: a comparative EPR study at low temperature. Phys. Chem. 5: 2442–2453, https://doi.org/10.1039/b302601a . (PMID: 10.1039/b302601a)
Maltempo, M.M. and Moss, T.H. (1976). The spin 3/2 state and quantum spin mixtures in haem proteins. Q. Rev. Biophys. 9: 181–215, https://doi.org/10.1017/s0033583500002407 . (PMID: 10.1017/s0033583500002407)
Matile, P. (1980). Die Senfölbombe. Zur Kompartimentierung des Myrosinasesystems. Biochem. Physiol. Pflanz. 175: 722–731, https://doi.org/10.1016/s0015-3796(80)80059-x . (PMID: 10.1016/s0015-3796(80)80059-x)
Molecular Operating Environment (MOE), 2019.01 (2019). Chemical Computing Group ULC, 910-1010 Sherbrooke St. W., Montreal, QC H3A 2R7, Canada.
Mumm, R., Burow, M., Bukovinszkine’Kiss, G., Kazantzidou, E., Wittstock, U., Dicke, M., and Gershenzon, J. (2008). Formation of simple nitriles upon glucosinolate hydrolysis affects direct and indirect defense against the specialist herbivore, Pieris rapae. J. Chem. Ecol. 34: 1311–1321, https://doi.org/10.1007/s10886-008-9534-z . (PMID: 10.1007/s10886-008-9534-z)
Neese, F. (2009). Spin-Hamiltonian parameters from first principle calculations: Theory and application. In: Berliner, L. and Hanson, G. (Eds.), High resolution EPR applications to metalloenzymes and metals in medicine, biological magnetic resonance . Springer, New York, pp. 175–229.
Noveron, J.C., Olmstead, M.M., and Mascharak, P.K. (1998). Effect of carboxamido N coordination to iron on the redox potential of low-spin non-Heme iron centers with N,S coordination: relevance to the iron site of nitrile hydratase. Inorg. Chem. 37: 1138–1139, https://doi.org/10.1021/ic971388a . (PMID: 10.1021/ic971388a)
Palmer, G. (1985). The electron paramagnetic resonance of metalloproteins. Biochem. Soc. Trans. 13: 548–560, https://doi.org/10.1042/bst0130548 . (PMID: 10.1042/bst0130548)
Peisach, J., Blumberg, W.E., Lode, E.T., and Coon, R.M. (1971a). An analysis of the electron paramagnetic resonance spectrum of pseudomonas oleovorans rubredoxin. A method for determination of the ligands of ferric iron in completely rhombic sites. J. Biol. Chem. 246: 5877–5881, https://doi.org/10.1016/s0021-9258(18)61807-1 . (PMID: 10.1016/s0021-9258(18)61807-1)
Peisach, J., Blumberg, W.E., Ogawa, S., Rachmilewitz, E.A., and Oltzik, R. (1971b). The effects of protein conformation on the heme symmetry in high spin ferric heme proteins as studied by electron paramagnetic resonance. J. Biol. Chem. 246: 3342–3355, https://doi.org/10.1016/s0021-9258(18)62232-x . (PMID: 10.1016/s0021-9258(18)62232-x)
Preoteasa, E.A., Schianchi, G., Camillo Giori, D., Duliu, O.G., Butturini, A., and Izzi, G. (2013). Unexpected detection of low and high spin ferrihemoglobin derivatives in blood serum of polytransfused patients with homozygous β-thalassemia under chelation therapy. An EPR study. Dig. J. Nanomater. Biostruct. 8: 469–499.
Que, L.Jr and Ho, R.Y. (1996). Dioxygen activation by enzymes with mononuclear non-Heme iron active sites. Chem. Rev. 96: 2607–2624, https://doi.org/10.1021/cr960039f . (PMID: 10.1021/cr960039f)
Rask, L., Andréasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B., and Meijer, J. (2000). Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42: 93–114, https://doi.org/10.1023/a:1006380021658 .
