Discovery of a linoleate 9S-dioxygenase and an allene oxide synthase in a fusion protein of Fusarium oxysporum

Journal of Lipid Research

Volumn 54, Issue 12, 2013, Pages 3471-3480

  Hoffmann, Inga ^a   Oliw, Ernst H ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Cytochrome P450 class III; Heme peroxidase; Linoleate diol synthase; Mutagenesis site specific; Oxygenation mechanism; Oxylipin biosynthesis

Indexed keywords

11 HYDROPEROXIDE DERIVATIVE; 9 HYDROPEROXIDE DERIVATIVE; ALLENE OXIDE DERIVATIVE; ALLENE OXIDE SYNTHASE; ASPARAGINE; DIOXYGENASE; FATTY ACID; FOXB 01332 PROTEIN; FUNGAL PROTEIN; GLUTAMINE; HYBRID PROTEIN; HYDROPEROXIDE; LINOLEATE 9S DIOXYGENASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; FUSARIUM OXYSPORUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

CYTOCHROME P450 CLASS III; HEME PEROXIDASE; LINOLEATE DIOL SYNTHASE; MUTAGENESIS SITE-SPECIFIC; OXYGENATION MECHANISM; OXYLIPIN BIOSYNTHESIS;

ALPHA-LINOLENIC ACID; AMINO ACID SEQUENCE; BIOCATALYSIS; COMPUTATIONAL BIOLOGY; FUSARIUM; HYDROLYSIS; INTRAMOLECULAR OXIDOREDUCTASES; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; RECOMBINANT FUSION PROTEINS;

EID: 84887940806     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M044347     Document Type: Article

References (45)

