Photosynthesis Research

, Volume 130, Issue 1–3, pp 167–182 | Cite as

Characterization of nineteen antimony(III) complexes as potent inhibitors of photosystem II, carbonic anhydrase, and glutathione reductase

  • Mehmet Sayım Karacan
  • Margarita V. Rodionova
  • Turgay Tunç
  • Kübra Begüm Venedik
  • Serhat Mamaş
  • Alexandr V. Shitov
  • Sergei K. Zharmukhamedov
  • Vyacheslav V. Klimov
  • Nurcan Karacan
  • Suleyman I. Allakhverdiev
Original Article

Abstract

Nineteen antimony(III) complexes were obtained and examined as possible herbicides. Six of these were synthesized for the first time, and their structures were identified using elemental analyses, 1H-NMR, 13C-NMR, FTIR, LCMS, magnetic susceptibility, and conductivity measurement techniques. For the nineteen examined antimony(III) complexes their most-stable forms were determined by DFT/B3LYP/LanL2DZ calculation method. These compounds were examined for effects on photosynthetic electron transfer and carbonic anhydrase activity of photosystem II, and glutathione reductase from chloroplast as well were investigated. Our results indicated that all antimony(III) complexes inhibited glutathione reductase activity of chloroplast. A number of these also exhibited good inhibitory efficiency of the photosynthetic and carbonic anhydrase activity of Photosystem II.

Keywords

Photosystem II (PSII) Carbonic anhydrase Glutathione reductase Antimony(III) complexes Inhibitors 

Supplementary material

11120_2016_236_MOESM1_ESM.docx (433 kb)
Supplementary material 1 (DOCX 879 kb)

