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Coordination chemistry mimics of nuclease-activity in the hydrolytic cleavage of phosphodiester bond

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Chinese Science Bulletin

Abstract

In vivo, there occurs the synthesis and degradation of the nucleic acids, involving the formation and cleavage of phosphodiester bond. The cleavage modes of phosphodiester bond can be divided into two types, oxidative and hydrolytic, only the hydrolytic products are sticky and connectable, allowing to be religated by ligases. In recent years, great progresses have been made in chemical mimics in the hydrolytic cleavage of phosphodiester bond. Among the found metal complexes with the activity of nucleic acid cleavage, there are mononuclear and dinuclear metal complexes, the adopted metal ions including transitional and lanthanide metal ions. However, the reaction rates are still several orders less than those of the natural enzymes. It should be a prosperous and expedient direction to mimic the hydrolytic cleavage of phosphodiester bond by taking the advantages of dinuclear metal complexes.

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References

  1. Wolfenden, R., Ridgway, C., Young, G., Spontaneous hydrolysis of ionized phosphate monoesters and diesters and the proficiencies of phosphatases and phosphodiesterases as catalysts, J. Am. Chem. Soc., 1998, 120: 833–834.

    Article  Google Scholar 

  2. Williams, N. H., Takasaki, B., Chin, J., Structure and nuclease activity of simple dinuclear metal complexes: Quantitative dissection of the role of metal ions, Acc. Chem. Res., 1999, 32: 485–493.

    Article  Google Scholar 

  3. Westheimer, F. H., Why nature chose phosphates, Science, 1987, 235: 1173–1178.

    Article  Google Scholar 

  4. Sigman, D. S., Mazumder, A., Perrin, D. M., Chemical nucleases, Chem. Rev., 1993, 93: 2295–2316.

    Article  Google Scholar 

  5. Chen, C. B., Sigman, D. S., Nuclease activity of 1, 10-phenanthroline-copper: sequence-specific targeting, Proc. Natl. Acad. Sci. USA, 1986, 83: 7147–7151.

    Article  Google Scholar 

  6. Mejia-Radillo, Y., Yatsmirsky, A. K., Complex formation and kinetics of phosphodiester cleavage in the hydrogen peroxide-lanthanide(III) system, Inorg. Chim. Acta, 2003, 351: 97–106.

    Article  Google Scholar 

  7. Dhar, S., Chakravarty, A. R., Efficient visible light induced nuclease activity of a ternary mono-1, 10-phenanthroline copper(II) complex containing 2-(methylthio) ethylsalicyladimine, Inorg. Chem., 2003, 42(8): 2483–2485.

    Article  Google Scholar 

  8. Moser, H. E., Dervan, P. B., Sequence-specific cleavage of double-helical DNA by triple helix formation, Science, 1987, 238: 645–650.

    Article  Google Scholar 

  9. Gonzalez-Alvarez, M., Alzuet, G., Castineiras, A., Oxidative cleavage of DNA by a new ferromagnetic linear trinuclear copper(II) complex in the presence of H2O2/sodium ascorbate, Inorg. Chem., 2003, 42(9): 2992–2998.

    Article  Google Scholar 

  10. Sigman, D. S., Chen, C. B., Gorin, M. B., Sequence-specific scission of DNA by RNAs linked to a chemical nuclease, Nature, 1993, 363: 474–475.

    Article  Google Scholar 

  11. Pendergrast, P. S., Ebright, Y. W., Ebright, R. H., High-specifity DNA cleavage agent: Design and application to kilobase and megabase DNA substrates, Science, 1994, 265: 959–962.

    Article  Google Scholar 

  12. Sitlani, A., Barton, J. K., Sequence-specific recognition of DNA by phenanthrenequinone diimne complexes of rhodium(III): importance of steric and van der Waals interaction, Bochemistry, 1994, 33: 12100–12108.

    Article  Google Scholar 

  13. Mack, D. P., Dervan, P. B., Nickel-mediated squence-specific oxidative cleavage of DNA by a designed metalloprotein, J. Am. Chem. Soc., 1990, 112: 4604–4606.

