Vanadium pp 95-125 | Cite as

Structure and Function of Vanadium Haloperoxidases

  • Ron WeverEmail author


Vanadium haloperoxidases contain the bare metal oxide vanadate as a prosthetic group and differ strongly from the heme peroxidases in substrate specificity and molecular properties. The substrates of these enzymes are limited to halides and sulfides, which in the presence of hydrogen peroxide are converted into hypohalous acids or sulfoxides, respectively. Several seaweeds contain iodo- and bromoperoxidases and their direct or indirect involvement in the production of the huge amounts of brominated, iodinated compounds and the formation of I2 in the marine environment will be reviewed. Vanadium chloroperoxidases occur in a group of common terrestrial fungi and are probably involved in the degradation of plant cell walls and breakdown of the leaf cuticle. The natural presence of high-molecular-weight chloro-aromatics in the environment is probably be due to the activity of these enzymes. Based upon several X-ray structures of the enzymes and detailed kinetics a molecular mechanism is proposed and discussed in detail. As will be shown the metal oxide in the active site binds hydrogen peroxide in a side-on fashion and acts as a Lewis acid allowing nucleophilic attack of an incoming halide and formation of HOX. The surprising evolutionary relationship between the bacterial and mammalian acid phosphatases that hydrolyze phosphate monoesters and the vanadium haloperoxidases will be shown.


Vanadium iodoperoxidases Vanadium bromoperoxidases Vanadium chloroperoxidase Steady-state kinetics X-ray structures Active site structures Mutants Sulfoxidation Acid phosphatases Halometobolites Biological importance Environmental significance Atmospheric chemistry 


  1. 1.
    Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms Butler. Science 281:207–210CrossRefGoogle Scholar
  2. 2.
    Lagerkvist BJ, Oskarsson A (2007) Vanadium. In: Nordberg GF, Fowler BA, Nordberg M, Friberg L (eds) Handbook on the toxicology of metals, 3rd edn. Academic, San Diego, pp 905–924CrossRefGoogle Scholar
  3. 3.
    Vilter H (1984) Peroxidases from phaeophyceae- a vanadium (V) dependent peroxidase from Ascophyllum nodosum. Phytochemistry 23:1387–1390CrossRefGoogle Scholar
  4. 4.
    Wever R, Plat H, DeBoer E (1985) Isolation procedure and some properties of the bromoperoxidase from the seaweed Ascophyllum nodosum. Biochim Biophys Acta 830:181–186CrossRefGoogle Scholar
  5. 5.
    De Boer E, van Kooy Y, Tromp MGM, Plat H, Wever R (1986) Bromoperoxidase from Ascophyllum nodosum: a novel class of enzymes containing vanadium as a prosthetic group? Biochim Biophys Acta 869:48–53CrossRefGoogle Scholar
  6. 6.
    De Boer E, Tromp MGM, Plat H, Krenn GE, Wever R (1986) Vanadium (V) as an essential element for haloperoxidase activity in marine brown algae: purification and characterization of a vanadium (V)-containing bromoperoxidase from Laminaria saccharina. Biochim Biophys Acta 872:104–115CrossRefGoogle Scholar
  7. 7.
    VanSchijndel JWPM, Vollenbroek EGM, Wever R (1993) The chloroperoxidase from the fungus Curvularia inaequalis; a novel vanadium enzyme. Biochim Biophys Acta 1161: 249–256CrossRefGoogle Scholar
  8. 8.
    Vollenbroek EGM, Simons LH, van Schijndel J, Barnett P, Balzar M, Dekker H, van der Linden C, Wever R (1995) Vanadium chloroperoxidases occur widely in nature. Biochem Soc Trans 23:267–271Google Scholar
  9. 9.
    De Boer E, Boon K, Wever R (1988) Electron paramagnetic resonance studies on conformational states and metal ion exchange properties of vanadium bromoperoxidase. Biochemistry 27:1629–1635CrossRefGoogle Scholar
  10. 10.
    Colin C, Leblanc C, Wagner E, Delage L, Leize-Wagner E, van Dorsselaer A, Kloareg B, Potin P (2003) The brown algal kelp Laminaria digitata features distinct bromoperoxidase and iodoperoxidase activities. J Biol Chem 278:23545–23552CrossRefGoogle Scholar
  11. 11.
