Abstract
We successfully synthesized the first hemin-montmorillonite bio-conjugate with an amino acid residue to mimic natural peroxidase enzyme. Histamine was intercalated in montmorillonite by cation exchange, then a hemin molecule was loaded onto the histamine-montmorillonite with an adsorption capacity of 7.0 mg g−1. The hemin-histamine-montmorillonite conjugate shows high peroxidase activity as indicated by the oxidation of guaiacol, which is attributed to the activation of hemin by Fe-N complex formation between the imidazole group in histamine and the iron ion in the hemin molecule. Temperature-dependent peroxidase activity for this synthesized biomimetic material indicates that raising the reaction temperature could significantly enhance the activity of the conjugate. The biomimetic catalyst has good reusability; nearly 100% activity can be retained after three cycles. Because montmorillonite clay is widely distributed in the environment, this material offers great potential for in situ and ex situ remediation of many organic contaminants in surface/subsurface soils.
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Denisov I, Makris T, Sligar S, Schlichting I. Structure and chemistry of cytochrome P450. Chem Rev, 2005, 105: 2253–2277
Costas M, Mehn MP, Jensen MP, Que L Jr. Dioxygen activation at mononuclear nonheme iron active sites: enzymes, models, and intermediates. Chem Rev, 2004, 104: 939–986
Meunier B, de Visser S, Shaik S. Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem Rev, 2004, 104: 3947–3980
Nam W. High-valent iron(IV)-oxo complexes of heme and non-heme ligands in oxygenation reactions. Acc Chem Res, 2007, 40: 522–531
Roth J, Cramer C. Direct examination of H2O2 activation by a heme peroxidase. J Am Chem Soc, 2008, 130: 7802–7803
Shintaku M, Matsuura K, Yoshioka S, Takahashi S, Ishimori K, Morishima I. Absence of a detectable intermediate in the compound I formation of horseradish peroxidase at ambient temperature. J Biol Chem, 2005, 280: 40934–40938
Kazunga C, Aitken M, Gold A. Primary product of the horseradish peroxidase-catalyzed oxidation of pentachlorophenol. Environ Sci Technol, 1999, 33: 1408–1412
Samokyszyn V, Freeman J, Maddipati K, Lloyd R. Peroxidase-catalyzed oxidation of pentachlorophenol. Chem Res Toxicol, 1995, 8: 349–355
Dai J, Wright M. Manderville R. An oxygen-bonded C8-deoxyguanosine nucleoside adduct of pentachlorophenol by peroxidase activation: evidence for ambident C8 reactivity by phenoxyl radicals. Chem Res Toxicol, 2003, 16: 817–821
Kazunga C, Aitken M, Gold A. Primary product of the horseradish peroxidase-catalyzed oxidation of pentachlorophenol. Environ Sci Technol, 1999, 33: 1408–1412
Samokyszyn V, Freeman J, Maddipati K, Lloyd R. Peroxidase-catalyzed oxidation of pentachlorophenol. Chem Res Toxicol, 1995, 8: 349–355
Dai J, Wright M. Manderville R. An oxygen-bonded C8-deoxyguanosine nucleoside adduct of pentachlorophenol by peroxidase activation: evidence for ambident C8 reactivity by phenoxyl radicals. Chem Res Toxicol, 2003, 16: 817–821
Niu J, Xu J, Dai Y, Xu J, Guo H, Sun K, Liu R. Immobilization of horseradish peroxidase by electrospun fibrous membranes for adsorption and degradation of pentachlorophenol in water. J Hazad Mater, 2013, 246-247: 119–125
Colosi LM, Pinto RA, Huang QG, Weber WJ Jr. Peroxidase-mediated degradation of perfluorooctanoic acid. Environ Toxicol Chem, 2009, 28: 264–271