    Article  Google Scholar 

  14. Roelfes, G., Banum, M. E., Que, L. Jr., Efficient DNA cleavage with an iron complex without added reductant, J. Am. Chem. Soc., 2000, 122: 11517–11518.

    Article  Google Scholar 

  15. Komiyama, M., Takeda, N., Shigekawa, H., Hydrolysis of DNA and RNA by lanthanide ions: mechanism studies leading to new applications, Chem. Commu., 1999: 1443–1451.

  16. Takeda, N., Shibata, M., Tajjima, N. et al., Kinetic and theoretical studies on the mechanism of alkaline hydrolysis of DNA, J. Org. Chem., 2000, 65: 4391–4396.

    Article  Google Scholar 

  17. Lahiri, S. D., Zhang, F. F., Dunaway-Mariano, D. et al., The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction, Science, 2003, 299: 2067–2071.

    Article  Google Scholar 

  18. Iranzo, O., Kovalecsky, A. Y., Morow, J. R. et al., Physical and kinetic analysis of the cooperative role of metal ions in catalysis of phosphodiester cleavage by a dinuclear Zn(II) complex, J. Am. Chem. Soc., 2003, 125: 1988–1993.

    Article  Google Scholar 

  19. Chapman, W. H. Jr., Breslow, R., Selective hydrolysis of phosphate esters, nitrophenyl phosphates and UpU by dimeric zinc complexes depends on the spacer length, J. Am. Chem. Soc., 1995, 117: 5462–5469.

    Article  Google Scholar 

  20. Tsubouchi, A., Bruice, C., Phosphonate ester hydrolysis catalyzed by two lanthanum ions, J. Am. Chem. Soc., 1995, 117: 7399–7411.

    Article  Google Scholar 

  21. Jurek, P. E., Martell, A. E., Dinuclear lanthanide complex catalyzes the hydrolysis of a phosphate diester with unprecedented speed, Chem. Commun., 1999: 1609–1610.

  22. Branum, M. E., Tipton, A. K., Que, L. Jr., Double-strand hydrolysis of plasmid DNA by dicerium complexes at 37°C, J. Am. Chem. Soc., 2001, 123: 1898–1904.

    Article  Google Scholar 

  23. Ren, R., Yang, P., Zheng, W. et al., A simple copper(II)-L-histidine system for efficient hydrolytic cleavage of DNA, Inorg. Chem., 2000, 39: 5454–5463.

    Article  Google Scholar 

  24. Zhou, C. Q., Gao, F., Li, S. E. et al., Synthesis and characterization of bieuropium complex coordinating Hbbimp, and its hydrolytic kinetic research for cleaving an activated phosphate diester BDNPP, J. Chinese Rare Earth Society, 2003, 21(5): 499–503.

    Google Scholar 

  25. Yang, P., Zhou, C. Q., Li, S. E. et al., Synthesis, characterization and crystal structure of binuclear nickel(II) complex [Ni2(bbimp)(CH3CH3OH)2Cl2]Cl · 4H2O, Chin. J. Inorg. Chem., 2003, 19(4): 415–418.

    Google Scholar 

  26. Yang, P., Zhou, C. Q., Synthesis and characterization of two new rare-earth complexes and their research for cleaving an activated phosphate diester BDNPP and DNA, Acta Chimica Sinica, 2003, 61(9): 1455–1460.

    Google Scholar 

  27. Lu, L. P., Zhu, M. L., Yang, P., Crystal structure and nuclease activity of mono(1, 10-phenanthroline) copper complex, J. Inorg. Biochem., 2003, 95(1): 31–36.

    Article  Google Scholar 

  28. Yang, P., Guo, M. L., DNA interact with metal ions and their complexes, J. Inorg. Biochem., 2001, 86(1): 115.

    Google Scholar 

  29. Song, Y. F., Yang, P., Synthesis, DNA scission chemistry, and an investigation of the reactive oxygen species of two 2,6-dimethoxyhydroquinone-3-mercaptoacetic acid-peptide conjugates, Austr. J. Chem., 2001, 54(4): 253–259.