    Wever R, Hemrika W (2001) Vanadium haloperoxidases. In: Messerschmidt A, Hubert R, Poulos T, Wieghardt K (eds) Handbook of metalloproteins. Wiley, Chichester, pp 1417–1428Google Scholar
  12. 12.
    Suthiphongchai T, Boonsiri P, Panijpan B (2008) Vanadium-dependent bromoperoxidases from Gracilaria algae. J Appl Phycol 20:271–278CrossRefGoogle Scholar
  13. 13.
    Wever R, Tromp MGM, Van Schijndel JWPM, Vollenbroek E (1993) Bromoperoxidases: their role in the formation of HOBr and bromoform by seaweeds. In: Oremland RD (ed) Biogeochemistry of global change. Chapman and Hall, New York, pp 811–824CrossRefGoogle Scholar
  14. 14.
    Moore RM, Webb M, Tokarczyk R, Wever R (1996) Bromoperoxidase and iodoperoxidase enzymes and production of halogenated methanes in marine diatom culture. J Geophys Res 101:20899–20908CrossRefGoogle Scholar
  15. 15.
    Ohshiro T, Nakano S, Takahashi Y, Suzuki M, Izumi Y (1999) Occurrence of bromoperoxidase in the marine green macro-alga, Ulvella lens, and emission of volatile brominated methane by the enzyme. Phytochemistry 52:1211–1215CrossRefGoogle Scholar
  16. 16.
    Carpenter LJ, Liss PS (2000) On temperate sources of bromoform and other reactive organic bromine gases. J Geophys Res 105:20539–20547CrossRefGoogle Scholar
  17. 17.
    Simpson WR, von Glasow R, Riedel K, Anderson P, Ariya P, Bottenheim J, Burrows J, Carpenter LJ, Friess U, Goodsite ME, Heard D, Hutterli M, Jacobi HW, Kaleschke L, Neff B, Plane J, Platt U, Richter A, Roscoe H, Sander R, Shepson P, Sodeau J, Steffen A, Wagner T, Wolff E (2007) Halogens and their role in polar boundary-layer ozone depletion. Atmos Chem Phys 7:4375–4418CrossRefGoogle Scholar
  18. 18.
    Read KA, Mahajan AS, Carpenter LJ, Evans MJ, Faria BVE, Heard DE, Hopkins JR, Lee JD, Moller SJ, Lewis AC, Mendes L, McQuaid JB, Oetjen H, Saiz-Lopez A, Pilling MJ, Plane JMC (2008) Extensive halogen-mediated ozone destruction over the tropical Atlantic Ocean. Nature 453:1232–1235CrossRefGoogle Scholar
  19. 19.
    Itoh N, Shinya M (1994) Seasonal evolution of bromomethanes from coralline algae (Corallinaceae) and its effect on atmospheric chemistry. Mar Chem 45:95–103CrossRefGoogle Scholar
  20. 20.
    Dyrssen D, Fogelqvist E (1981) Bromoform concentrations of the Artic Ocean in the Svalbard area. Oceanol Acta 43:313–317Google Scholar
  21. 21.
    Krysell M (1999) Bromoform in the Nansen Basin in the Arctic Ocean. Mar Chem 33: 187–197CrossRefGoogle Scholar
  22. 22.
    Wever R, Tromp MGM, Krenn BE, Marjani A, van Tol M (1991) Brominating activity of the seaweed Ascophyllum nodosum – impact on the biosphere. Environ Sci Technol 25:446–449CrossRefGoogle Scholar
  23. 23.
    Almeida M, Filipe S, Humanes M, Maia MF, Melo R, Severino N, da Silva JAL, da Silva JJRF, Wever R (2001) Vanadium haloperoxidases from brown algae of the Laminariaceae family. Phytochemistry 57:633–642CrossRefGoogle Scholar
  24. 24.
    Krenn BE, Tromp MGM, Wever R (1989) The brown alga Ascophyllum nodosum contains 2 different vanadium bromoperoxidases. J Biol Chem 264:19287–19292Google Scholar
  25. 25.
    Almeida MG, Humanes M, Melo R, Silva JA, Frausto Da Silva JJR, Wever R (2000) Purification and characterisation of vanadium haloperoxidases from the brown alga Pelvetia canaliculata. Phytochemistry 54:5–11CrossRefGoogle Scholar
  26. 26.
