The crystal structure of α-dioxygenase provides insight into diversity in the cyclooxygenase-peroxidase superfamily

Biochemistry

Volumn 52, Issue 8, 2013, Pages 1364-1372

  Goulah, Christopher C ^a   Zhu, Guangyu ^a   Koszelak Rosenblum, Mary ^a   Malkowski, Michael G ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ARABIDOPSIS THALIANA; CARBOXYLATE GROUPS; CATALYTIC DOMAINS; CHLORIDE IONS; CYCLOOXYGENASES; DEGREE OF SIMILARITY; DIOXYGENASES; HEME BINDING; HYDROPEROXIDES; KINETIC ANALYSIS; LOW DEGREE; LOW LEVEL; PEROXIDASE ACTIVITIES; SEQUENCE IDENTITY; STRUCTURAL HOMOLOGY; TWO DOMAINS; TYROSYL RADICALS; X RAY CRYSTAL STRUCTURES;

AMINO ACIDS; CARBOXYLATION; CATALYSIS; CHLORINE COMPOUNDS; ENZYMES;

PORPHYRINS;

ALPHA DIOXYGENASE; ARGININE; CARBOXYL GROUP; CHLORIDE ION; DIOXYGENASE; FATTY ACID; HEME; HISTIDINE; PEROXIDASE; PROSTAGLANDIN SYNTHASE; THREONINE; TYROSINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARABIDOPSIS; ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; MEMBRANE BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; STRUCTURAL HOMOLOGY; X RAY CRYSTALLOGRAPHY;

ANIMALS; ARABIDOPSIS; BINDING SITES; CALCIUM; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DIOXYGENASES; HEME; MICE; MODELS, MOLECULAR; PEROXIDASE; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84874413608     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400013k     Document Type: Article

References (38)