    Article  Google Scholar 

  30. Yang, P., Song, A. X., Fan, X. Y., Mechanism of cleaving DNA through hydrolysis of a novel complex of Mg containing dien ligand, Chin. Chem. Lett., 2000, 11(1): 35–36.

    Google Scholar 

  31. Screedhara, A., Freed, J. D., Cowan, J. A., Efficient inorganic deoxyribonucleases greater than 50-milion-fold rate enhancement in enzyme-like DNA cleavage, J. Am. Chem. Soc., 2000, 122: 8814–8824.

    Article  Google Scholar 

  32. Bencini, A., Berni, E., Bianchi, A. et al., Proton and Cu(II) binding to tren-based tris-macrocycles, Affinity towards nucleic acids and nuclease activity, Dalton Trans., 2003: 793–800.

  33. Abe, K., Matsufuji, K., Ohba, M. et al., Site specificity of metal ions in heterodinuclear complexes derived from an “end-off” compartmental ligand, Inorg. Chem., 2002, 41(17): 4461–4467.

    Article  Google Scholar 

  34. Basile, L. A., Barton, J. K., Design of a double-stranded DNA cleavage agent with two polyamine metal-binding arms: Ru(DIP)2macron2, J. Am. Chem. Soc., 1987, 109: 7548–7550.

    Article  Google Scholar 

  35. Basile, L. A., Raphael, A. L., Barton, J. K., Metal-activated hydrolytic cleavage of DNA, J. Am. Chem. Soc., 1987, 109: 7550–7551.

    Article  Google Scholar 

  36. Schnaith, L. M. T., Hanson, R. S., Que, L. Jr., Double-stranded cleavage of pBR322 by a diiron complex via a “hydrolitic” mechanism, Proc. Natl. Acad. Sci. USA, 1994, 91: 569–573.

    Article  Google Scholar 

  37. Schneider, H. J., Rammo, J., Hettich, R., Catalysis of hydrolysis of phosphoric acid diesters by lanthanide ions and influence of ligands, Angew. Chem. Int. Ed., 1993, 32: 1716–1719.

    Article  Google Scholar 

  38. Breslow, R., Zhang, B., Cleavage of phosphate esters by a cyclodextrin dimer catalyst that binds the substrates together with La3+ and hydrogen peroxide, J. Am. Chem. Soc., 1994, 116: 7893–7894.

    Article  Google Scholar 

  39. Yang, P., Ren, R., Guo, M. et al., Double-strand hydrolysis of DNA by a magnesium(II) complex with diethylenetriamine, J. Biol. Inorg. Chem., 2004, 9: 495–506.

    Article  Google Scholar 

  40. Takeda, N., Irisawa, M., Komiyama, M., Coopoeration of lanthanide ion and non-lanthanide ions for the hydrolysis of bis(4-nitrophenyl)phosphate, J. Chem. Soc. Chem. Commun., 1994: 2773–2774.

  41. Takasaki, B. K., Chin, J., La(III)-hydrogen-peroxide cooperativity in phosphate diester cleavage: a mechanistic study, J. Am. Chem. Soc., 1995, 117: 8582–8585.

    Article  Google Scholar 

  42. Oh, S. J., Song, K. H., Park, J. W., Catalytic hydrolysis of phosphate monoesters by lanthanide(III) crytate(2.2.1) complexes, J. Chem. Soc. Chem. Commun., 1995: 575–576.

  43. Welch, J. T., Sirish, M., Lindstorm, K. M. et al., De novo nucleases based on HTH and EF-Hand chimeras, Inorg. Chem., 2001, 40: 1982–1984.

    Article  Google Scholar 

  44. Tagle, P. G., Yatsmirsky, A. K., Phosphodiester hydrolysis by lanthanide complexes of bis-tris propane, Inog. Chem., 2001, 40: 3786–3796.