    Borchardt SA, Allain EJ, Michels JJ, Stearns GW, Kelly RF, Mccoy WF (2001) Reaction of acetylated homoserine lactone signaling molecules with oxidized halogen antimicrobials. Appl Environ Microbiol 67:3174–3179CrossRefGoogle Scholar
  27. 27.
    Sauvageau C (1926) Sur quelques algues floridée renformant du brome a l’etat libre. Bull Stat Biol D’Arcachon 23:1–23Google Scholar
  28. 28.
    Mtolera MSP, Collen J, Pedersen M, Ekdahl A, Abrahamsson K, Semesi AK (1996) Stress-induced production of volatile halogenated organic compounds in Eucheuma denticulatum (Rhodophyta) caused by elevated pH and high light intensities. Eur J Phycol 31:89–95CrossRefGoogle Scholar
  29. 29.
    Bondu S, Cocquempot B, Deslandes E, Morin P (2008) Effects of salt and light stress on the release of volatile halogenated organic compounds by Solieria chordalis: a laboratory incubation study. Bot Mar 51:485–492CrossRefGoogle Scholar
  30. 30.
    Nightingale PD, Malin G, Liss PS (1995) Production of chloroform and other low- molecular weight halocarbons by some species of macro algae. Limnol Oceanogr 40:680–689CrossRefGoogle Scholar
  31. 31.
    Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress an signal transduction. Ann Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  32. 32.
    Hansen EH, Albertsen L, Schafer T, Johansen C, Frisvad JC, Molin S, Gram L (2003) Curvularia haloperoxidase: antimicrobial activity and potential application as a surface disinfectant. Appl Environ Microbiol 69:4611–4617CrossRefGoogle Scholar
  33. 33.
    Renirie R, Dewilde A, Pierlot C, Wever R, Hober D, Aubry J-M (2008) Bactericidal and virucidal activity of the alkalophilic P395D⁄L241V⁄T343A mutant of vanadium chloroperoxidase. J Appl Microbiol 105:264–270CrossRefGoogle Scholar
  34. 34.
    Theiler R, Cook JC, Hager LP, Siuda JF (1978) Halohydrocarbon synthesis by bromoperoxidase. Science 202:1094–1096CrossRefGoogle Scholar
  35. 35.
    Jaworske DA, Helz GR (1985) Rapid consumption of bromine oxidants in river and estuarine waters. Environ Sci Technol 19:1188–1191CrossRefGoogle Scholar
  36. 36.
    Leblanc C, Colin C, Cosse A, Delage L, La Barre S, Morin P, Fievet B, Voiseux C, Ambroise Y, Verhaeghe E, Amouroux D, Donard O, Tessier E, Potin P (2006) Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochemie 88:1773–1785CrossRefGoogle Scholar
  37. 37.
    Colin C, Leblanc C, Michel G, Wagner E, Leize-Wagner E, Dorsselaer V, Potin P (2005) Vanadium-dependent iodoperoxidases in Laminaria digitata, a novel biochemical function diverging from brown algal bromoperoxidases. J Biol Inorg Chem 10:156–166CrossRefGoogle Scholar
  38. 38.
    Palmer CJT, Anders L, Carpenter LJ, Küpper FC, McFiggans G (2005) Iodine and halocarbon response of Laminaria digitata to oxidative stress and links to atmospheric new particle production. Environ Chem 2:282–290CrossRefGoogle Scholar
  39. 39.
    Laturnus F, Svensson T, Wiencke C, Öberg G (2004) Ultraviolet radiation affects emission of ozone-depleting substances by marine macroalgae: results from a laboratory incubation study. Environ Sci Technol 38:6605–6609CrossRefGoogle Scholar
  40. 40.
    Dixneuf S, Ruth AA, Vaughan S, Varma RM, Orphal J (2009) The time dependence of molecular iodine emission from Laminaria digitata. Atmos Chem Phys 9:823–829CrossRefGoogle Scholar
  41. 41.
    Saiz-Lopez A, Plane JMC, McFiggans G, Williams PI, Ball SM, Bitter M, Jones RL, Hongwei C, Hoffmann T (2006) Modeling molecular iodine emissions in a coastal marine environment: the link to new particle formation. Atmos Chem Phys 6:883–895CrossRefGoogle Scholar
  42. 42.
    O’Dowd D, Jimenez JL, Bahreini R, Flagan RC, Seinfeld JH, Hämeri K, Pirjola L, Kulmala M, Jennings GS, Hoffmann T (2002) Marine aerosol formation from biogenic iodine emissions. Nature 417:632–636CrossRefGoogle Scholar
  43. 43.
