Table of Contents Author Guidelines Submit a Manuscript
Bioinorganic Chemistry and Applications
Volume 2012, Article ID 626909, 13 pages
http://dx.doi.org/10.1155/2012/626909
Review Article

Alkene Cleavage Catalysed by Heme and Nonheme Enzymes: Reaction Mechanisms and Biocatalytic Applications

Department of Chemistry, Organic and Bioorganic Chemistry, University of Graz, Heinrichstrasse 28, 8010 Graz, Austria

Received 29 April 2012; Accepted 13 May 2012

Academic Editor: Ian Butler

Copyright © 2012 Francesco G. Mutti. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. A. Berglund, Encyclopedia of Reagents for Organic Synthesis, vol. 6, Wiley, New York, NY, USA, 1995.
  2. K. Koike, G. Inoue, and T. Fukuda, “Explosion hazard of gaseous ozone,” Journal of Chemical Engineering of Japan, vol. 32, no. 3, pp. 295–299, 1999. View at Google Scholar · View at Scopus
  3. R. A. Ogle and J. L. Schumacher, “Investigation of an explosion and flash fire in a fixed bed reactor,” Process Safety Progress, vol. 17, no. 2, pp. 127–133, 1998. View at Google Scholar · View at Scopus
  4. J. March, Advanced Organic Chemistry. Reactions, Mechanisms and Structures, Wiley, New York, NY, USA, 4th edition, 1992.
  5. P. Y. Bruice, Organic Chemistry. International Edition, Pearson Education, Upper Saddle River, NJ, USA, 4th edition, 2004.
  6. R. U. Lemieux and E. Von Rudloff, “Periodate-permanganate oxidations: I. Oxidation of olefins,” Canadian Journal of Chemistry, vol. 33, no. 11, pp. 1701–1709, 1955. View at Google Scholar
  7. C. E. Paul, A. Rajagopalan, I. Lavandera, V. Gotor-Fernandez, W. Kroutil, and V. Gotor, “Expanding the regioselective enzymatic repertoire: oxidative mono-cleavage of dialkenes catalyzed by Trametes hirsuta,” Chemical Communications, vol. 48, no. 27, pp. 3303–3305, 2012. View at Publisher · View at Google Scholar
  8. M. Lara, F. G. Mutti, S. M. Glueck, and W. Kroutil, “Biocatalytic cleavage of alkenes with O2 and Trametes hirsuta G FCC 047,” European Journal of Organic Chemistry, no. 21, pp. 3668–3672, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Lara, F. G. Mutti, S. M. Glueck, and W. Kroutil, “Oxidative enzymatic alkene cleavage: indications for a nonclassical enzyme mechanism,” Journal of the American Chemical Society, vol. 131, no. 15, pp. 5368–5369, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Schrader, M. M. W. Etschmann, D. Sell, J. M. Hilmer, and J. Rabenhorst, “Applied biocatalysis for the synthesis of natural flavour compounds-current industrial processes and future prospects,” Biotechnology Letters, vol. 26, no. 6, pp. 463–472, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Adam, M. Lazarus, C. R. Saha-Moller et al., “Biotransformations with peroxidases,” in Advanced in Biochemical Engineering/Biotechnology, T. Sheper, Ed., vol. 63, pp. 73–108, Springer-Verlag, Berlin, Germany, 1999. View at Google Scholar
  12. G. I. Berglund, G. H. Carlsson, A. T. Smith, H. Szöke, A. Henriksen, and J. Hajdu, “The catalytic pathway of horseradish peroxidase at high resolution,” Nature, vol. 417, no. 6887, pp. 463–468, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Schlichting, J. Berendzen, K. Chu et al., “The catalytic pathway of cytochrome P450cam at atomic resolution,” Science, vol. 287, no. 5458, pp. 1615–1622, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Cilento and W. Adam, “From free radicals to electronically excited species,” Free Radical Biology and Medicine, vol. 19, no. 1, pp. 103–114, 1995. View at Publisher · View at Google Scholar · View at Scopus
  15. P. D. Shaw and L. P. Hager, “Biological Chlorination: VI: chloroperoxidase: a component of the β-ketoadipate chlorinase system,” Journal of Biological Chemistry, vol. 236, no. 6, pp. 1626–1630, 1961. View at Google Scholar