Reed, A.C. and Guiset, F.A. (1996). “Magnetochemical” series. Ligand field strengths of weakly binding anions deduced from S = 3/2, 5/2 spin state mixing in iron (III) porphyrins. J. Am. Chem. Soc. 118: 3281–3282, https://doi.org/10.1021/ja954263i . (PMID: 10.1021/ja954263i)
Rowland, J.M., Olmstead, M., and Mascharak, P.K. (2001). Syntheses, structures, and reactivity of low spin iron(III) complexes containing a single carboxamido nitrogen in a (FeN5L) chromophore. Inorg. Chem. 40: 2810–2817, https://doi.org/10.1021/ic001127s . (PMID: 10.1021/ic001127s)
Shankar, S., Peters, M., Steinborn, K., Krahwinkel, B., Sönnichsen, F.D., Grote, D., Sander, W., Lohmiller, T., Rüdiger, O., and Herges, R. (2018). Light-controlled switching of the spin state of iron (III). Nat. Commun. 9: 4750, https://doi.org/10.1038/s41467-018-07023-1 . (PMID: 10.1038/s41467-018-07023-1)
Simonato, J.P., Pécaut, J., Le Pape, L., Oddou, J.L., Jeandey, C., Shang, M., Scheidt, W.R., Wojaczyński, J., Wołowiec, S., Latos-Grazyński, L., et al.. (2000). An integrated approach to the mid-spin state (S = 3/2) in six-coordinate iron (III) chiroporphyrins. Inorg. Chem. 39: 3978–3987, https://doi.org/10.1021/ic000150a . (PMID: 10.1021/ic000150a)
Ślawska-Waniewska, A., Mosiniewicz-Szablewska, E., Nedelko, N., Gałązka-Friedman, J., and Friedman, A. (1993). Magnetic studies of iron-entities in human tissues. J. Magn. Magn. Mater. 272–276: 2417–2419, https://doi.org/10.1016/j.jmmm.2003.12.843 . (PMID: 10.1016/j.jmmm.2003.12.843)
Solomon, E.I., Brunold, T.C., Davis, M.I., Kemsley, J.N., Lee, S.K., Lehnert, N., Neese, F., Skulan, A.J., Yang, Y.S., and Zhou, J. (2000). Geometric and electronic structure/function correlations in non-heme iron enzymes. Chem. Rev. 100: 235–350, https://doi.org/10.1021/cr9900275 . (PMID: 10.1021/cr9900275)
Traka, M.H., Saha, S., Huseby, S., Kopriva, S., Walley, P.G., Barker, G.C., Moore, J., Mero, G., van den Bosch, F., Constant, H., et al.. (2013). Genetic regulation of glucoraphanin accumulation in Beneforté broccoli. New Phytol. 198: 1085–1095, https://doi.org/10.1111/nph.12232 . (PMID: 10.1111/nph.12232)
Vinck, E. (2007). The strength of EPR and ENDOR techniques in revealing structure–function relationships in metalloproteins. Phys.Chem. Chem. Phys. 9: 4620–4638, https://doi.org/10.1039/b701568b . (PMID: 10.1039/b701568b)
Van Doorslaer, S. (2017). Understanding heme proteins with hyperfine spectroscopy. J. Magn. Reson. 280: 79–88, https://doi.org/10.1016/j.jmr.2017.01.008 . (PMID: 10.1016/j.jmr.2017.01.008)
van Gastel, M., Lubitz, W., Lassmann, G., and Neese, F. (2004). Electronic structure of the cysteine thiyl radical: a DFT and correlated ab initio study. J. Am. Chem. Soc. 126: 2237–2246, https://doi.org/10.1021/ja038813l . (PMID: 10.1021/ja038813l)
Walker, F.A. (1999). Magnetic spectroscopic (EPR, ESEEM, Mössbauer, MCD and NMR) studies of low-spin ferri heme centers and their corresponding heme proteins. Coord. Chem. Rev. 185–186: 471–534, https://doi.org/10.1016/s0010-8545(99)00029-6 . (PMID: 10.1016/s0010-8545(99)00029-6)
Wang, Y., Davis, I., Chan, Y., Naik, S.G., Griffith, W.P., and Liu, A. (2020). Characterization of the nonheme iron center of cysteamine dioxygenase and its interaction with substrates. J. Biol. Chem. 33: 11789–11802, https://doi.org/10.1074/jbc.ra120.013915 . (PMID: 10.1074/jbc.ra120.013915)
Wittstock, U., Kliebenstein, D.J., Lambrix, V.M., Reichelt, M., and Gershenzon, J. (2003). Glucosinolate hydrolysis and its impact on generalist and specialist insect herbivores. In: Romeo, J.T. (Ed.). Recent advances in phytochemistry , Vol. 37. Elsevier, pp. 101–125.
Wittstock, U., Kurzbach, E., Herfurth, A.M., and Stauber, E.J. (2016). Glucosinolate breakdown. Adv Bot Res. 80: 125–169.
Zhang, W., Wang, W., Liu, Z., Xie, Y., Wang, H., Mu, Y., Huang, Y., and Feng, Y. (2016). Crystal structure of the Epithiospecifier Protein, ESP from Arabidopsis thaliana provides insights into its product specificity. Biochem. Biophys. Res. Commun. 478: 746–751, https://doi.org/10.1016/j.bbrc.2016.08.019 . (PMID: 10.1016/j.bbrc.2016.08.019)
Zhang, W., Zhou, Y., Wang, K., Dong, Y., Wang, W., Feng, Y. (2017). Crystal structure of the nitrile-specifier protein NSP1 from Arabidopsis thaliana. Biochem. Biophys. Res. Commun . 488: 147–152, https://doi.org/10.1016/j.bbrc.2017.05.027 . (PMID: 10.1016/j.bbrc.2017.05.027)
فهرسة مساهمة: Keywords: allylglucosinolate; catalysis; electron paramagnetic resonance; non-heme iron proteins; specifier proteins
المشرفين على المادة: O748SU14OM (thiocyanate)
0 (Thiocyanates)
E1UOL152H7 (Iron)
تواريخ الأحداث: Date Created: 20230816 Date Completed: 20240216 Latest Revision: 20240216
رمز التحديث: 20240216
DOI: 10.1515/hsz-2023-0187
PMID: 37586381
قاعدة البيانات: MEDLINE
الوصف
تدمد:1437-4315
DOI:10.1515/hsz-2023-0187