    Article  Google Scholar 

  45. Magda, D., Miller, R. A., Sessler, J. L. et al., Site-specific hydrolysis of RNA by europium(III) texaphyrin conjugated to a synthetic oligodeoxyribonucleotide, J. Am. Chem. Soc., 1994, 116: 7439–7440.

    Article  Google Scholar 

  46. Matsumura, K., Endo, M., Komiyama, M., Lanthanide complex-oligo-DNA hybrid for sequence-selective hydrolysis of RNA, J. Chem. Soc. Chem. Commun., 1994: 2019–2020.

  47. Rammo, J., Hettich, R., Roigk, A. et al., Catalysis of DNA cleavage by Lanthanide complexes with nucleophilic or intercalating ligands and their kinetic characterization, Chem. Commun., 1996: 105–107.

  48. Sumaoka, J., Igawa, T., Furuki, K. et al., Homogeneous Ce(IV) complexes for efficient hydrolysis of plasmid DNA, Chem. Lett., 2000: 56–57.

  49. Hettich, R., Schneider, H. -J. J., Evidence for hydrolytic DNA cleavage by lanthanide(III) and cobalt(III) derivatives, Chem. Soc. Perkin. Trans. II., 1997: 2069–2072.

  50. Zhu, B., Li, X. M., Zhao, D. Q. et al., Hydrolytic cleavage of adenosine-3′-monophosphare and guanosine-5′-monophosphate by lanthanides, Acta Chimica Sinica, 1998, 56: 47–51.

    Google Scholar 

  51. Zhu, B., Li, X. M., Zhao, D. Q. et al., Hydrolysis of adenosine monophosphare and guanosine monophosphate by lanthanides, Acta Chimica Sinica, 1996, 54: 1089–1093.

    Google Scholar 

  52. Shen, H. B., Xia, J. F., Yang, H. F. et al., Hydrolysis of oligodeoxynucleotide phosphodiester linkages, Sci. China, Ser. B, 2001, 44(2): 169–174.

    Article  Google Scholar 

  53. Wang, C., Choudhary, S., Vink, C. B. et al., Harnessing thorium (IV) as a catalyst: RNA and phosphate diester cleavage by a thorium(IV) macrocyclic complex, Chem. Commun., 2000: 2509–2510.

  54. Moss, R. A., Bracken, K., Zhang, J., Actinide (uranyl) hydrolysis of phosphodiesters, Chem. Commun., 1997: 563–564.

  55. Hegg, E. L., Deal, K. A., Kiessling, L. L. et al., Hydrolysis of double-stranded and single-stranded RNA in hairpin structure by one copper(II) macrocycle Cu([9]ane N3)Cl2, Inorg. Chem., 1997, 36: 1715–1718.

    Article  Google Scholar 

  56. Hegg, E. L., Burstyn, J. N., Copper(II) macrocycles cleave single-stranded and double-stranded DNA under aerobic and anaerobic conditions, Inorg. Chem., 1996, 35: 7474–7481.

    Article  Google Scholar 

  57. Itoh, T., Hisada, H., Sumiya, T. et al., Hydrolytic cleavage of DNA by a novel copper(II) complex with cis-cis-1,3,5-triaminocyclohexane, Chem. Commun., 1997: 677–678.

  58. Sissi, C., Rossi, P., Felluga, F. et al., Dinucear Zn2+ complexes of synthetic heptapeptides as artificial nucleases, J. Am. Chem. Soc., 2001, 123: 3169–3170.

    Article  Google Scholar 

  59. Worm, K., Chu, F., Matsumoto, K. et al., Preorganized bis-zinc phosphodiester cleavage catalysts possessing natural ligands: a lesson pertinent to bimetallic artificial enzymes, Chem. Eur. J., 2003, 9: 741–747.

    Article  Google Scholar 

  60. Bernard, E., Moneta, W., Laugier, J. et al., A mixed-valent, unsymmetrical FeIIFeIII complex with a terminal phonolato ligand as a model for the active site of purple acid phosphatases, Angew. Chem. Int. Ed., 1994, 33: 887–889.