Kumar C, Chaudhari A. High temperature peroxidase activities of HRP and hemoglobin in the galleries of layered Zr(IV)phosphate. Chem Commun, 2002, 20: 2382–2383
Lin Y, Ren J, Qu X. Catalytically active nanomaterials: a promising candidate for artificial enzymes. Acc Chem Res, 2014, 47: 1097–1105
Wang X, Chrzanowski M, Yuan D, Sweeting B, Ma S. Covalent heme framework as a highly active heterogeneous biomimetic oxidation catalyst. Chem Mater, 2014, 26: 1639–1644
Lu C, Qi X, Orbach R, Yang H, Mironi-Harpaz I, Seliktar D, Willner I. Switchable catalytic acrylamide hydrogels cross-linked by hemin/ G-quadruplexes. Nano Lett, 2013, 13:1298–1302
Zhu L, Li C, Zhu Z, Liu D, Zou Y, Wang C, Fu H, Yang CY. In vitro selection of highly efficient G-quadruplex-based DNA enzymes. Anal Chem, 2012, 84: 8383–8390
Kotchey G, Hasan S, Kapralov A, Ha S, Kim K, Shvedova A, Kagan V, Star A. A natural vanishing act: the enzyme-catalyzed degradation of carbon nanomaterials. Acc Chem Res, 2012, 45: 1770–1781
Huang Y, Ma W, Li J, Cheng M. Zhao J. A novel β-CD-hemin complex photocatalyst for efficient degradation of organic pollutants at neutral pHs under visible irradiation. J Phys Chem B, 2003, 107: 9409–9419
Jiang Z, Liu X, Bu J. Removal of 2,4,6-trichlorophenol by iron and manganese oxides/granular activated carbon with H2O2. Adv Mater Res, 2010, 154-155: 28–33
Vinita M, Praveena Juliya Dorathi R, Palanivelu K. Degradation of 2,4,6-trichlorophenol by photo Fenton’s like method using nano heterogeneous catalytic ferric ion. Sol Energy, 2010, 84: 1613–1618
Díaz-Díaz G, Celis-García M, Carmen Blanco-López M, Jesús Lobo-Castañón M, Miranda-Ordieres A, Tuñón-Blanco P. Heterogeneous catalytic 2, 4, 6-trichlorophenol degradation at hemin-acrylic copolymer. Appl Catal B: Environ, 2010, 96: 51–56
Hu P, Han L, Dong S. A facile one-pot method to synthesize a polypyrrole/hemin nanocomposite and its application in biosensor, dye removal, and photothermal therapy. ACS Appl Mater Inter, 2014, 6: 500–506
Wang Q, Yang Z, Zhang X, Xiao X, Chang C, Xu B. A supramolecular-hydrogel-encapsulated hemin as an artificial enzyme to mimic peroxidase. Angew Chem Int Ed, 2007, 46: 4285–4289
Gharibi H, Moosavi-Movahedi Z, Javadian S, Nazari K, Moosavi-Movahedi A. Vesicular mixed gemini-SDS-hemin-imidazole complex as a peroxidase-like nano artificial enzyme. J Phys Chem B, 2011, 115: 4671–4679
Xue T, Jiang S, Qu Y, Su Q, Cheng R, Dubin S, Chiu C, Kaner R, Huang Y, Duan X. Graphene-supported hemin as a highly active biomimetic oxidation catalyst. Angew Chem Int Ed, 2012, 51: 3822–3825
Bhattacharyya D, Banerjee R. Chemical and kinetic evidence for an essential histidine in horseradish peroxidase for iodide oxidation. J Biol Chem, 1992, 267: 9800–9804
Bhattacharyya D, Bandyopadhyay U, Banerjee R. Chemical and kinetic evidence for an essential histidine residue in the electron transfer from aromatic donor to horseradish peroxidase compound I. J Biol Chem, 1993, 268: 22292–22298
Hartmann C, Montellano R. Baculovirus expression and characterization of catalytically active horseradish peroxidase. Biochem Biophys, 1992, 297: 61–72
Howes B, Rodriguez-Lopez J, Smith A, Smulevich G. Mutation of distal residues of horseradish peroxidase: influence on substrate binding and cavity properties. Biochem, 1997, 36: 1532–1543