    McFiggans G, Coe H, Burgess R, Allan J, Cubison M, Alfarra MR, Saunders R, Saiz-Lopez A, Plane JMC, Wevill DJ, Carpenter LJ, Rickard AR, Monks PS (2004) Direct evidence for coastal iodine particles from Laminaria macroalgae – linkage to emissions of molecular iodine. Atmos Chem Phys 4:701–713CrossRefGoogle Scholar
  44. 44.
    McFiggans G, Bale CSE, Ball SM, Beames JM, Bloss WJ, Carpenter LJ et al (2010) Iodine-mediated coastal particle formation: an overview of the reactive halogens in the marine boundary layer (RHaMBLe) Roscoff coastal study. Atmos Chem Phys 10:2975–2999CrossRefGoogle Scholar
  45. 45.
    Ball SM, Hollingsworth AM, Humbles J, Leblanc C, Potin P, McFiggans G (2010) Spectroscopic studies of molecular iodine emitted into the gas phase by seaweed. Atmos Chem Phys 10:6237–6254CrossRefGoogle Scholar
  46. 46.
    Kupper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Walte TJ, Boneberg EM, Woitsch S, Weiller M, Abela R, Grolimund D, Potin P, Butler A, Luther GW, Kroneck PMH, Meyer-Klaucke W, Feiters MC (2008) Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc Natl Acad Sci USA 105:6954–6958CrossRefGoogle Scholar
  47. 47.
    Manley SL (2002) Phytogenesis of halomethanes: a product of selection or a metabolic accident? Biogeochemistry 60:163–180CrossRefGoogle Scholar
  48. 48.
    Verhaeghe EF, Fraysse A, Guerquin-Kern JL, Wu TD, Deves G, Mioskowski C, Leblanc C, Ortega R, Ambroise Y, Potin P (2008) Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. J Biol Inorg Chem 13:257–269CrossRefGoogle Scholar
  49. 49.
    Hunter-Cevera JC, Sotos LS (1986) Screening for new enzyme in nature: haloperoxidase production by Death Valley dematiaceous hyphomyctes. Microb Ecol 12:121–127CrossRefGoogle Scholar
  50. 50.
    Hunter JC, Belt A, Sotos LS, Fonda ME (1990) Fungal chloroperoxidase method. US Patent 4,937,192Google Scholar
  51. 51.
    Barnett P, Hemrika W, Hl D, Muijsers AO, Renirie R, Wever R (1998) Isolation, characterization, and primary structure of the vanadium chloroperoxidase from the fungus Embellisia didymospora. J Biol Chem 273:23381–23387CrossRefGoogle Scholar
  52. 52.
    Bar-Nunn N, Shcolnick S, Mayer AM (2002) Presence of a vanadium dependent peroxidase in Botrytis cinerea. FEMS Microbiol Lett 217:121–124CrossRefGoogle Scholar
  53. 53.
    Barnett P, Kruitbosch DL, Hemrika W, Dekker HL, Wever R (1997) The regulation of the vanadium chloroperoxidase from Curvularia inaequalis. Biochim Biophys Acta 1352:73–84Google Scholar
  54. 54.
    Bengtson P, Bastviken D, de Boer W, Öberg G (2009) Possible role of reactive chlorine in microbial antagonism and organic matter chlorination in terrestrial environments. Environ Microbiol 11:1330–1339CrossRefGoogle Scholar
  55. 55.
    Ortiz-Bermúdez P, Hirth KC, Srebotnik E, Hammel KE (2007) Chlorination of lignin by ubiquitous fungi has a likely role in global organochlorine production. Proc Natl Acad Sci USA 104:3895–3900CrossRefGoogle Scholar
  56. 56.
    Fujimori DG, Walsh CT (2007) What is new in enzymatic halogenations. Curr Opin Chem Biol 11:553–560CrossRefGoogle Scholar
  57. 57.
    Wagner C, El Omari M, Konig G (2009) Biohalogenation: nature’s way to synthesize halogenated metabolites. J Nat Prod 72:540–553CrossRefGoogle Scholar
  58. 58.
    Verhaeghe E, Buisson D, Zekri E, Leblanc C, Potin P, Ambroise Y (2008) A colorimetric assay for steady state analysis of iodo- and bromoperoxidase activities. Anal Biochem 379:60–65CrossRefGoogle Scholar
  59. 59.