  16. L. P. Hager, D. R. Morris, F. S. Brown, and H. Eberwein, “Chloroperoxidase. II. Utilization of halogen anions,” Journal of Biological Chemistry, vol. 241, no. 8, pp. 1769–1777, 1966. View at Google Scholar · View at Scopus
  17. J. A. Thomas, D. R. Morris, and L. P. Hager, “Chloroperoxidase. VII. Classical peroxidatic, catalatic, and halogenating forms of the enzyme,” Journal of Biological Chemistry, vol. 245, no. 12, pp. 3129–3134, 1970. View at Google Scholar · View at Scopus
  18. A. Zaks and D. R. Dodds, “Chloroperoxidase-catalyzed asymmetric oxidations: substrate specificity and mechanistic study,” Journal of the American Chemical Society, vol. 117, no. 42, pp. 10419–10424, 1995. View at Google Scholar · View at Scopus
  19. M. P. J. Van Deurzen, F. Van Rantwijk, and R. A. Sheldon, “Selective oxidations catalyzed by peroxidases,” Tetrahedron, vol. 53, no. 39, pp. 13183–13220, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Colonna, N. Gaggero, C. Richelmi, and P. Pasta, “Recent biotechnological developments in the use of peroxidases,” Trends in Biotechnology, vol. 17, no. 4, pp. 163–168, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. S. R. Blanke and L. P. Hager, “Identification of the fifth axial heme ligand of chloroperoxidase,” Journal of Biological Chemistry, vol. 263, no. 35, pp. 18739–18743, 1988. View at Google Scholar · View at Scopus
  22. P. R. Ortiz De Montellano, Y. S. Choe, G. DePillis, and C. E. Catalano, “Structure-mechanism relationships in hemoproteins. Oxygenations catalyzed by chloroperoxidase and horseradish peroxidase,” Journal of Biological Chemistry, vol. 262, no. 24, pp. 11641–11646, 1987. View at Google Scholar · View at Scopus
  23. J. Geigert, T. D. Lee, D. J. Dalietos, D. S. Hirano, and S. L. Neidleman, “Epoxidation of alkenes by chloroperoxidase catalysis,” Biochemical and Biophysical Research Communications, vol. 136, no. 2, pp. 778–782, 1986. View at Google Scholar · View at Scopus
  24. E. J. Allain, L. P. Hager, L. Deng, and E. N. Jacobsen, “Highly enantioselective epoxidation of disubstituted alkenes with hydrogen peroxide catalyzed by chloroperoxidase,” Journal of the American Chemical Society, vol. 115, no. 10, pp. 4415–4416, 1993. View at Google Scholar · View at Scopus
  25. D. J. Bougioukou and I. Smonou, “Chloroperoxidase-catalyzed oxidation of conjugated dienoic esters,” Tetrahedron Letters, vol. 43, no. 2, pp. 339–342, 2002. View at Google Scholar · View at Scopus
  26. D. J. Bougioukou and I. Smonou, “Mixed peroxides from the chloroperoxidase-catalyzed oxidation of conjugated dienoic esters with a trisubstituted terminal double bond,” Tetrahedron Letters, vol. 43, no. 25, pp. 4511–4514, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Chamulitrat, N. Takahashi, and R. P. Mason, “Peroxyl, alkoxyl, and carbon-centered radical formation from organic hydroperoxides by chloroperoxidase,” Journal of Biological Chemistry, vol. 264, no. 14, pp. 7889–7899, 1989. View at Google Scholar · View at Scopus
  28. M. Gajhede, D. J. Schuller, A. Henriksen, A. T. Smith, and T. L. Poulos, “Crystal structure of horseradish peroxidase C at 2.15 Å resolution,” Nature Structural Biology, vol. 4, no. 12, pp. 1032–1038, 1997. View at Google Scholar · View at Scopus
  29. P. R. Ortiz De Montellano and L. A. Grab, “Cooxidation of styrene by horseradish peroxidase and phenols: a biochemical model for protein-mediated cooxidation,” Biochemistry, vol. 26, no. 17, pp. 5310–5314, 1987. View at Google Scholar · View at Scopus
  30. S.-I. Ozaki and P. R. Ortiz De Montellano, “Molecular engineering of horseradish peroxidase: thioether sulfoxidation and styrene epoxidation by Phe-41 leucine and threonine mutants,” Journal of the American Chemical Society, vol. 117, no. 27, pp. 7056–7064, 1995. View at Google Scholar · View at Scopus
