Structure of 2-methylisoborneol synthase from Streptomyces coelicolor and implications for the cyclization of a noncanonical C -methylated monoterpenoid substrate

Biochemistry

Volumn 51, Issue 14, 2012, Pages 3011-3020

  Köksal, Mustafa ^a   Chou, Wayne K W ^b   Cane, David E ^b   Christianson, David W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2-METHYLISOBORNEOL; BICYCLIC PRODUCTS; CATALYTIC MECHANISMS; CLASS I; CYCLASES; DIPHOSPHATES; FARNESYL DIPHOSPHATE SYNTHASE; ISOPRENOID SUBSTRATES; NATURALLY OCCURRING; QUATERNARY STRUCTURE; STREPTOMYCES COELICOLOR; STREPTOMYCES COELICOLOR A3(2); SYNTHASES; TERPENOIDS; TERTIARY STRUCTURES;

BACTERIA; CRYSTAL STRUCTURE; LIPIDS; STEREOCHEMISTRY;

CYCLIZATION;

2 METHYLGERANYL DIPHOSPHATE; 2 METHYLISOBORNEOL; 2 METHYLISOBORNEOL SYNTHASE; ADENYLATE CYCLASE; BACTERIAL ENZYME; FARNESYL DIPHOSPHATE; PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CYCLIZATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; STEREOCHEMISTRY; STREPTOMYCES COELICOLOR;

BACTERIAL PROTEINS; BINDING SITES; BORNANES; CRYSTALLOGRAPHY, X-RAY; CYCLIZATION; MODELS, MOLECULAR; MONOTERPENES; PROTEIN CONFORMATION; STREPTOMYCES COELICOLOR;

FUNGI; STREPTOMYCES COELICOLOR;

EID: 84859593281     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201827a     Document Type: Article

References (43)