    Article  Google Scholar 

  61. Seo, J. S., Hynes, R. C., Chin, J., Structure and reactivity of dinuclear cobalt(III) complexes with peroxide and phosphate diester analogues bridging the metal ions, J. Am. Chem. Soc., 1998, 120: 9943–9944.

    Article  Google Scholar 

  62. Dixon, N. E., Geue, R. J., Lambert, J. N. et al., DNA hydrolysis by stable metal complexes, Chem. Commun., 1996: 1287–1288.

  63. Yamaguchi, K., Akagi, F., Fujinami, S. et al., Hydrolysis of phophodiester with hydroxoor carboxylate-bridged dinuclear Ni(II) and Cu(II) complexes, Chem. Commun., 2001: 375–376.

  64. Kong, D., Reibenspies, J., Mao, J. -G. et al., Novel 30-membered octaazamacrocyclic ligand: synthesis, characterization, thermodynamics stabilities and DNA cleavage activity of homodinuclear copper and nickel complexes, Inorg. Chim. Acta, 2003, 342: 158–170.

    Article  Google Scholar 

  65. Belle, C., Gautier-Luneau, I., Karmazin, L. et al., Regio-directed synthesis of a ZnIIFeIII complex from unsymmetrical ligand and its relevance to purple acid phosphatases, Eur. J. Inorg. Chem., 2002: 3087–3090.

  66. Lanznaster, M., Neves, A., Bortoluzzi, A. J. et al., New FeIIIZnII complex containing a single terminal Fe-O phenolate bond as a structure and functional model for the active site of red kidney bean purple acid phosphatase, Inorg. Chem., 2002, 41: 5641–5643.

    Article  Google Scholar 

  67. Ott, R., Kramer, R., Rapid phosphodiester hydrolysis by zirconium(IV), Angew. Chem. Int. Ed., 1998, 37: 1957–1960.

    Article  Google Scholar 

  68. Stulz, E., Leumann, C., X-ray structure and solvolytic activity towards phosphate diesters of a zirconium(IV) complex, Chem. Commun., 1999: 239–240.

  69. Otieno, T., Bond, M. R., Mokry, L. M. et al., Plasmid DNA cleavage by oxo-bridged vanadium(III) dimer without added co-oxidants or reductants, Chem. Commun., 1996: 37–38.

  70. Young, M. J., Chin, J., Dinuclear copper(II) complex that hydrolyzes RNA, J. Am. Chem. Soc., 1995, 117: 10577–10584.

    Article  Google Scholar 

  71. Yashiro, M., Ishikubo, K., Komiyama, M., Efficient and unique cooperation of three zinc(II) ions in the hydrolysis of diribonucleotides by a trinuclear zinc(II) complex, Chem. Commun., 1997: 83–84.

  72. Fritsky, I. O., Ott, R., Kramer, R., Allosteric regulation of artificial phosphoesterase activity by metal ions, Angew. Chem. Int. Ed., 2000, 18: 3255–3258.

    Article  Google Scholar 

  73. Korupoju, S. R., Mangayakarasi, N., Zaxharias, P. S. et al., Synthesis, structure and DNA cleavage activity of new trinuclear Zn3 and Zn2Cu complexes of a chiral macrocycle: structure correlation with the active center of P1 nuclease, Inorg. Chem., 2002, 41: 4099–4101.

    Article  Google Scholar 

  74. Wahnon, D., Lebuis, A. M., Chin, J., Hydrolysis of a phosphate diester doubly coordinated to a dinuclear cobalt(III) complex: a novel mechanism, Angew. Chem. Int. Ed., 1995, 34: 2412–2414.

    Article  Google Scholar 

  75. Williams, N. H., William, C., Chin, J., Reactivity of phosphate diester doubly coordinated to a dinuclear cobalt(III) complex: dependence of the reactivity on the basicity of the leaving group, J. Am. Chem. Soc., 1998, 120: 8079–8087.