    De Boer E, Wever R (1988) The reaction mechanism of the novel vanadium-bromoperoxidase, a steady-state kinetic analysis. J Biol Chem 263:12326–12332Google Scholar
  60. 60.
    Soedjak HS, Walker JV, Butler A (1995) Inhibition and inactivation of vanadium bromoperoxidase by the substrate hydrogen peroxide and further mechanistic studies. Biochemistry 34:12689–12696CrossRefGoogle Scholar
  61. 61.
    Renirie R, Pierlot C, Aubry JM, Hartog AF, Schoemaker HE, Alsters PL, Wever R (2003) Vanadium chloroperoxidase as a catalyst for hydrogen peroxide disproportionation to singlet oxygen in mildly acidic environment. Adv Synth Catal 345:849–858CrossRefGoogle Scholar
  62. 62.
    De Boer E, Plat H, Tromp MGM, Wever R, Franssen MCR, van der Plas HC, Meijer EM, Schoemaker HE (1987) Vanadium containing bromoperoxidase: an example of an oxidoreductase with high operational stability in aqeous and organic media. Biotechnol Bioeng 30:607–610CrossRefGoogle Scholar
  63. 63.
    Hasan Z, Renirie R, Kerkman R, Ruijssenaars HJ, Hartog AF, Wever R (2006) Laboratory-evolved vanadium chloroperoxidase exhibits 100-fold higher halogenating activity at alkaline pH; catalytic effects from first and second coordination sphere mutations. J Biol Chem 281:9738–9744CrossRefGoogle Scholar
  64. 64.
    Hemrika W, Renirie R, Macedo-Ribeiro S, Messerschmidt A, Wever R (1999) Heterologous expression of the vanadium-containing chloroperoxidase from Curvularia inaequalis in Saccharomyces cerevisiae and site-directed mutagenesis of the active site residues His496, Lys353, Arg360 and Arg490. J Biol Chem 274:23820–23827CrossRefGoogle Scholar
  65. 65.
    VanSchijndel JWPM, Barnett P, Roelse J, Vollenbroek EGM, Wever R (1994) The stability and steady state kinetics of vanadium chloroperoxidase from the fungus Curvularia inaequalis. Eur J Biochem 22:151–157CrossRefGoogle Scholar
  66. 66.
    Tanaka N, Hasan Z, Wever R (2003) Kinetic characterization of the active site mutants Ser402Ala and Phe397His of vanadium chloroperoxidase from the fungus Curvularia inaequalis. Inorg Chem Acta 356:288–296CrossRefGoogle Scholar
  67. 67.
    Feiters MC, Leblanc C, Kupper FC, Meyer-Klaucke W, Michel G, Potin P (2005) Bromine is an endogenous component of a vanadium bromoperoxidase. J Am Chem Soc 127: 15340–15341CrossRefGoogle Scholar
  68. 68.
    Martínez VM, De Cremer G, Roeffaers MBJ, Sliwa M, Mukulesh M, De Vos DE, Hofkens J, Sels BF (2008) Exploration of single molecule events in a haloperoxidase and its biomimic: localization of halogenation activity. J Am Chem Soc 130:13192–13193CrossRefGoogle Scholar
  69. 69.
    Carter-Franklin JN, Butler A (2004) Vanadium bromoperoxidase-catalyzed biosynthesis of halogenated marine natural products. J Am Chem Soc 126:15060–15066CrossRefGoogle Scholar
  70. 70.
    Butler A, Carter-Franklin JN (2004) The role of vanadium bromoperoxidase in the biosynthesis of halogenated marine natural products. Nat Prod Rep 21:180–188CrossRefGoogle Scholar
  71. 71.
    Weyand M, Hecht HJ, Kiess M, Liaud MF, Vilter H, Schomburg D (1999) X-ray structure determination of a vanadium-dependent haloperoxidase from Ascophyllum nodosum at 2.0 Å resolution. J Mol Biol 293:595–611CrossRefGoogle Scholar
  72. 72.
    Isupov MN, Dalby AR, Brindley AA, Izumi Y, Tanabe T, Murshudov GN, Littlechild JA (2000) Crystal structure of dodecameric vanadium-dependent bromoperoxidase from the red algae Corallina officinalis. J Mol Biol 299:1035–1049CrossRefGoogle Scholar
  73. 73.