La Mar G, Hernandez G, de Ropp J. Proton NMR investigation of the influence of interacting sites on the dynamics and thermodynamics of substrate and ligand binding to horseradish peroxidase. Biochem, 1992, 31: 9158–9168
Newmyer S, Ortiz de Montellano P. Horseradish peroxidase His-42 →Ala, His-42 →Val, and Phe-41→Ala mutants. Histidine catalysis and control of substrate access to the heme iron. J Biol Chem, 1995, 270: 19430–19438
Savenkova M, Newmyer S, Ortiz de Montellano P. Rescue of His-42 →Ala horseradish peroxidase by a Phe-41→His mutation engineering of a surrogate catalytic histidine. J Biol Chem, 1996, 271: 24598–24603
Uno T, Takeda A, Shimabayashi S. Effects of imidazoles and pH on the peroxidase activity of the hemin-hydrogen peroxide system. Inorg Chem, 1995, 34: 1599–1607
Veitch N, Smith A. Horseradish peroxidase. Adv Inorg Chem, 2001, 51: 107–162
Newmyer S, Sun J, Loehr T, Ortizde Montellano P. Rescue of the horseradish peroxidase His-170→Ala mutant activity by imidazole: importance of proximal ligand tethering. Biochem, 1996, 35: 12788–12795
Rodriguez-Lopez J, Smith A, Thorneley R. Effect of distal cavity mutations on the binding and activation of oxygen by ferrous horseradish peroxidase. J Biol Chem, 1997, 272: 389–395
Itoh T, Yamada T, Kodera Y, Matsushima A, Hiroto M, Sakurai K, Nishimura H, Inada Y. Hemin (Fe3+)-and Heme (Fe2+)-Smectite conjugates as a model of hemoprotein based on spectrophotometry. Bioconjuge Chem, 2001, 12: 3–6
Kurosawa M, Itoh T, Kodera Y, Matsushima A, Hiroto M, Nishimura H, Inada Y. Formation of a bioconjugate composed of hemin, smectite, and quaternary ammonium chloride that is soluble and active in hydrophobic media. Bioconjugate Chem, 2002, 13: 167–171
Arroyo L, Li H, Teppen B, Body S. A simple method for partial purification of reference clays. Clay Clay Mater, 2005, 53: 511–519
Vianelloab R, Mavri J. Microsolvation of the histamine monocation in aqueous solution: the effect on structure, hydrogen bonding ability and vibrational spectrum. New J Chem, 2012, 36: 954–962
Tapia O, Cárdenas R, Smeyers Y, Hernández-Laguna A, Hernández-Laguna A, Rández J, Rández F. Exploring the potential energy hypersurface of histamine monocation: tautomerism in gas phase. Int J Quantum Chem, 1990, 38: 727–740
Kulshrestha P, Giese RF Jr, Aga DS. Investigating the molecular interactions of oxytetracycline in clay and organic matter: insights on factors affecting its mobility in soil. Environ Sci Technol, 2004, 38: 4097–4105
Parida K, Varadwaj G, Sahu S, Sahoo P. Schiff base Pt(II) complex intercalated montmorillonite: a robust catalyst for hydrogenation of aromatic nitro compounds at room temperature. Ind Eng Chem Res, 2011, 50: 7849–7856
Collado J, Ramirez F. Vibrational spectra and assignments of histamine dication in the solid state and in solution. J Raman Spectrosc, 2000, 31: 925–931
Collado J, Ramirez F. Infrared and Raman spectra of histamine-NH4 and histamine-ND4 monohydrochlorides. J Raman Spectrosc, 1999, 30: 391–397
Travascio P, Li Y, Sen D. DNA-enhanced peroxidase activity of a DNA-aptamer-hemin complex. Chem Biol, 1998, 5: 505–517
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Zhang, L., Gu, C., Xiong, J. et al. Hemin-histamine-montmorillonite clay conjugate as a model biocatalyst to mimic natural peroxidase. Sci. China Chem. 58, 731–737 (2015). https://doi.org/10.1007/s11426-014-5196-6
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DOI: https://doi.org/10.1007/s11426-014-5196-6