1. Davis, E. M. and Croteau, R. (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes Top. Curr. Chem. 209, 53-95
2. Wendt, K. U., Schulz, G. E., Corey, E. J., and Liu, D. R. (2000) Enzyme mechanisms for polycyclic triterpene formation Angew. Chem., Int. Ed. 39, 2812-2833
3. Christianson, D. W. (2006) Structural biology and chemistry of the terpenoid cyclases Chem. Rev. 106, 3412-3442
4. Christianson, D. W. (2008) Unearthing the roots of the terpenome Curr. Opin. Chem. Biol. 12, 141-150
5. Allemann, R. K. (2008) Chemical wizardry? The generation of chemical diversity in terpenoid biosynthesis Pure Appl. Chem. 80, 1791-1798
6. Tantillo, D. J. (2010) The carbocation continuum in terpene biosynthesis - where are the secondary cations? Chem. Soc. Rev. 39, 2847-2854
7. Aaron, J. A. and Christianson, D. W. (2010) Trinuclear metal clusters in catalysis by terpenoid synthases Pure. Appl. Chem. 82, 1585-1597
8. Cane, D. E. and Ikeda, H. (2011) Exploration and mining of the bacterial terpenome Acc. Chem. Res. 45, 463-472
9. Cane, D. E. and Tsantrizos, Y. S. (1996) Aristolochene synthase. Elucidation of the cryptic germacrene A synthase activity using the anomalous substrate dihydrofarnesyl diphosphate J. Am. Chem. Soc. 118, 10037-10040
10. Miller, D. J., Yu, F., and Allemann, R. K. (2007) Aristolochene synthase-catalyzed cyclization of 2-fluorofarnesyl-diphosphate to 2-fluorogermacrene A ChemBioChem 8, 1819-1825
11. Miller, D. J., Yu, F., Knight, D. W., and Allemann, R. K. (2009) 6- and 14-Fluoro farnesyl diphosphate: mechanistic probes for the reaction catalysed by aristolochene synthase Org. Biomol. Chem. 7, 962-975
12. Vedula, L. S., Zhao, Y., Coates, R. M., Koyama, T., Cane, D. E., and Christianson, D. W. (2007) Exploring biosynthetic diversity with trichodiene synthase Arch. Biochem. Biophys. 466, 260-266
13. Buttery, R. G. and Garibaldi, J. A. (1976) Geosmin and methylisoborneol in garden soil J. Agric. Food Chem. 24, 1246-1247
14. Martin, J. F., Bennett, L. W., and Graham, W. H. (1988) Off-flavor in the channel catfish (Ictalurus punctatus) due to 2-methylisoborneol and its dehydration products Water Sci. Technol. 20, 99-105
15. McCallum, R., Pendleton, P., Schumann, R., and Trinh, M. U. (1998) Determination of geosmin and 2-methylisoborneol in water using solid-phase microextraction and gas chromatography-chemical ionisation/electron impact ionisation-ion-trap mass spectrometry Analyst 123, 2155-2160
16. Jüttner, F. and Watson, S. B. (2007) Biochemical and ecological control of geosmin and 2-methylisoborneol in source waters Appl. Environ. Microbiol. 73, 4395-4406
17. Karahadian, C., Josephson, D. B., and Lindsay, R. C. (1985) Volatile compounds from Penicillium sp. contributing musty-earthy notes to Brie and Camembert cheese flavors J. Agric. Food Chem. 33, 339-343
18. Wang, C. M. and Cane, D. E. (2008) Biochemistry and molecular genetics of the biosynthesis of the earthy odorant methylisoborneol in Streptomyces coelicolor J. Am. Chem. Soc. 130, 8908-8909
19. Komatsu, M., Tsuda, M., Omura, S., Oikawa, H., and Ikeda, H. (2008) Identification and functional analysis of genes controlling biosynthesis of 2-methylisoborneol Proc. Natl. Acad. Sci. U. S. A. 105, 7422-7427
20. Chou, W. K., Ikeda, H., and Cane, D. E. (2011) Cloning and characterization of Pfl-1841, a 2-methylenebornane synthase in Pseudomonas fluorescens PfO-1 Tetrahedron 67, 6627-6632
21. Giglio, S., Chou, W. K., Ikeda, H., Cane, D. E., and Monis, P. T. (2011) Biosynthesis of 2-methylisoborneol in cyanobacteria Environ. Sci. Technol. 45, 992-998
22. Wang, Z., Xu, Y., Shao, J., Wang, J., and Li, R. (2011) Genes associated with 2-methylisoborneol biosynthesis in cyanobacteria: isolation, characterization, and expression in response to light PLoS One 6, e18665
23. Cane, D. E., Saito, A., Croteau, R., Shaskus, J., and Felton, M. (1982) Enzymic cyclization of geranyl pyrophosphate to bornyl pyrophosphate. Role of the pyrophosphate moiety J. Am. Chem. Soc. 104, 5831-5833
24. Croteau, R. B., Shaskus, J. J., Renstrøm, B., Felton, N. M., Cane, D. E., Saito, A., and Chang, C. (1985) Mechanism of the pyrophosphate migration in the enzymic cyclization of geranyl and linalyl pyrophosphates to (+)- and (-)-bornyl pyrophosphates Biochemistry 24, 7077-7085
25. Croteau, R., Felton, N. M., and Wheeler, C. J. (1985) Stereochemistry at C-1 of geranyl pyrophosphate and neryl pyrophosphate in the cyclization to (+)- and (-)-bornyl pyrophosphate J. Biol. Chem. 260, 5956-5962
26. Wise, M. L., Pyun, H.-J., Helms, G., Assink, B., Coates, R. M., and Croteau, R. B. (2001) Stereochemical disposition of the geminal dimethyl groups in the enzymatic cyclization of geranyl diphosphate to (+)-bornyl diphosphate by recombinant (+)-bornyl diphosphate synthase from Salvia officinalis Tetrahedron 57, 5327-5334
27. Hyatt, D. C., Youn, B., Zhao, Y., Santhamma, B., Coates, R. M., Croteau, R. B., and Kang, C.-H. (2007) Structure of limonene synthase, a simple model for terpenoid cyclase catalysis Proc. Natl. Acad. Sci. U. S. A. 104, 5360-5365
28. Karp, F., Zhao, Y., Santhamma, B., Assink, B. K., Coates, R. M., and Croteau, R. B. (2007) Inhibition of monoterpene cyclases by inert analogues of geranyl diphosphate and linalyl diphosphate Arch. Biochem. Biophys. 468, 140-146
29. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
30. Pape, T. and Schneider, T. R. (2004) HKL2MAP: a graphical user interface for phasing with SHELX programs J. Appl. Crystallogr. 37, 843-844
31. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
32. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
33. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
34. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR System: A new software suite for macromolecular structure determination Acta Crystallogr. D54, 905-921
35. Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., and Jones, D. T. (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life J. Mol. Biol. 337, 635-645
36. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797
37. Tarshis, L. C., Yan, M., Poulter, C. D., and Sacchettini, J. C. (1994) Crystal structure of recombinant farnesyl diphosphate synthase at 2.6-Å resolution Biochemistry 33, 10871-10877
38. Shishova, E. Y., Yu, F., Miller, D. J., Faraldos, J. A., Zhao, Y., Coates, R. M., Allemann, R. K., Cane, D. E., and Christianson, D. W. (2008) X-ray crystallographic studies of substrate binding to aristolochene synthase suggest a metal ion binding sequence for catalysis J. Biol. Chem. 283, 15431-15439
39. Shishova, E. Y., Di Costanzo, L., Cane, D. E., and Christianson, D. W. (2007) X-ray crystal structure of aristolochene synthase from Aspergillus terreus and the evolution of templates for the cyclization of farnesyl diphosphate Biochemistry 46, 1941-1951
40. Whittington, D. A., Wise, M. L., Urbansky, M., Coates, R. M., Croteau, R. B., and Christianson, D. W. (2002) Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase Proc. Natl. Acad. Sci. U. S. A. 99, 15375-15380
41. 18O]geranyl pyrophosphate to l-endo -fenchol J. Am. Chem. Soc. 106, 1142-1143
42. Hong, Y. J. and Tantillo, D. J. (2010) Quantum chemical dissection of the classic terpinyl/pinyl/bornyl/camphyl cation conundrum-the role of pyrophosphate in manipulating pathways to monoterpenes Org. Biomol. Chem. 8, 4589-4600
43. Weitman, M. and Major, D. T. (2010) Challenges posed to bornyl diphosphate synthase: diverging reaction mechanisms in monoterpenes J. Am. Chem. Soc. 132, 6349-6360