  31. K. Q. Ling and L. M. Sayre, “Horseradish peroxidase-mediated aerobic and anaerobic oxidations of 3-alkylindoles,” Bioorganic and Medicinal Chemistry, vol. 13, no. 10, pp. 3543–3551, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. F. G. Mutti, M. Lara, M. Kroutil, and W. Kroutil, “Ostensible enzyme promiscuity: alkene cleavage by peroxidases,” Chemistry, vol. 16, no. 47, pp. 14142–14148, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Tuynman, J. L. Spelberg, I. M. Kooter, H. E. Schoemaker, and R. Wever, “Enantioselective epoxidation and carbon-carbon bond cleavage catalyzed by Coprinus cinereus peroxidase and myeloperoxidase,” Journal of Biological Chemistry, vol. 275, no. 5, pp. 3025–3030, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. U. T. Bornscheuer and R. J. Kazlauskas, “Catalytic promiscuity in biocatalysis: using old enzymes to form new bonds and follow new pathways,” Angewandte Chemie, vol. 43, no. 45, pp. 6032–6040, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Hult and P. Berglund, “Enzyme promiscuity: mechanism and applications,” Trends in Biotechnology, vol. 25, no. 5, pp. 231–238, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. P. J. O'Brien and D. Herschlag, “Catalytic promiscuity and the evolution of new enzymatic activities,” Chemistry and Biology, vol. 6, no. 4, pp. R91–R105, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Sono, M. P. Roach, E. D. Coulter, and J. H. Dawson, “Heme-containing oxygenases,” Chemical Reviews, vol. 96, no. 7, pp. 2841–2887, 1996. View at Google Scholar · View at Scopus
  38. S. G. Cady and M. Sono, “1-methyl-DL-tryptophan, β-(3-benzofuranyl)-DL-alanine (the oxygen analog of tryptophan), and β-[3-benzo(b)thienyl]-DL-alanine (the sulfur analog of tryptophan) are competitive inhibitors for indoleamine 2,3-dioxygenase,” Archives of Biochemistry and Biophysics, vol. 291, no. 2, pp. 326–333, 1991. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Chauhan, S. J. Thackray, S. A. Rafice et al., “Reassessment of the reaction mechanism in the heme dioxygenases,” Journal of the American Chemical Society, vol. 131, no. 12, pp. 4186–4187, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Chauhan, J. Basran, I. Efimov et al., “The role of serine 167 in human indoleamine 2,3-dioxygenase: a comparison with tryptophan 2,3-dioxygenase,” Biochemistry, vol. 47, no. 16, pp. 4761–4769, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. S. J. Thackray, C. Bruckmann, J. L. R. Anderson et al., “Histidine 55 of tryptophan 2,3-dioxygenase is not an active site base but regulates catalysis by controlling substrate binding,” Biochemistry, vol. 47, no. 40, pp. 10677–10684, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. G. Yagil, “The proton dissociation constant of pyrrole, indole and related compounds,” Tetrahedron, vol. 23, no. 6, pp. 2855–2861, 1967. View at Google Scholar · View at Scopus
  43. I. Efimov, J. Basran, S. J. Thackray, S. Handa, C. G. Mowat, and E. L. Raven, “Structure and reaction mechanism in the heme dioxygenases,” Biochemistry, vol. 50, no. 14, pp. 2717–2724, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Basran, I. Efimov, N. Chauhan et al., “The mechanism of formation of N-formylkynurenine by heme dioxygenases,” Journal of the American Chemical Society, vol. 133, no. 40, pp. 16251–16257, 2011. View at Publisher · View at Google Scholar
  45. A. Lewis-Ballester, D. Batabyal, T. Egawa et al., “Evidence for a ferryl intermediate in a heme-based dioxygenase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 41, pp. 17371–17376, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. L. W. Chung, X. Li, H. Sugimoto, Y. Shiro, and K. Morokuma, “ONIOM study on a missing piece in our understanding of heme chemistry: bacterial tryptophan 2,3-dioxygenase with dual oxidants,” Journal of the American Chemical Society, vol. 132, no. 34, pp. 11993–12005, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. T. D. H. Bugg and C. J. Winfield, “Enzymatic cleavage of aromatic rings: mechanistic aspects of the catechol dioxygenases and later enzymes of bacterial oxidative cleavage pathways,” Natural Product Reports, vol. 15, no. 5, pp. 513–530, 1998. View at Google Scholar · View at Scopus