    Tromp MGM, Olafsson G, Krenn BE, Wever R (1990) Some structural aspects of vanadium bromoperoxidase from Ascophyllum nodosum. Biochim Biophys Acta 1040:192–198CrossRefGoogle Scholar
  74. 74.
    Arber JM, De Boer E, Garner CD, Hasnain SS, Wever R (1989) Vanadium K-Edge X-ray absorption spectroscopy of bromoperoxidase from Ascophyllum nodosum. Biochemistry 28:7968–7973CrossRefGoogle Scholar
  75. 75.
    Carrano CJ, Mohan M, Holmes SM, Delarosa R, Butler A, Charnock JM, Garner CD (1994) Oxovanadium (V) alkoxy chlorocomplexes of the hydridotripyrozolyl-borates as models for the binding-site in bromoperoxidase. Inorg Chem 33:646–655CrossRefGoogle Scholar
  76. 76.
    De Boer E, Keijzers CP, Klaasen AAK, Reijerse EJ, Collison D, Garner CD, Wever R (1998) N-14-coordination to VO2+ in reduced vanadium bromoperoxidase, an electron spin echo study. FEBS Lett 235:93–97Google Scholar
  77. 77.
    Ohshiro T, Hemrika W, Aibara T, Wever R, Izumi Y (2002) Expression of the vanadium-dependent bromoperoxidase gene from a marine macro-alga Corallina pilulifera in Saccharomyces cerevisiae and characterization of the recombinant enzyme. Phytochemistry 60:595–601CrossRefGoogle Scholar
  78. 78.
    Coupe EE, Smyth MG, Fosberry A, Hall RM, Littlechild JA (2007) The dodecameric vanadium-dependent haloperoxidase from the marine algae Corallina officinalis: Cloning, expression, and refolding of the recombinant enzyme. Protein Expr Purif 52:265–272CrossRefGoogle Scholar
  79. 79.
    Hemrika W, Renirie R, Dekker HL, Barnett P, Wever R (1997) From phosphatases to vanadium peroxidases: a similar architecture of the active site. Proc Natl Acad Sci USA 94:2145–2149CrossRefGoogle Scholar
  80. 80.
    Renirie R, Hemrika W, Piersma SR, Wever R (2000) Cofactor and substrate binding to vanadium-chloroperoxidase determined by UV-VIS spectroscopy and evidence for high affinity for pervanadate. Biochemistry 39:1133–1141CrossRefGoogle Scholar
  81. 81.
    Renirie R, Hemrika W, Wever R (2000) Peroxidase and phosphatase activity of active-site mutants of vanadium chloroperoxidase from the fungus Curvularia inaequalis, implications for the catalytic mechanism. J Biol Chem 275:11650–11657CrossRefGoogle Scholar
  82. 82.
    Smith TS, Pecoraro VL (2002) Oxidation of organic sulfides by vanadium haloperoxidase model complexes. Inorg Chem 41:6754–6760CrossRefGoogle Scholar
  83. 83.
    Zampella G, Fantucci PVL, De Gioia L (2005) Reactivity of Peroxo Forms of the Vanadium Haloperoxidase Cofactor. A DFT investigation. J Am Chem Soc 127:953–960CrossRefGoogle Scholar
  84. 84.
    Pooransingh-Margolis N, Renirie R, Hasan Z, Wever R, Vega AJ, Polenova T (2006) 51V Solid-state magic angle spinning NMR spectroscopy of vanadium chloroperoxidase. J Am Chem Soc 128:5190–5208CrossRefGoogle Scholar
  85. 85.
    Macedo-Ribeiro S, Hemrika W, Renirie R, Wever R, Messerschmidt A (1999) X-ray crystal structures of active site mutants of the vanadium-containing chloroperoxidase from the fungus Curvularia inaequalis. J Biol Inorg Chem 4:209–219CrossRefGoogle Scholar
  86. 86.
    Borowski T, Szczepanik W, Chruszcz M, Broclawik E (2004) First-principle calculations for the active centers in vanadium-containing chloroperoxidase and its functional models: geometrical and spectral properties. Int J Quantum Chem 99:864–875CrossRefGoogle Scholar
  87. 87.
    Plat H, Krenn BE, Wever R (1987) The bromoperoxidase from the lichen Xanthoria parietina is a novel vanadium enzyme. Biochem J 248:277–279Google Scholar
  88. 88.