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
2. Lopez, M. A., Bannenberg, G., and Castresana, C. (2008) Controlling hormone signaling is a plant and pathogen challenge for growth and survival Curr. Opin. Plant Biol. 11, 420-427
3. Blee, E. (2002) Impact of phyto-oxylipins in plant defense Trends Plant Sci. 7, 315-322
4. Funk, C. D. (2001) Prostaglandins and leukotrienes: Advances in eicosanoid biology Science 294, 1871-1875
5. Sanz, A., Moreno, J. I., and Castresana, C. (1998) PIOX, a new pathogen-induced oxygenase with homology to animal cyclooxygenase Plant Cell 10, 1523-1537
6. Hamberg, M., Ponce de Leon, I., Sanz, A., and Castresana, C. (2002) Fatty acid α-dioxygenases Prostaglandins Other Lipid Mediators 68-69, 363-374
7. Zamocky, M., Jakopitsch, C., Furtmuller, P. G., Dunand, C., and Obinger, C. (2008) The peroxidase-cyclooxygenase superfamily: Reconstructed evolution of critical enzymes of the innate immune system Proteins 72, 589-605
8. Hamberg, M., Sanz, A., and Castresana, C. (1999) α-Oxidation of fatty acids in higher plants J. Biol. Chem. 274, 24503-24513
9. Koszelak-Rosenblum, M., Krol, A. C., Simmons, D. M., Goulah, C. C., Wroblewski, L., and Malkowski, M. G. (2008) His-311 and Arg-559 are key residues involved in fatty acid oxygenation in pathogen-inducible oxygenase J. Biol. Chem. 283, 24962-24971
10. Liu, W., Rogge, C. E., Bambai, B., Palmer, G., Tsai, A. L., and Kulmacz, R. J. (2004) Characterization of the heme environment in Arabidopsis thaliana fatty acid α-dioxygenase-1 J. Biol. Chem. 279, 29805-29815
11. Mancia, F. and Love, J. (2010) High-throughput expression and purification of membrane proteins J. Struct. Biol. 172, 85-93
12. Koszelak-Rosenblum, M., Krol, A., Mozumdar, N., Wunsch, K., Ferin, A., Cook, E., Veatch, C. K., Nagel, R., Luft, J. R., Detitta, G. T., and Malkowski, M. G. (2009) Determination and application of empirically derived detergent phase boundaries to effectively crystallize membrane proteins Protein Sci. 18, 1828-1839
13. Luft, J. R., Snell, E. H., and DeTitta, G. T. (2011) Lessons from high-throughput protein crystallization screening: 10 years of practical experience Expert Opin. Drug Discovery 6, 465-480
14. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. In Methods in Enzymology (Carter, C. W., Jr. and Sweet, R. M., Eds.) pp 307-326, Academic Press, New York.
15. Sheldrick, G. M. (2008) A short history of SHELX Acta Crystallogr. A64, 112-122
16. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
17. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 3, 1171-1179
18. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
19. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
20. Winn, M. C., Isupov, M. N., and Murshudov, G. (2000) Use of TLS parameters to model anisotrophic displacements in macromolecular refinement Acta Crystallogr. D57, 122-133
21. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., III, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35, W375-W383
22. Kleywegt, G. J. and Jones, T. A. (1994) Detection, delineation, measurement and display of cavities in macromolecular structures Acta Crystallogr. D50, 178-185
23. The PyMOL Molecular Graphics System, version 1.3r1 (2010) Schrodinger, LLC, New York.
24. Liu, W., Wang, L. H., Fabian, P., Hayashi, Y., McGinley, C. M., van der Donk, W. A., and Kulmacz, R. J. (2006) Arabidopsis thaliana fatty acid α-dioxygenase-1: Evaluation of substrates, inhibitors and amino-terminal function Plant Physiol. Biochem. 44, 284-293
25. Hamberg, M., Sanz, A., and Castresana, C. (2002) α-Dioxygenase, a new enzyme in fatty acid metabolism Int. Congr. Ser. 1233, 307-317
26. Malkowski, M. G., Ginell, S. L., Smith, W. L., and Garavito, R. M. (2000) The productive conformation of arachidonic acid bound to prostaglandin synthase Science 289, 1933-1937
27. Vecchio, A. J., Simmons, D. M., and Malkowski, M. G. (2010) Structural basis of fatty acid substrate binding to cyclooxygenase-2 J. Biol. Chem. 285, 22152-22163
28. Malkowski, M. G., Theisen, M. J., Scharmen, A., and Garavito, R. M. (2000) The formation of stable fatty acid substrate complexes in prostaglandin H(2) synthase-1 Arch. Biochem. Biophys. 380, 39-45
29. Furtmuller, P. G., Zederbauer, M., Jantschko, W., Helm, J., Bogner, M., Jakopitsch, C., and Obinger, C. (2006) Active site structure and catalytic mechanisms of human peroxidases Arch. Biochem. Biophys. 445, 199-213
30. Picot, D., Loll, P. J., and Garavito, R. M. (1994) The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1 Nature 367, 243-249
31. Vecchio, A. J., Orlando, B. J., Nandagiri, R., and Malkowski, M. G. (2012) Investigating substrate promiscuity in cyclooxygenase-2: The role of Arg-120 and residues lining the hydrophobic groove J. Biol. Chem. 287, 24619-24630
32. Thuresson, E. D., Lakkides, K. M., Rieke, C. J., Sun, Y., Wingerd, B. A., Micielli, R., Mulichak, A. M., Malkowski, M. G., Garavito, R. M., and Smith, W. L. (2001) Prostaglandin endoperoxide H synthase-1: The functions of cyclooxygenase active site residues in the binding, positioning, and oxygenation of arachidonic acid J. Biol. Chem. 276, 10347-10357
33. Landino, L. M., Crews, B. C., Gierse, J. K., Hauser, S. D., and Marnett, L. J. (1997) Mutational analysis of the role of the distal histidine and glutamine residues of prostaglandin-endoperoxide synthase-2 in peroxidase catalysis, hydroperoxide reduction, and cyclooxygenase activation J. Biol. Chem. 272, 21565-21574
34. Koeduka, T., Matsui, K., Akakabe, Y., and Kajiwara, T. (2002) Catalytic properties of rice α-oxygenase J. Biol. Chem. 277, 22648-22655
35. Mukherjee, A., Angeles-Boza, A. M., Huff, G. S., and Roth, J. P. (2011) Catalytic mechanism of a heme and tyrosyl radical-containing fatty acid α-(di)oxygenase J. Am. Chem. Soc. 133, 227-238
36. Garavito, R. M., Malkowski, M. G., and DeWitt, D. L. (2002) The structures of prostaglandin endoperoxide H synthases-1 and -2 Prostaglandins Other Lipid Mediators 68-69, 129-152
37. Dong, L., Vecchio, A. J., Sharma, N. P., Jurban, B. J., Malkowski, M. G., and Smith, W. L. (2011) Human Cyclooxygenase-2 Is a Sequence Homodimer That Functions as a Conformational Heterodimer J. Biol. Chem. 286, 19035-19046
38. Evans, P. (2006) Scaling and assessment of data quality Acta Crystallogr. D62, 72-82