  48. O. Hayaishi, M. Katagiri, and S. Rothberg, “Mechanism of the pyrocatechase reaction,” Journal of the American Chemical Society, vol. 77, no. 20, pp. 5450–5451, 1955. View at Google Scholar · View at Scopus
  49. O. Hayaishi, “Crystalline oxygenases of pseudomonads,” Bacteriological Reviews, vol. 30, no. 4, pp. 720–731, 1966. View at Google Scholar · View at Scopus
  50. R. J. Mayer and L. Que, “18O studies of pyrogallol cleavage by catechol 1,2-dioxygenase,” Journal of Biological Chemistry, vol. 259, no. 21, pp. 13056–13060, 1984. View at Google Scholar · View at Scopus
  51. E. L. Spence, G. J. Langley, and T. D. H. Bugg, “Cis-trans isomerization of a cyclopropyl radical trap catalyzed by extradiol catechol dioxygenases: evidence for a semiquinone intermediate,” Journal of the American Chemical Society, vol. 118, no. 35, pp. 8336–8343, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. F. H. Vaillancourt, C. J. Barbosa, T. G. Spiro et al., “Definitive evidence for monoanionic binding of 2,3-dihydroxybiphenyl to 2,3-dihydroxybiphenyl 1,2-dioxygenase from UV resonance Raman spectroscopy, UV/Vis absorption spectroscopy, and crystallography,” Journal of the American Chemical Society, vol. 124, no. 11, pp. 2485–2496, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Sanvoisin, G. J. Langley, and T. D. H. Bugg, “Mechanism of extradiol catechol dioxygenases: evidence for a lactone intermediate in the 2,3-dihydroxyphenylpropionate 1,2-dioxygenase reaction,” Journal of the American Chemical Society, vol. 117, no. 29, pp. 7836–7837, 1995. View at Google Scholar · View at Scopus
  54. D. P. Kloer and G. E. Schulz, “Structural and biological aspects of carotenoid cleavage,” Cellular and Molecular Life Sciences, vol. 63, no. 19-20, pp. 2291–2303, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. M. E. Auldridge, D. R. McCarty, and H. J. Klee, “Plant carotenoid cleavage oxygenases and their apocarotenoid products,” Current Opinion in Plant Biology, vol. 9, no. 3, pp. 315–321, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. E. K. Marasco, K. Vay, and C. Schmidt-Dannert, “Identification of carotenoid cleavage dioxygenases from Nostoc sp. PCC 7120 with different cleavage activities,” Journal of Biological Chemistry, vol. 281, no. 42, pp. 31583–31593, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. J. A. Olson and O. Hayaishi, “The enzymatic cleavage of beta-carotene into vitamin A by soluble enzymes of rat liver and intestine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 54, no. 5, pp. 1364–1370, 1965. View at Google Scholar · View at Scopus
  58. M. G. Leuenberger, C. Engeloch-Jarret, and W. D. Woggon, “The reaction mechanism of the enzyme-catalyzed central cleavage of β-carotene to retinal,” Angewandte Chemie, vol. 40, no. 14, pp. 2614–2617, 2001. View at Google Scholar · View at Scopus
  59. A. During and E. H. Harrison, “Intestinal absorption and metabolism of carotenoids: insights from cell culture,” Archives of Biochemistry and Biophysics, vol. 430, no. 1, pp. 77–88, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. H. Schmidt, R. Kurtzer, W. Eisenreich, and W. Schwab, “The carotenase AtCCD1 from Arabidopsis thaliana is a dioxygenase,” Journal of Biological Chemistry, vol. 281, no. 15, pp. 9845–9851, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. D. P. Kloer, S. Ruch, S. Al-Babili, P. Beyer, and G. E. Schulz, “The structure of a retinal-forming carotenoid oxygenase,” Science, vol. 308, no. 5719, pp. 267–269, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Borowski, M. R. A. Blomberg, and