Catalytic convergence of manganese and iron lipoxygenases by replacement of a single amino acid

Journal of Biological Chemistry

Volumn 287, Issue 38, 2012, Pages 31757-31765

  Wennman, Anneli ^a   Jernerén, Fredrik ^a   Hamberg, Mats ^b   Oliw, Ernst H ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN ABSTRACTION; HYDROPEROXIDES; HYDROPHOBIC RESIDUES; HYDROPHOBIC SUBSTRATE; LIPOXYGENASES; REGIOSPECIFICITY; STEREOSPECIFIC; STEREOSPECIFICITY;

ABSTRACTING; AMINO ACIDS; BIOMOLECULES; HYDROPHOBICITY; MANGANESE; METABOLITES; OXYGENATION; OXYGENATORS; PORPHYRINS; STEREOCHEMISTRY;

HYDROGEN;

ACID; ALANINE; AMINO ACID; GLYCINE; HISTIDINE; HYDROGEN; HYDROPEROXYOCTADECATRIENOIC ACID; IRON LIPOXYGENASE; ISOLEUCINE; LEUCINE; LIPOXYGENASE; MANGANESE LIPOXYGENASE; PHENYLALANINE; RECOMBINANT ENZYME; RECOMBINANT MANGANESE LIPOXYGENASE; UNCLASSIFIED DRUG; VALINE;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; ENZYME ACTIVITY; HYDROPHOBICITY; METABOLITE; MUTATION; OXIDATION; OXYGENATION; PRIORITY JOURNAL; PROTEIN MOTIF; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; ANTHOZOA; ARACHIDONATE LIPOXYGENASES; CATALYSIS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HUMANS; HYDROGEN; IRON; KINETICS; LIPOXYGENASE; MANGANESE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; OXYGEN; PICHIA; SEQUENCE HOMOLOGY, AMINO ACID; SOYBEANS;

GLYCINE MAX;

EID: 84866356189     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.364331     Document Type: Article

References (52)