    Andersson M, Willetts A, Allenmark S (1997) Asymmetric sulfoxidation catalyzed by a vanadium-containing bromoperoxidase. J Org Chem 62:8455–8458CrossRefGoogle Scholar
  89. 89.
    Ten Brink HB, Tuynman A, Dekker HL, Hemrika W, Izumi Y, Oshiro T, Schoemaker HE, Wever R (1998) Enantioselective sulfoxidation catalyzed by vanadium peroxidases. Inorg Chem 37:6780–6784CrossRefGoogle Scholar
  90. 90.
    Ten Brink HB, Schoemaker HE, Wever R (2001) Sulfoxidation mechanism of vanadium bromoperoxidase from Ascophyllum nodosum. Eur J Biochem 268:132–138CrossRefGoogle Scholar
  91. 91.
    Ten Brink HB, Holland HL, Schoemaker HE, Van Lingen H, Wever R (1999) Probing the scope of the sulfoxidation activity of vanadium bromoperoxidase from Ascophyllum nodosum. Tetrahedron Asym 10:4563–4572CrossRefGoogle Scholar
  92. 92.
    Ten Brink HB, Dekker HL, Schoemaker HE, Wever R (2000) Oxidation reactions catalyzed by vanadium chloroperoxidase from Curvularia inaequalis. J Inorg Biochem 80:91–98CrossRefGoogle Scholar
  93. 93.
    Sheffield DJ, Harry T, Smith AJ, Rogers LJ (1993) Purification and characterization of the vanadium bromoperoxidase from the macroalga Corallina officinalis. Phytochemistry 32:21–26CrossRefGoogle Scholar
  94. 94.
    Zhang B, Cao X, Chenf X, Wu P, Xiao T, Zhang W (2010) Efficient purification with high recovery of vanadium bromoperoxidase from Corallina officinalis. Biotechnol Lett. doi:10.1007/s10529-010-0454-yGoogle Scholar
  95. 95.
    Garcia-Rodriguez E, Ohshiro T, Aibara T, Izumi Y, Littlechild J (2005) Enhancing effect of calcium and vanadium ions on thermal stability of bromoperoxidase from Corallina pilulifera. J Biol Inorg Chem 10:275–282CrossRefGoogle Scholar
  96. 96.
    Renirie R, Pierlot C, Wever R, Aubry JM (2008) Singlet oxygenation in microemulsion catalyzed by vanadium chloroperoxidase. J Mol Catal B Enzym 56:259–264CrossRefGoogle Scholar
  97. 97.
    Hoogenkamp MA, Crielaard W, Ten Cate JM, Wever R, Hartog AF, Renirie R (2009) Antimicrobial activity of vanadium chloroperoxidase on planktonic Streptococcus mutans cells and Streptococcus mutans biofilms. Caries Res 43:334–338CrossRefGoogle Scholar
  98. 98.
    Littlechild J, Garcia-Rodriguez E, Dalby A, Isupov M (2002) Structural and functional comparisons between vanadium haloperoxidase and acid phosphatase enzymes. J Mol Recognit 15:291–296CrossRefGoogle Scholar
  99. 99.
    Messerschmidt A, Prade L, Wever R (1997) Implications for the catalytic mechanism of the vanadium-containing enzyme chloroperoxidase from the fungus Curvularia inaequalis by X-ray structures of the native and peroxide form. Biol Chem 378:309–315CrossRefGoogle Scholar
  100. 100.
    Messerschmidt A, Wever R (1996) X-ray structure of a vanadium-containing enzyme: chloroperoxidase from the fungus Curvularia inaequalis. Proc Natl Acad Sci USA 93: 392–396CrossRefGoogle Scholar
  101. 101.
    Renirie R, Charnock JM, Garner CD, Wever R (2010) Vanadium K-edge XAS studies on the native and peroxo forms of vanadium chloroperoxidase from Curvularia inaequalis. J Inorg Biochem 104:657–664CrossRefGoogle Scholar
  102. 102.
    Tanaka N, Wever R (2004) Hydroxyalamine, hydrazine and azide inhibition and phosphate inactivation of vanadium chloroperoxidase from the fungus Curvularia inaequalis. J Inorg Biochem 98:625–630CrossRefGoogle Scholar
  103. 103.
    Kravitz JY, Pecoraro VL, Carlson HA (2005) Quantum mechanics calculation of the vanadium dependent chloroperoxidase. J Chem Theory Comput 1:1265–1274CrossRefGoogle Scholar
  104. 104.
