Formation of a Novel Macrocyclic Alkaloid from the Unnatural Farnesyl Diphosphate Analogue Anilinogeranyl Diphosphate by 5-Epi-Aristolochene Synthase

ACS Chemical Biology

Volumn 10, Issue 7, 2015, Pages 1729-1736

  Rising, Kathleen A ^a   Crenshaw, Charisse M ^d   Koo, Hyun Jo ^d   Subramanian, Thangaiah ^b   Chehade, Kareem A H ^b   Starks, Courtney ^d   Allen, Keith D ^a   Andres, Douglas A ^b   Spielmann, H Peter ^a,b,c   Noel, Joseph P ^d   Chappell, Joe ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 EPI SRISTOLOCHENE SYNTHASE; ALKALOID DERIVATIVE; ANILINOGERANYL DIPHOSPHATE; ARISTOLOCHENE; MACROCYCLIC ALKALOID; PYROPHOSPHATE; PYROPHOSPHORIC ACID DERIVATIVE; UNCLASSIFIED DRUG; 5-EPI-ARISTOLOCHENE SYNTHASE; ALKALOID; FARNESYL DIPHOSPHATE; ISOPRENOID PHOSPHATE; MACROCYCLIC COMPOUND; SESQUITERPENE; TERPENE; TRANSFERASE;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CYCLIZATION; DRUG SYNTHESIS; ELECTROPHILICITY; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; HYDROGEN BOND; HYDROXYLATION; IONIZATION; MASS FRAGMENTOGRAPHY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; STATIC ELECTRICITY; STEROL SYNTHESIS; STRUCTURAL HOMOLOGY; TOBACCO; X RAY DIFFRACTION; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL;

NICOTIANA TABACUM;

ALKALOIDS; ALKYL AND ARYL TRANSFERASES; MACROCYCLIC COMPOUNDS; MODELS, MOLECULAR; POLYISOPRENYL PHOSPHATES; SESQUITERPENES; TERPENES; TOBACCO;

EID: 84937152625     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00145     Document Type: Article

References (35)