1. Schneider, C., Pratt, D. A., Porter, N. A., and Brash, A. R. (2007) Control of oxygenation in lipoxygenase and cyclooxygenase catalysis. Chem. Biol. 14, 473-488 (Pubitemid 46765155)
2. Andreou, A., and Feussner, I. (2009) Lipoxygenases - structure and reaction mechanism. Phytochemistry 70, 1504-1510
3. Ivanov, I., Heydeck, D., Hofheinz, K., Roffeis, J., O'Donnell, V. B., Kuhn, H., and Walther, M. (2010) Molecular enzymology of lipoxygenases. Arch. Biochem. Biophys. 503, 161-174
4. Haeggström, J. Z., and Funk, C. D. (2011) Lipoxygenase and leukotriene pathways: biochemistry, biology, and roles in disease. Chem. Rev. 111, 5866-5898
5. Brodhun, F., and Feussner, I. (2011) Oxylipins in fungi. FEBS J. 278, 1047-1063
6. Duroudier, N. P., Tulah, A. S., and Sayers, I. (2009) Leukotriene pathway genetics and pharmacogenetics in allergy. Allergy 64, 823-839
7. Pidgeon, G. P., Lysaght, J., Krishnamoorthy, S., Reynolds, J. V., O'Byrne, K., Nie, D., and Honn, K. V. (2007) Lipoxygenase metabolism: roles in tumor progression and survival. Cancer Metastasis Rev. 26, 503-524 (Pubitemid 350115127)
8. Yoshida, H., and Kisugi, R. (2010) Mechanisms of LDL oxidation. Clin. Chim. Acta 411, 1875-1882
9. Gfeller, A., Dubugnon, L., Liechti, R., and Farmer, E. E. (2010) Jasmonate biochemical pathway. Sci. Signal. 3, cm3
10. Vicente, J., Cascón, T., Vicedo, B., García-Agustín, P., Hamberg, M., and Castresana, C. (2012) Role of 9-lipoxygenase and α-dioxygenase oxylipinpathways as modulators of local and systemic defense. Mol. Plant 5, 914-928
11. Cristea, M., Engström, Å., Su, C., Hörnsten, L., and Oliw, E. H. (2005) Expression of manganese lipoxygenase in Pichia pastoris and site-directed mutagenesis of putative metal ligands. Arch. Biochem. Biophys. 434, 201-211 (Pubitemid 40040485)
12. Liavonchanka, A., and Feussner, I. (2006) Lipoxygenases: occurrence, functions and catalysis. J. Plant Physiol. 163, 348-357 (Pubitemid 43112088)
13. Kuhn, H., Saam, J., Eibach, S., Holzhütter, H. G., Ivanov, I., and Walther, M. (2005) Structural biology of mammalian lipoxygenases: enzymatic consequences of targeted alterations of the protein structure. Biochem. Biophys. Res. Commun. 338, 93-101 (Pubitemid 41540542)
14. Youn, B., Sellhorn, G. E., Mirchel, R. J., Gaffney, B. J., Grimes, H. D., and Kang, C. (2006) Crystal structures of vegetative soybean lipoxygenase VLX-B and VLX-D, and comparisons with seed isoforms LOX-1 and LOX-3. Proteins 65, 1008-1020 (Pubitemid 44772897)
15. Gilbert, N. C., Bartlett, S. G., Waight, M. T., Neau, D. B., Boeglin, W. E., Brash, A. R., and Newcomer, M. E. (2011) The structure of human 5-lipoxygenase. Science 331, 217-219
16. Neau, D. B., Gilbert, N. C., Bartlett, S. G., Boeglin, W., Brash, A. R., and Newcomer, M. E. (2009) The 1.85 Å structure of an 8R-lipoxygenase suggests a general model for lipoxygenase product specificity. Biochemistry 48, 7906-7915
17. Gillmor, S. A., Villaseñor, A., Fletterick, R., Sigal, E., and Browner, M. F. (1997) The structure of mammalian 15-lipoxygenase reveals similarity to the lipases and the determinants of substrate specificity. Nat. Struct. Biol. 4, 1003-1009 (Pubitemid 27525804)
18. Gilbert, N. C., Rui, Z., Neau, D. B., Waight, M. T., Bartlett, S. G., Boeglin, W. E., Brash, A. R., and Newcomer, M. E. (2012) Conversion of human 5-lipoxygenase to a 15-lipoxygenase by a point mutation to mimic phosphorylation at serine-663. FASEB J. 26, 3222-3229
19. Garreta, A., Carpena i Vilella, X., Busquets Abió, M., Fusté Munné, M. C., Fita Rodríguez, I., and Manresa Presas, M. Á. (2011) in Recent Advances in Pharmaceutical Sciences (Muñoz-Torrero, D., ed) pp. 247-273, Transworld Research Network, Kerala, India
20. Sloane, D. L., Leung, R., Craik, C. S., and Sigal, E. (1991) A primary determinant for lipoxygenase positional specificity. Nature 354, 149-152 (Pubitemid 21896799)
21. Schwarz, K., Gerth, C., Anton, M., and Kuhn, H. (2000) Alterations in leukotriene synthase activity of the human 5-lipoxygenase by site-directed mutagenesis affecting its positional specificity. Biochemistry 39, 14515-14521
22. Jisaka, M., Kim, R. B., Boeglin, W. E., and Brash, A. R. (2000) Identification of amino acid determinants of the positional specificity of mouse 8S-lipoxygenase and human 15S-lipoxygenase-2. J. Biol. Chem. 275, 1287-1293 (Pubitemid 30051183)
23. Hughes, R. K., Lawson, D. M., Hornostaj, A. R., Fairhurst, S. A., and Casey, R. (2001) Mutagenesis and modelling of linoleate-binding to pea seed lipoxygenase. Eur. J. Biochem. 268, 1030-1040 (Pubitemid 32328347)
24. Schwarz, K., Walther, M., Anton, M., Gerth, C., Feussner, I., and Kuhn, H. (2001) Structural basis for lipoxygenase specificity. Conversion of the human leukocyte 5-lipoxygenase to a 15-lipoxygenating enzyme species by site-directed mutagenesis. J. Biol. Chem. 276, 773-779 (Pubitemid 32050377)
25. Meruvu, S., Walther, M., Ivanov, I., Hammarström, S., Fürstenberger, G., Krieg, P., Reddanna, P., and Kuhn, H. (2005) Sequence determinants for reaction specificity of the murine 12(R)-lipoxygenase. Targeted substrate modification and site directed mutagenesis. J. Biol. Chem. 280, 36633-36641 (Pubitemid 41587740)
26. Hamberg, M., Su, C., and Oliw, E. (1998) Manganese lipoxygenase. Discovery of a bis-allylic hydroperoxide as product and intermediate in a lipoxygenase reaction. J. Biol. Chem. 273, 13080-13088 (Pubitemid 28246874)