    Article  Google Scholar 

  76. Matsuda, S., Ishikubo, A., Komiyama, M., Conjugates of a dinuclear zinc(II) complex and DNA oligomers as novel sequence-selective artificial ribonucleases, Angew. Chem. Int. Ed., 1998, 37: 3284–3286.

    Article  Google Scholar 

  77. Ragunathan, K. G., Schneider, H. J., Binuclear lanthanide complexes as catalyst for the hydrolysis of bis-(p-nitrophenyl)-phosphate and double-stranded DNA, Angew. Chem. Int. Ed., 1996, 35: 1219–1221.

    Article  Google Scholar 

  78. Myers, A. G., Kort, M. E., Hammond, M. A., Comparison of DNA cleavage by neocarsinostatin chromophore and its aglycon: evaluating the role of the carbohydrate residue, J. Am. Chem. Soc., 1997, 119: 2965–2972.

    Article  Google Scholar 

  79. Kovacic, R. T., Welch, J. T., Franklin, S. J., Sequence-selective DNA cleavage by a chimeric metallopeptide, J. Am. Chem. Soc., 2003, 125: 6656–6662.

    Article  Google Scholar 

  80. Berg, T., Simeonov, A., Janda, K. D., A combined parallel synthesis and screening of macrocyclic lanthanide complexes for the cleavage of phosphodiand tri-esters and double-stranded DNA, J. Combinat. Chem., 1999, 1: 96–100.

    Article  Google Scholar 

  81. Berkessel, A., Herault, D. A., Discovery of peptide-zirconium complexes that mediate phosphate hydrolysis by batch screening of a combinatorial undecapeptide library, Angew. Chem. Int. Ed., 1999, 38(1/2): 102–105.

    Article  Google Scholar 

  82. Wilcox, D. E., Binuclear metallohydrolases, Chem. Rev., 1996, 96: 2435–2458.

    Article  Google Scholar 

  83. Sam, M. D., Perona, J. J., Catalytic role of divalent metal ions in phosphoryl transfer by rcoRV, Biochemistry, 1999, 38: 6576–6586.

    Article  Google Scholar 

  84. Xu, R. X., Hassel, A. M., Vanderwall, D. et al., Atomic structure of PDE4: insights into phosphodiesterase mechanism and specificity, Science, 2000, 288: 1822–1825.

    Article  Google Scholar 

  85. Zhan, C. -G., Fang, Z., First computational evidence for a catalytic bridging hydroxide ion in a phosphodiesterase active site, J. Am. Chem. Soc., 2001, 123: 2835–2838.

    Article  Google Scholar 

  86. Jedrzejas, M. J., Setlow, P., Comparison of the binuclear metalloenzymes, Chem. Rev., 2001, 101: 607–618.

    Article  Google Scholar 

  87. William, N. H., Chin, J., Metal-ion catalyzed phosphate diester transesterfication: quantifying double Lewisacid activation, J. Chem. Soc. Chem. Commun., 1996: 131–136.

  88. Hendry, P., Sargeson, A. M., Base hydrolysis of the penta-ammine (trimethyl phosphate)iridium ion, J. Chem. Soc. Chem. Commun., 1984: 164–167.

  89. Hendry, P., Sargeson, A. M., Reactivity of coordinated phosphate esters, Inorg. Chem., 1990, 29: 92–98.

    Article  Google Scholar 

  90. Ausubel, F. M., Brent, R., Kingston, R. E. et al., Short Protocols in Molecular Biology, 3rd ed. (Chinese Ed.) (Translated by Yan, Z. Y., Wang, H. L.), Beijing: Science Press, 1999, 185–191.

    Google Scholar 

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  1. Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Institute of Molecular Science, Shanxi University, 030006, Taiyuan, China

    Fei Gao, Caixia Yin & Pin Yang

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  1. Fei Gao
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  2. Caixia Yin
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Gao, F., Yin, C. & Yang, P. Coordination chemistry mimics of nuclease-activity in the hydrolytic cleavage of phosphodiester bond. Chin. Sci. Bull. 49, 1667–1680 (2004). https://doi.org/10.1007/BF03184297

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