1. Christianson, D. W. (2006) Structural biology and chemistry of the terpenoid cyclases Chem. Rev. 106, 3412-3442
2. Davis, E. M. and Croteau, R. (2000) Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes Biosynthesis: Aromatic Polyketides, Isoprenoids, Alkaloids 209, 53-95
3. Connolly, J. D. and Hill, R. A. (1991) Dictionary of Terpenoids, Chapman & Hall, London.
4. Vogeli, U., Freeman, J. W., and Chappell, J. (1990) Purification and characterization of an inducible sesquiterpene cyclase from elicitor-treated tobacco cell-suspension cultures Plant Physiol. 93, 182-187
5. Takahashi, S., Zhao, Y. X., O'Maille, P. E., Greenhagen, B. T., Noel, J. P., Coates, R. M., and Chappell, J. (2005) Kinetic and molecular analysis of 5-epiaristolochene 1,3-dihydroxylase, a cytochrome P450 enzyme catalyzing successive hydroxylations of sesquiterpenes J. Biol. Chem. 280, 3686-3696
6. Newman, D. J. and Cragg, G. M. (2007) Natural products as sources of new drugs over the last 25 years J. Nat. Prod. 70, 461-477
7. Newman, D. J. and Cragg, G. M. (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010 J. Nat. Prod. 75, 311-335
8. Newman, D. J., Cragg, G. M., and Snader, K. M. (2003) Natural products as sources of new drugs over the period 1981-2002 J. Nat. Prod. 66, 1022-1037
9. Ortholand, J. Y. and Ganesan, A. (2004) Natural products and combinatorial chemistry: back to the future Cur. Opin. Chem. Biol. 8, 271-280
10. Driggers, E. M., Hale, S. P., Lee, J., and Terrett, N. K. (2008) The exploration of macrocycles for drug discovery-an underexploited structural class Nature Rev. Drug Discovery 7, 608-624
11. Mallinson, J. and Collins, I. (2012) Macrocycles in new drug discovery Future Med. Chem. 4, 1409-1438
12. Parenty, A., Moreau, X., and Campagne, J. M. (2006) Macrolactonizations in the total synthesis of natural products Chem. Rev. 106, 911-939
13. Wessjohann, L. A., Ruijter, E., Garcia-Rivera, D., and Brandt, W. (2005) What can a chemist learn from nature's macrocycles?-A brief, conceptual view Mol. Diversity 9, 171-186
14. Gradillas, A. and Perez-Castells, J. (2006) Macrocyclization by ring-closing metathesis in the total synthesis of natural products: Reaction conditions and limitations Angew. Chem., Int. Ed. 45, 6086-6101
15. March, J. (1992) Advanced Organic Chemistry: Reactions, Mechanisms, and Structure, 4 th ed., Wiley, New York.
16. Marsault, E. and Peterson, M. L. (2011) Macrocycles are great cycles: Applications, opportunities, and challenges of synthetic macrocycles in drug discovery J. Med. Chem. 54, 1961-2004
17. Monfette, S. and Fogg, D. E. (2009) Equilibrium ring-closing metathesis Chem. Rev. 109, 3783-3816
18. Rising, K. A., Starks, C. M., Noel, J. P., and Chappell, J. (2000) Demonstration of germacrene A as an intermediate in 5-epi-aristolochene synthase catalysis J. Am. Chem. Soc. 122, 6526-6526
19. Lee, H. Y., Yerkes, N., and O'Connor, S. E. (2009) Aza-tryptamine substrates in monoterpene indole alkaloid biosynthesis Chem. Biol. 16, 1225-1229
20. Chehade, K. A., Andres, D. A., Morimoto, H., and Spielmann, H. P. (2000) Design and synthesis of a transferable farnesyl pyrophosphate analogue to Ras by protein farnesyltransferase J. Org. Chem. 65, 3027-3033
21. Subramanian, T., Liu, S., Troutman, J. M., Andres, D. A., and Spielmann, H. P. (2008) Protein farnesyltransferase-catalyzed isoprenoid transfer to peptide depends on lipid size and shape, not hydrophobicity Chembiochem 9, 2872-2882
22. Troutman, J. M., Subramanian, T., Andres, D. A., and Spielmann, H. P. (2007) Selective modification of CaaX peptides with ortho-substituted anilinogeranyl lipids by protein farnesyl transferase: Competitive substrates and potent inhibitors from a library of farnesyl diphosphate analogues Biochemistry 46, 11310-11321
23. Chen, M., Knifley, T., Subramanian, T., Spielmann, H. P., and O'Connor, K. L. (2014) Use of synthetic isoprenoids to target protein prenylation and Rho GTPases in breast cancer invasion PloS One 9, e89892
24. Noel, J. P., Dellas, N., Faraldos, J. A., Zhao, M., Hess, B. A., Smentek, L., Coates, R. M., and O'Maille, P. E. (2010) Structural elucidation of cisoid and transoid cyclization pathways of a sesquiterpene synthase using 2-fluorofamesyl diphosphates ACS Chem. Biol. 5, 377-392
25. Starks, C. M., Back, K. W., Chappell, J., and Noel, J. P. (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase Science 277, 1815-1820
26. Greenhagen, B. T., O'Maille, P. E., Noel, J. P., and Chappell, J. (2006) Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases Proc. Natl. Acad. Sci. U.S.A. 103, 9826-9831
27. O'Maille, P. E., Chappell, J., and Noel, J. P. (2004) A single-vial analytical and quantitative gas chromatography-mass spectrometry assay for terpene synthases Anal. Biochem. 335, 210-217
28. Jahnke, W., Rondeau, J. M., Cotesta, S., Marzinzik, A., Pelle, X., Geiser, M., Strauss, A., Gotte, M., Bitsch, F., Hemmig, R., Henry, C., Lehmann, S., Glickman, J. F., Roddy, T. P., Stout, S. J., and Green, J. R. (2010) Allosteric non-bisphosphonate FPPS inhibitors identified by fragment-based discovery Nat. Chem. Biol. 6, 660-666
29. Mathis, J. R., Back, K., Starks, C., Noel, J., Poulter, C. D., and Chappell, J. (1997) Pre-steady-state study of recombinant sesquiterpene cyclases Biochemistry 36, 8340-8348
30. Whitehead, I. M., Threlfall, D. R., and Ewing, D. F. (1989) 5-Epi-aristolochene is a common precursor of the sesquiterpenoid phytoalexins capsidiol and debneyol Phytochemistry 28, 775-779
31. Cane, D. E. (1990) Enzymatic formation of sesquiterpenes Chem. Rev. 90, 1089-1103
32. Grimme, S., Pischel, I., Laufenberg, S., and Vogtle, F. (1998) Synthesis, structure, and chiroptical properties of the first 4-oxa[7]paracyclophane Chirality 10, 147-153
33. Adams, P. D., Afonine, P. V., Bunkoczi, 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., Sect. D: Biol. Crystallogr. 66, 213-221
34. Moriarty, N. W., Grosse-Kunstleve, R. W., and Adams, P. D. (2009) electronic Ligand Builder and Optimization Workbench (eLBOW): a tool for ligand coordinate and restraint generation Acta Crystallogr., Sect. D: Biol. Crystallogr. 65, 1074-1080
35. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132