27. Andreou, A., Göbel, C., Hamberg, M., and Feussner, I. (2010) A bisallylic mini-lipoxygenase from cyanobacterium Cyanothece sp. that has an iron as cofactor. J. Biol. Chem. 285, 14178-14186
28. Su, C., and Oliw, E. H. (1998) Manganese lipoxygenase. Purification and characterization. J. Biol. Chem. 273, 13072-13079 (Pubitemid 28246873)
29. Hörnsten, L., Su, C., Osbourn, A. E., Hellman, U., and Oliw, E. H. (2002) Cloning of the manganese lipoxygenase gene reveals homology with the lipoxygenase gene family. Eur. J. Biochem. 269, 2690-2697 (Pubitemid 34595635)
30. Oliw, E. H., Jernerén, F., Hoffmann, I., Sahlin, M., and Garscha, U. (2011) Manganese lipoxygenase oxidizes bis-allylic hydroperoxides and octadecenoic acids by different mechanisms. Biochim. Biophys. Acta 1811, 138-147
31. Goldsmith, C. R., and Stack, T. D. (2006) Hydrogen atom abstraction by a mononuclear ferric hydroxide complex: insights into the reactivity of lipoxygenase. Inorg. Chem. 45, 6048-6055
32. Hamberg, M. (1971) Steric analysis of hydroperoxides formed by lipoxygenase oxygenation of linoleic acid. Anal. Biochem. 43, 515-526
33. Rickert, K. W., and Klinman, J. P. (1999) Nature of hydrogen transfer in soybean lipoxygenase 1: separation of primary and secondary isotope effects. Biochemistry 38, 12218-12228
34. Coffa, G., and Brash, A. R. (2004) A single active site residue directs oxygenation stereospecificity in lipoxygenases: stereocontrol is linked to the position of oxygenation. Proc. Natl. Acad. Sci. U.S.A. 101, 15579-15584 (Pubitemid 39473530)
35. Haas, U., Raschperger, E., Hamberg, M., Samuelsson, B., Tryggvason, K., and Haeggström, J. Z. (2011) Targeted knock-down of a structurally atypical zebrafish 12S-lipoxygenase leads to severe impairment of embryonic development. Proc. Natl. Acad. Sci. U.S.A. 108, 20479-20484
36. Jansen, C., Hofheinz, K., Vogel, R., Roffeis, J., Anton, M., Reddanna, P., Kuhn, H., and Walther, M. (2011) Stereocontrol of arachidonic acid oxygenation by vertebrate lipoxygenases. Newly cloned zebrafish lipoxygenase 1 does not follow the Ala-versus-Gly concept. J. Biol. Chem. 286, 37804-37812
37. Zheng, Y., and Brash, A. R. (2010) On the role of molecular oxygen in lipoxygenase activation: comparison and contrast of epidermal lipoxygenase-3 with soybean lipoxygenase-1. J. Biol. Chem. 285, 39876-39887
38. Cristea, M., and Oliw, E. H. (2006) A G316A mutation of manganese lipoxygenase augments hydroperoxide isomerase activity: mechanism of biosynthesis of epoxyalcohols. J. Biol. Chem. 281, 17612-17623 (Pubitemid 44035560)
39. Walther, M., Hofheinz, K., Vogel, R., Roffeis, J., and Kühn, H. (2011) The N-terminal β-barrel domain of mammalian lipoxygenases includingmouse 5-lipoxygenase is not essential for catalytic activity and membrane binding but exhibits regulatory functions. Arch. Biochem. Biophys. 516, 1-9
40. Oliw, E. H. (2008) Factors influencing the rearrangement of bis-allylic hydroperoxides by manganese lipoxygenase. J. Lipid Res. 49, 420-428
41. Hamberg, M. (2011) Stereochemistry of hydrogen removal during oxygenation of linoleic acid by singlet oxygen and synthesis of 11(S)-deuterium-labeled linoleic acid. Lipids 46, 201-206
42. Cheng, H. R., and Jiang, N. (2006) Extremely rapid extraction of DNA from bacteria and yeasts. Biotechnol. Lett. 28, 55-59
43. Leber, A., Hemmens, B., Klösch, B., Goessler, W., Raber, G., Mayer, B., and Schmidt, K. (1999) Characterization of recombinant human endothelial nitric-oxide synthase purified from the yeast Pichia pastoris. J. Biol. Chem. 274, 37658-37664 (Pubitemid 30026823)
44. McClellan, J. E., Murphy, J. P., 3rd, Mulholland, J. J., and Yost, R. A. (2002) Effects of fragile ions on mass resolution and on isolation for tandem mass spectrometry in the quadrupole ion trap mass spectrometer. Anal. Chem. 74, 402-412 (Pubitemid 34072707)
45. Garscha, U., Nilsson, T., and Oliw, E. H. (2008) Enantiomeric separation and analysis of unsaturated hydroperoxy fatty acids by chiral column chromatography-mass spectrometry. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 872, 90-98
46. Schneider, C., Yu, Z., Boeglin, W. E., Zheng, Y., and Brash, A. R. (2007) Enantiomeric separation of hydroxy and hydroperoxy eicosanoids by chiral column chromatography. Methods Enzymol. 433, 145-157
47. Hellman, U., Wernstedt, C., Góñez, J., and Heldin, C. H. (1995) Improvement of an "In-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224, 451-455
48. Vogel, R., Jansen, C., Roffeis, J., Reddanna, P., Forsell, P., Claesson, H. E., Kuhn, H., and Walther, M. (2010) Applicability of the triad concept for the positional specificity of mammalian lipoxygenases. J. Biol. Chem. 285, 5369-5376
49. Gardner, H. W. (1989) Soybean lipoxygenase-1 enzymically forms both (9S)- and (13S)-hydroperoxides from linoleic acid by a pH-dependent mechanism. Biochim. Biophys. Acta 1001, 274-281
50. Hornung, E., Walther, M., Kühn, H., and Feussner, I. (1999) Conversion of cucumber linoleate 13-lipoxygenase to a 9-lipoxygenating species by site-directed mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 96, 4192-4197 (Pubitemid 29169059)
51. Zheng, Y., and Brash, A. R. (2010) Dioxygenase activity of epidermal lipoxygenase-3 unveiled: typical and atypical features of its catalytic activity with natural and synthetic polyunsaturated fatty acids. J. Biol. Chem. 285, 39866-39875
52. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (Pubitemid 43205406)