References

  1. Alcona MJ, Iglesias M, Sanchez F, Viani I (2001) Synthesis of Rh(I) and Ir(I) complexes with chiral C2-multitopic ligands Structural and catalytic properties. J Organomet Chem 634:25–33CrossRefGoogle Scholar
  2. Allakhverdiev SI, Zharmukhamedov SK, Klimov VV, Vasiliev SS, Korvatovsky BN, Pashchenko VZ (1989) Effect of dinoseb and other phenolic-compounds on fluorescence decay kinetics of photosystem-II chlorophyll in higher-plants. Biol Membr 6:1147–1153Google Scholar
  3. Alscher RG (1989) Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant 77:457–464CrossRefGoogle Scholar
  4. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefPubMedPubMedCentralGoogle Scholar
  5. Asada K (1999) The water–water cycle in chloroplasts: scavenging active oxygen species and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639CrossRefPubMedGoogle Scholar
  6. Aslan HG, Ozcan S, Karacan N (2011) Synthesis, characterization and antimicrobial activity of salicylaldehyde benzenesulfonylhydrazone (Hsalbsmh) and its Nickel(II), Palladium(II), Platinum(II), Copper(II), Cobalt(II) complexes. Inorg Chem Commun 14:1550–1553CrossRefGoogle Scholar
  7. Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Phys and Plant Mol Biol 45:369–393CrossRefGoogle Scholar
  8. Balaban A, Colak N, Unver H (2008) Synthesis, spectroscopic studies and crystal structure of N, N’-bis((thiophene-2-carboxamido)propyl)piperazine. J Chem Crystallogr 38:369–372CrossRefGoogle Scholar
  9. Baranski AS, Fawcett WR, Gilbert CM (1985) Use of microelectrodes for the rapid determination of the number of electrons involved in an electrode reaction. Anal Chem 57:166–170CrossRefGoogle Scholar
  10. Carlberg I, Mannervik B (1985) Glutathione reductase assay. Meth Enzymol 113:484–495CrossRefPubMedGoogle Scholar
  11. Disli A, Mercan S, Yavuz S (2013) Synthesis and antimicrobial activity of new pyrimidine derivatives incorporating 1H-tetrazol-5-ylthio moiety. J Heterocycl Chem 50:1446–1450CrossRefGoogle Scholar
  12. Duke SO, Dayan FE (2011) Bioactivity of herbicides. In: Moo-Young Murray (ed) Comprehensive biotechnology, vol 4, 2nd edn. Elsevier Press, Amsterdam, pp 23–35CrossRefGoogle Scholar
  13. Eckes P, van Almsick C, Weilder M (2004) Gene expression profiling, a revolutionary tool in bayer crop science herbicide discovery. Pflanzenschutz-Nachrichten Bayer 57:62–77Google Scholar
  14. Fedorchuk TP, Rudenko NN, Ignatova LK, Ivanov BN (2014) The presence of soluble carbonic anhydrase in the thylakoid lumen of chloroplasts from Arabidopsis leaves. J Plant Physiol 171:903–906CrossRefPubMedGoogle Scholar
  15. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavacharin K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA (2003) Gaussian, Inc., Pittsburgh PA., Gaussian 03 (Revision B.04)Google Scholar
  16. Govindjee and Eaton-Rye JJ (1986) Electron transfer through photosystem II acceptors: interactions with anions. Photosynth Res 10:365–379CrossRefPubMedGoogle Scholar
  17. Granero GE, Longhi MR, Becker C, Junginger HE, Kopp S, Midha KK, Shah VP, Stavchansky S, Dressman JB, Barends DM (2008) Biowaiver monographs for immediate release solid oral dosage forms: acetazolamide. J Pharm Sci 97:3691–3699CrossRefPubMedGoogle Scholar
  18. Grellier P, Marozienė A, Nivinskas H, Dolidze A, Chedia R, Kavtaradze N, Čėnas N (2011) Antiplasmodial in vitro activity of chysanthemoylsubstituted quinones: roles of single-electron reduction potential and glutathione reductase inhibition. Chemija 22:229–233Google Scholar
  19. Ignatova LK, Rudenko NN, Khristin MS, Ivanov BN (2006) Heterogeneous origin of carbonic anhydrase activity of thylakoid membranes. Biochemistry (Moscow) 71:525–532CrossRefGoogle Scholar
  20. Kaplan NO (1985) Methods in enzymology. Academic Press, Orlando, (113) 484–495Google Scholar
  21. Karacan MS, Yakan C, Yakan M, Karacan N, Zharmukhamedov SK, Shitov A, Los DA, Klimov VV, Allakhverdiev SI (2012) Quantitative structure-activity relationship analysis of perfluoroiso-propyldinitrobenzene derivatives known as photosystem II electron transfer inhibitors. BBA (Bioenergetics) 1817:1229–1236CrossRefGoogle Scholar
  22. Karacan MS, Zharmukhamedov SK, Mamas S, Kupriyanova EV, Shitov AV, Klimov VV, Ozbek N, Ozmen U, Gunduzalp A, Schmitt F-J, Karacan N, Friedrich T, Los DA, Carpentier R, Allakhverdiev SI (2014) Screening of novel chemical compounds as possible inhibitors of carbonic anhydrase and photosynthetic activity of photosystem II. J Photochem Photobiol, B 137:156–167CrossRefGoogle Scholar
  23. Karacan MS, Tunç T, Oruç T, Mamas S, Karacan N (2015) A new method for screening glutathione reductase inhibitors using square wave voltammetry. Anal Methods 7:5142–5148CrossRefGoogle Scholar
  24. Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G (1998) A novel alpha-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17:1208–1216CrossRefPubMedPubMedCentralGoogle Scholar
  25. Klimov VV, Allakhverdiev SI, Shuvalov VA, Krasnovsky AA (1982) Effect of extraction and re-addition of manganese on light reactions of photosystem-II preparations. FEBS Lett 148:307–312CrossRefPubMedGoogle Scholar
  26. Klimov VV, Allakhverdiev SI, Zharmukhamedov SK (1989) Redox interactions of the phenolic herbicide Dinoseb and chlorophyll P680-pheophytin pair [P680 Pp] in the reaction center of photosystem 2 in plants. Fiziol Rastenii 36:770–777Google Scholar
  27. Lewis RA, Schoenwald RD, Eller MG, Barfknecht ChF, Phelps ChD (1984) Ethoxzolamide analogue gel. Arch Ophthalmol 102:1821–1824CrossRefPubMedGoogle Scholar
  28. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760CrossRefPubMedGoogle Scholar
  29. Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res 109:133–149CrossRefPubMedGoogle Scholar