    Ohshiro T, Littlechild J, Garcia-Rodriguez E, Isupov MN, Iida Y, Kobayashi T, Izumi Y (2004) Modification of halogen specificity of a vanadium-dependent bromoperoxidase. Protein Sci 13:1566–1571CrossRefGoogle Scholar
  105. 105.
    Pacois LF, Galvez O (2010) Active site, catalytic cycle, and iodination reactions of vanadium iodoperoxidase: a computational study. J Chem Theory Comput 6:1738–1752CrossRefGoogle Scholar
  106. 106.
    Tanaka N, Dumay V, Liao Q, Lange AJ, Wever R (2002) Bromoperoxidase activity of vanadate-substituted acid phosphatases from Shigella flexneri and Salmonella enterica ser. typhimurium. Eur J Biochem 269:2162–2167CrossRefGoogle Scholar
  107. 107.
    Ishikawa K, Mihara Y, Gondoh K, Suzuki E, Asano Y (2000) X-ray structures of a novel acid phosphatase from Escherichia blattae and its complex with the transition-state analog molybdate. EMBO J 19:2412–2423CrossRefGoogle Scholar
  108. 108.
    Makde RD, Mahajan SK, Kumar V (2007) Structure and mutational analysis of the PhoN protein of Salmonella typhimurium provide insight into mechanistic details. Biochemistry 46:2079–2090CrossRefGoogle Scholar
  109. 109.
    Zampella G, Fantucci P, Pecoraro VL, De Gioia L (2006) Insight into the catalytic mechanism of vanadium haloperoxidases. DFT investigation of vanadium cofactor reactivity. Inorg Chem 45:7133–7143CrossRefGoogle Scholar
  110. 110.
    Bangesh M, Plass W (2005) TD-DFT studies on the electronic structure of imidazole bound vanadate in vanadium containing haloperoxidases (VHPO). J Mol Struct Theochem 725: 163–175CrossRefGoogle Scholar
  111. 111.
    Raugei S, Carloni P (2006) Structure and function of vanadium haloperoxidases. J Phys Chem B 110:3747–3758CrossRefGoogle Scholar
  112. 112.
    Waller MP, Buhl M, Geethalakshmi KR, Wang DQ, Thiel W (2007) V-51 NMR chemical shifts calculated from QM/MM models of vanadium chloroperoxidase. Chem Eur J 13: 4723–4732CrossRefGoogle Scholar
  113. 113.
    Zhang Y, Gascón J (2008) QM/MM investigation of structure and spectroscopic properties of a vanadium-containing peroxidase. J Inorg Biochem 102:1684–1690CrossRefGoogle Scholar
  114. 114.
    Littlechild J, Garcia-Rodriguez E, Isupov M (2009) Vanadium containing bromoperoxidase – insights into the enzymatic mechanism using X-ray crystallography. J Inorg Biochem 103: 617–621CrossRefGoogle Scholar
  115. 115.
    Winter JM, Moffitt MC, Zazopoulos E, McAlpine JB, DorresteinPC MBS (2007) Molecular basis for chloronium-mediated meroterpene cyclization: cloning, sequencing, and heterologous expression of the napyradiomycin biosynthetic gene cluster. J Biol Chem 282: 16362–16368CrossRefGoogle Scholar
  116. 116.
    Neuwald AF (1997) An unexpected structural relationship between integral membrane phosphatases and soluble haloperoxidases. Protein Sci 6:1764–1767CrossRefGoogle Scholar
  117. 117.
    Stukey J, Carman GM (1997) Identification of a novel phosphatase sequence motif. Protein Sci 6:469–472CrossRefGoogle Scholar
  118. 118.
    Brindley DN, Waggoner DW (1998) Mammalian lipid phosphate phosphohydrolases. J Biol Chem 273:24281–24284CrossRefGoogle Scholar
  119. 119.
    Macedo-Ribeiro S, Renirie R, Wever R, Messerschmidt A (2008) Crystal structure of a trapped phosphate intermediate in vanadium apochloroperoxidase catalyzing a dephosphorylation reaction. Biochemistry 47:929–934CrossRefGoogle Scholar
  120. 120.
    Van de Velde F, Arends IWCE, Sheldon RA (2000) Biocatalytic and biomimetic oxidations with vanadium. J Inorg Biochem 80:81–89CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Van ‘t Hoff Institute for Molecular SciencesUniversity of AmsterdamAmsterdamThe Netherlands

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