1. Smith, W. L., Y. Urade, and P. J. Jakobsson. 2011. Enzymes of the cyclooxygenase pathways of prostanoid biosynthesis. Chem. Rev. 111:5821-5865.
2. Ullrich, V., and R. Brugger. 1994. Prostacyclin and thromboxane synthase: new aspects of hemethiolate catalysis. Angew. Chem. Int. Ed. Engl. 33:1911-1919.
3. Wasternack, C., and E. Kombrink. 2010. Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem. Biol. 5:63-77.
4. Hamberg, M., and H. W. Gardner. 1992. Oxylipin pathway to jasmonates: biochemistry and biological significance. Biochim. Biophys. Acta. 1165:1-18.
5. Gfeller, A., L. Dubugnon, R. Liechti, and E. E. Farmer. 2010. Jasmonate biochemical pathway. Sci. Signal. 3: cm3.
6. Hamberg, M. 2000. New cyclopentenone fatty acids formed from linoleic and linolenic acids in potato. Lipids. 35:353-363. (Pubitemid 30252611)
7. Brash, A. R., W. E. Boeglin, D. F. Stec, M. Voehler, C. Schneider, and J. K. Cha. 2013. Isolation and characterization of two geometric allene oxide isomers synthesized from 9S-hydroperoxylinoleic acid by cytochrome P450 CYP74C3: stereochemical assignment of natural fatty acid allene oxides. J. Biol. Chem. 288:20797-20806.
8. Wasternack, C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. (Lond.). 100:681-697. (Pubitemid 47511777)
9. Vick, B. A., and D. C. Zimmerman. 1984. Biosynthesis of jasmonic acid by several plant species. Plant Physiol. 75:458-461.
10. Cross, B. E., and G. R. B. Webster. 1970. New metabolites of Gibberella fujikuroi. Part XV. N-jasmonoyl- and N-dihydrojasmonoylisoleucine. J. Chem. Soc. C. 1970:1839-1842.
11. Aldridge, D. C., S. Galt, D. Giles, and W. B. Turner. 1971. Metabolites of Lasiodiplodia theobromae. J. Chem. Soc. C. 1971:1623-1627.
12. Miersch, O., H. Bohlmann, and C. Wasternack. 1999. Jasmonates and related compounds from Fusarium oxysporum. Phytochemistry. 50:517-523. (Pubitemid 29058482)
13. Miersch, O., T. Günther, W. Fritsche, and G. Sembdner. 1993. Jasmonates from different fungal species. Nat. Prod. Lett. 2:293-299.
14. Miersch, O., A. Preiss, G. Sembdner, and K. Schreiber. 1987. (+)-7-Iso-jasmonic acid and related compounds from Botryodiplodia theobromae. Phytochemistry. 26:1037-1039.
15. Tsukada, K., K. Takahashi, and K. Nabeta. 2010. Biosynthesis of jasmonic acid in a plant pathogenic fungus, Lasiodiplodia theobromae. Phytochemistry. 71:2019-2023.
16. Brodhun, F., A. Cristobal-Sarramian, S. Zabel, J. Newie, M. Hamberg, and I. Feussner. 2013. An iron 13S-lipoxygenase with an a-linolenic acid specific hydroperoxidase activity from Fusarium oxysporum. PLoS ONE. 8:e64919.
17. Jernerén, F., I. Hoffmann, and E. H. Oliw. 2010. Linoleate 9R-dioxygenase and allene oxide synthase activities of Aspergillus terreus. Arch. Biochem. Biophys. 495:67-73.
18. Hoffmann, I., F. Jernerén, and E. H. Oliw. 2013. Expression of fusion proteins of Aspergillus terreus reveals a novel allene oxide synthase. J. Biol. Chem. 288:11459-11469.
19. Dean, R., J. A. Van Kan, Z. A. Pretorius, K. E. Hammond-Kosack, A. Di Pietro, P. D. Spanu, J. J. Rudd, M. Dickman, R. Kahmann, J. Ellis, et al. 2012. The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13:414-430.
20. Lee, D. S., P. Nioche, M. Hamberg, and C. S. Raman. 2008. Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature. 455:363-368.
21. Garscha, U., F. Jernerén, D. Chung, N. P. Keller, M. Hamberg, and E. H. Oliw. 2007. Identification of dioxygenases required for Aspergillus development. Studies of products, stereochemistry, and the reaction mechanism. J. Biol. Chem. 282:34707-34718. (Pubitemid 350232447)
22. Brodhun, F., C. Göbel, E. Hornung, and I. Feussner. 2009. Identification of PpoA from Aspergillus nidulans as a fusion protein of a fatty acid heme dioxygenase/peroxidase and a cytochrome P450. J. Biol. Chem. 284:11792-11805.
23. Hoffmann, I., F. Jernerén, U. Garscha, and E. H. Oliw. 2011. Expression of 5, 8-LDS of Aspergillus fumigatus and its dioxygenase domain. A comparison with 7, 8-LDS, 10-dioxygenase, and cyclooxygenase. Arch. Biochem. Biophys. 506:216-222.
24. Oldham, M. L., A. R. Brash, and M. E. Newcomer. 2005. The structure of coral allene oxide synthase reveals a catalase adapted for metabolism of a fatty acid hydroperoxide. Proc. Natl. Acad. Sci. USA. 102:297-302. (Pubitemid 40116761)