  30. Moskvin OV, Shutova TV, Khristin MS, Ignatova LK, Villarejo A, Samuelsson G, Klimov VV, Ivanov BN (2004) Carbonic anhydrase activities in pea thylakoids. Photosynth Res 79:93–100CrossRefPubMedGoogle Scholar
  31. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefPubMedGoogle Scholar
  32. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53:1283–1304CrossRefPubMedGoogle Scholar
  33. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant, Cell Environ 35:454–484CrossRefGoogle Scholar
  34. Ozbek N, Alyar S, Karacan N (2009) Experimental and theoretical studies on methanesulfonic acid 1-methylhydrazide: antimicrobial activities of its sulfonyl hydrazone derivatives. J Mol Struct 938:48–53CrossRefGoogle Scholar
  35. Ozdemir UO, Güvenc P, Sahin E, Hamurcu F (2009) Synthesis, characterization and antibacterial activity of new sulfonamide derivatives and their nickel(II), cobalt(II) complexes. Inorganica Chim Acta 362:2613–2618CrossRefGoogle Scholar
  36. Ozdemir UO, Arslan F, Hamurcu F (2010) Synthesis, characterization, antibacterial activities and carbonic anhydrase enzyme inhibitor effects of new arylsulfonylhydrazone and their Ni(II), Co(II) complexes. Spectrochim Acta, Part A 75:121–126CrossRefGoogle Scholar
  37. Ozmen UO, Olgun G (2008) Synthesis, characterization and antibacterial activity of new sulfonyl hydrazone derivatives and their nickel(II) complexes. Spectrochim Acta, Part A 70:641–645CrossRefGoogle Scholar
  38. Pospišil P (2009) Production of reactive oxygen species by photosystem II. BBA 1787:1151–1160PubMedGoogle Scholar
  39. Rao VM, Hale BA, Omrod DP (1995) Amelioation of ozone induced oxidative damage in wheat plants grown under high carbon dioxide. Plant Physiol 109:421–432PubMedPubMedCentralGoogle Scholar
  40. Rudenko NN, Ignatova LK, Ivanov BN (2007) Multiple sources of carbonic anhydrase activity in pea thylakoids: soluble and membrane-bound forms. Photosynth Res 91:81–89CrossRefPubMedGoogle Scholar
  41. Schiller H, Dau H (2000) Preparation protocols for high-activity Photosystem II membrane particles of green algae and higher plants, pH dependence of oxygen evolution and comparison of the S2-state multiline signal by X-band EPR spectroscopy. J Photochem Photobiol, B 55:138–144CrossRefGoogle Scholar
  42. Shitov AV, Pobeguts OV, Smolova TN, Allakhverdiev SI, Klimov VV (2009) Manganese-dependent carboanhydrase activity of photosystem II proteins. Biochemistry (Moscow) 74:509–517CrossRefGoogle Scholar
  43. Shitov AV, Zharmukhamedov SK, Shutova TV, Allakhverdiev SI, Samuelsson G, Klimov VV (2011) A carbonic anhydrase inhibitor induces bicarbonate-reversible suppression. J Photochem Photobiol, B 104:366–371CrossRefGoogle Scholar
  44. Shutova T, Kenneweg H, Buchta J, Nikitina J, Terentyev V, Chernyshov S, Andersson S, Allakhverdiev SI, Klimov VV, Dau H, Junge W, Samuelsson G (2008) The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal. EMBO J 5:782–791CrossRefGoogle Scholar
  45. Stemler A (1986) Carbonic anhydrase associated with thylakoids and photosystem II particles from maize. BBA (Bioenergetics) 850:97–107CrossRefGoogle Scholar
  46. Supuran CT, Scozzafava A, Casini A (2003) Carbonic anhydrase inhibitors. Med Res Rev 23:146–189CrossRefPubMedGoogle Scholar
  47. Trebst A, Draber W (1979) Structure activity correlations of recent herbicides in photosynthetic reactions. In: Greissbuehler H (ed) Advances in pesticide science, synthesis of pesticides, chemical structure and biological activity, natural products with biological activity. Pergamon Press, Oxford and New York, Part 2 pp 223–234Google Scholar
  48. Tunc T, Karacan MS, Ertabaklar H, Sarı M, Karacan N, Büyükgüngör O (2015a) Antimony(III) complexes with 2-amino-4,6-dimethoxypyrimidines: synthesis, characterization and biological evaluation. J Photochem Photobiol, B 153:206–214CrossRefGoogle Scholar
  49. Tunc T, Koc Y, Acık L, Karacan MS, Karacan N (2015b) DNA cleavage, antimicrobial studies and a DFT-based QSAR study of new antimony(III) complexes as glutathione reductase inhibitor. Spectrochim Acta Mol Biomol Spectrosc 136:1418–1427CrossRefGoogle Scholar
  50. Vivancos PD, Dong Y, Ziegler K, Markovic J, Pallardo FV, Pellny TK, Verrier PJ, Foyer CH (2010) Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defense shield. Plant J 64:825–838CrossRefPubMedGoogle Scholar
  51. Wilbur KM, Anderson NG (1948) Electrometric and colorimetric determination of carbonic anhydrase. Biol Chem 176:147–154Google Scholar
  52. Wyllie S, Fairlamb AH (2006) Differential toxicity of antimonial compounds and their effects on glutathione homeostasis in a human leukaemia monocyte cell line. Biochem Pharmacol 1:257–267CrossRefGoogle Scholar
  53. Zhang DY, Pan XL, Mu GJ, Wang JL (2010) Toxic effects of antimony on photosystem II of Synechocystis sp. as probed by in vivo chlorophyll fluorescence. J Appl Phycol 22:479–488CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Mehmet Sayım Karacan
    • 1
  • Margarita V. Rodionova
    • 2
  • Turgay Tunç
    • 3
  • Kübra Begüm Venedik
    • 1
  • Serhat Mamaş
    • 1
  • Alexandr V. Shitov
    • 4
  • Sergei K. Zharmukhamedov
    • 4
  • Vyacheslav V. Klimov
    • 4
  • Nurcan Karacan
    • 1
  • Suleyman I. Allakhverdiev
    • 2
    • 4
    • 5
  1. 1.Department of Chemistry, Science FacultyGazi UniversityTeknikokullar, AnkaraTurkey
  2. 2.Controlled Photobiosynthesis Laboratory, Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  3. 3.Department of Chemistry and Process Engineering, Engineering and Architecture FacultyAhi Evran UniversityKırşehirTurkey
  4. 4.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchinoRussia
  5. 5.Department of Plant Physiology, Faculty of BiologyM.V. Lomonosov Moscow State UniversityMoscowRussia

Personalised recommendations