P. E. M. Siegbahn, “Reaction mechanism of apocarotenoid oxygenase (ACO): a DFT study,” Chemistry, vol. 14, no. 7, pp. 2264–2276, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. E. K. Marasco and C. Schmidt-Dannert, “Identification of bacterial carotenoid cleavage dioxygenase homologues that cleave the interphenyl α,β double bond of stilbene derivatives via a monooxygenase reaction,” ChemBioChem, vol. 9, no. 9, pp. 1450–1461, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Schilling, F. Patett, W. Schwab, and J. Schrader, “Influence of solubility-enhancing fusion proteins and organic solvents on the in vitro biocatalytic performance of the carotenoid cleavage dioxygenase AtCCD1 in a micellar reaction system,” Applied Microbiology and Biotechnology, vol. 75, no. 4, pp. 829–836, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Nacke and J. Schrader, “Micelle based delivery of carotenoid substrates for enzymatic conversion in aqueous media,” Journal of Molecular Catalysis B, vol. 77, pp. 67–73, 2012. View at Publisher · View at Google Scholar
  66. S. Kamoda, N. Habu, M. Samejima, and T. Yoshimoto, “Purification and some properties of lignostilbene-α,β-dioxygenase responsible for the C(α)-C(β) cleavage of a diarylpropane type lignin model compound from Pseudomonas sp. TMY1009,” Agricultural and Biological Chemistry, vol. 53, no. 10, pp. 2757–2761, 1989. View at Google Scholar · View at Scopus
  67. S. Kamoda, T. Terada, and Y. Saburi, “A common structure of substrate shared by lignostilbenedioxygenase isozymes from Sphingomonas paucimobilis TMY1009,” Bioscience, Biotechnology and Biochemistry, vol. 67, no. 6, pp. 1394–1396, 2003. View at Google Scholar · View at Scopus
  68. S. Kamoda and Y. Saburi, “Structural and enzymatical comparison of lignostilbene-alpha,beta-dioxygenase isozymes, I, II, and III, from Pseudomonas paucimobilis TMY1009,” Bioscience, Biotechnology, and Biochemistry, vol. 57, no. 6, pp. 931–934, 1993. View at Google Scholar · View at Scopus
  69. A. Makoto, A. Niwa, S. Kamoda, and Y. Saburi, “Reactivity and stability of Lignostilbene-α, β-dioxygenase-I in various pHs, temperatures, and in aqueous organic solvents,” Journal of Microbiology and Biotechnology, vol. 11, no. 5, pp. 884–886, 2001. View at Google Scholar · View at Scopus
  70. M. Yamada, Y. Okada, T. Yoshida, and T. Nagasawa, “Purification, characterization and gene cloning of isoeugenol-degrading enzyme from Pseudomonas putida IE27,” Archives of Microbiology, vol. 187, no. 6, pp. 511–517, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Braaz, P. Fischer, and D. Jendrossek, “Novel type of heme-dependent oxygenase catalyzes oxidative cleavage of rubber (poly-cis-1,4-isoprene),” Applied and Environmental Microbiology, vol. 70, no. 12, pp. 7388–7395, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Braaz, W. Armbruster, and D. Jendrossek, “Heme-dependent rubber oxygenase RoxA of Xanthomonas sp. cleaves the carbon backbone of poly(cis-1,4-isoprene) by a dioxygenase mechanism,” Applied and Environmental Microbiology, vol. 71, no. 5, pp. 2473–2478, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. G. Bourel, J. M. Nicaud, B. Nthangeni, P. Santiago-Gomez, J. M. Belin, and F. Husson, “Fatty acid hydroperoxide lyase of green bell pepper: cloning in Yarrowia lipolytica and biogenesis of volatile aldehydes,” Enzyme and Microbial Technology, vol. 35, no. 4, pp. 293–299, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. G. D. Straganz, H. Hofer, W. Steiner, and B. Nidetzky, “Electronic substituent effects on the cleavage specificity of a non-heme Fe2+-dependent β-diketone dioxygenase and their mechanistic implications,” Journal of the American Chemical Society, vol. 126, no. 39, pp. 12202–12203, 2004. View at Publisher · View at Google Scholar · View at Scopus