25. Hoffmann, I., and E. H. Oliw. 2013. 7, 8- and 5, 8-linoleate diol synthases support the heterolytic scission of oxygen-oxygen bonds by different amide residues. Arch. Biochem. Biophys. 539:87-91.
26. Oliw, E. H., A. Wennman, I. Hoffmann, U. Garscha, M. Hamberg, and F. Jernerén. 2011. Stereoselective oxidation of regioisomeric octadecenoic acids by fatty acid dioxygenases. J. Lipid Res. 52:1995-2004.
27. Matthew, J. A., H. W. Chan, and T. Galliard. 1977. A simple method for the preparation of pure 9-D-hydroperoxide of linoleic acid and methyl linoleate based on the positional specificity of lipoxygenase in tomato fruit. Lipids. 12:324-326. (Pubitemid 8062331)
28. Su, C, and E. H. Oliw. 1998. Manganese lipoxygenase. Purification and characterization. J. Biol. Chem. 273:13072-13079. (Pubitemid 28246873)
29. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
30. Hall, B. G. 2013. Building phylogenetic trees from molecular data with MEGA. Mol. Biol. Evol. 30:1229-1235.
31. MacMillan, D. K., and R C. Murphy. 1995. Analysis of lipid hydroperoxides and long-chain conjugated keto acids by negative ion electrospray mass spectrometry. J. Am. Soc. Mass Spectrom. 6:1190-1201.
32. Oliw, E. H., U. Garscha, T. Nilsson, and M. Cristea. 2006. Payne rearrangement during analysis of epoxyalcohols of linoleic and alpha-linolenic acids by normal phase liquid chromatography with tandem mass spectrometry. Anal. Biochem. 354:111-126. (Pubitemid 43816395)
33. Oliw, E. H., C. Su, T. Skogström, and G. Benthin. 1998. Analysis of novel hydroperoxides and other metabolites of oleic, linoleic, and linolenic acids by liquid chromatography-mass spectrometry with ion trap MSn. Lipids. 33:843-852. (Pubitemid 28460150)
34. Jernerén, F., F. Eng, M. Hamberg, and E. H. Oliw. 2012. Linolenate 9R-dioxygenase and allene oxide synthase activities of Lasiodiplodia theobromae. Lipids. 47:65-73.
35. Brash, A. R. 2009. Mechanistic aspects of CYP74 allene oxide synthases and related cytochrome P450 enzymes. Phytochemistry. 70:1522-1531.
36. Gao, B., W. E. Boeglin, and A R. Brash. 2008. Role of the conserved distal heme asparagine of coral allene oxide synthase (Asn137) and human catalase (Asn148): mutations affect the rate but not the essential chemistry of the enzymatic transformations. Arch. Biochem. Biophys. 477:285-290.
37. Schneider, C., D. A. Pratt, N. A. Porter, and A. R. Brash. 2007. Control of oxygenation in lipoxygenase and cyclooxygenase catalysis. Chem. Biol. 14:473-488. (Pubitemid 46765155)
38. Hoffmann, I., M. Hamberg, R. Lindh, and E. H. Oliw. 2012. Novel insights into cyclooxygenases, linoleate diol synthases, and lipoxygenases from deuterium kinetic isotope effects and oxidation of substrate analogs. Biochim. Biophys. Acta. 1821:1508-1517.
39. Rickert, K. W., and J. P. Klinman. 1999. Nature of hydrogen transfer in soybean lipoxygenase 1: separation of primary and secondary isotope effects. Biochemistry. 38:12218-12228.
40. Clapp, C. H., S. E. Senchak, T. J. Stover, T. C. Potter, P. M. Findeis, and M. J. Novak. 2001. Soybean lipoxygenase-mediated oxygenation of monounsaturated fatty acids to enones. J. Am. Chem. Soc. 123:747-748. (Pubitemid 32106020)
41. Oliw, E. H., F. Jernerén, I. Hoffmann, M. Sahlin, and U. Garscha. 2011. Manganese lipoxygenase oxidizes bis-allylic hydroperoxides and octadecenoic acids by different mechanisms. Biochim. Biophys. Acta. 1811:138-147.
42. Wu, G., J. M. Lü, W. A. van der Donk, R. J. Kulmacz, and A. L. Tsai. 2011. Cyclooxygenase reaction mechanism of prostaglandin H synthase from deuterium kinetic isotope effects. J. Inorg. Biochem. 105:382-390.
43. Li, L., Z. Chang, Z. Pan, Z. Q. Fu, and X. Wang. 2008. Modes of heme binding and substrate access for cytochrome P450 CYP74A revealed by crystal structures of allene oxide synthase. Proc. Natl. Acad. Sci. USA. 105:13883-13888.
44. Brash, A. R., S. W. Baertschi, C. D. Ingram, and T. M. Harris. 1988. Isolation and characterization of natural allene oxides: unstable intermediates in the metabolism of lipid hydroperoxides. Proc. Natl. Acad. Sci. USA. 85:3382-3386.
45. Poulos, T. L. 2005. Structural biology of heme monooxygenases. Biochem. Biophys. Res. Commun. 338:337-345. (Pubitemid 41541970)