Identification of amino acid networks governing catalysis in the closed complex of class i terpene synthases

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 8, 2016, Pages E958-E967

  Schrepfer, Patrick ^a   Buettner, Alexander ^a   Goerner, Christian ^a   Hertel, Michael ^a   Rijn, Jeaphianne Van ^b   Wallrapp, Frank ^a   Eisenreich, Wolfgang ^a   Sieber, Volker ^a   Kourist, Robert ^c   Brück, Thomas ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUT FÜR KOHLENFORSCHUNG   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TAXADIENE SYNTHASE; TERPENE DERIVATIVE; UNCLASSIFIED DRUG; TERPENE SYNTHASE; TRANSFERASE;

AMINO ACID ANALYSIS; ARTICLE; CATALYSIS; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME LOCALIZATION; METHODOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN MOTIF; PROTEIN TARGETING; CHEMISTRY; MOLECULAR MODEL; PROCEDURES; SEQUENCE ANALYSIS;

ALKYL AND ARYL TRANSFERASES; AMINO ACID MOTIFS; CATALYSIS; CATALYTIC DOMAIN; MODELS, MOLECULAR; SEQUENCE ANALYSIS, PROTEIN;

EID: 84959386599     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1519680113     Document Type: Article

References (61)

1. Gao Y, Honzatko RB, Peters RJ (2012) Terpenoid synthase structures: A so far incomplete view of complex catalysis. Nat Prod Rep 29(10):1153-1175.
2. Cao R, et al. (2010) Diterpene cyclases and the nature of the isoprene fold. Proteins 78(11):2417-2432.
3. Wani MC, Taylor HL, Wall ME, Coggon P, McPhail AT (1971) Plant antitumor agents. VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 93(9):2325-2327.
4. Koepp AE, et al. (1995) Cyclization of geranylgeranyl diphosphate to taxa-4(5), 11(12)-diene is the committed step of taxol biosynthesis in Pacific yew. J Biol Chem 270(15):8686-8690.
5. Lin X, Hezari M, Koepp AE, Floss HG, Croteau R (1996) Mechanism of taxadiene synthase, a diterpene cyclase that catalyzes the first step of taxol biosynthesis in Pacific yew. Biochemistry 35(9):2968-2977.
6. Williams DC, et al. (2000) Heterologous expression and characterization of a "pseudomature" form of taxadiene synthase involved in paclitaxel (Taxol) biosynthesis and evaluation of a potential intermediate and inhibitors of the multistep diterpene cyclization reaction. Arch Biochem Biophys 379(1):137-146.
7. Williams DC, et al. (2000) Intramolecular proton transfer in the cyclization of geranylgeranyl diphosphate to the taxadiene precursor of Taxol catalyzed by recombinant taxadiene synthase. Chem Biol 7(12):969-977.
8. KöksalM, Jin Y, Coates RM, Croteau R, Christianson DW(2011) Taxadiene synthase structure and evolution of modular architecture in terpene biosynthesis. Nature 469(7328):116-120.
9. Jin Q, Williams DC, Hezari M, Croteau R, Coates RM (2005) Stereochemistry of the macrocyclization and elimination steps in taxadiene biosynthesis through deuterium labeling. J Org Chem 70(12):4667-4675.
10. Jin Y, Williams DC, Croteau R, Coates RM (2005) Taxadiene synthase-catalyzed cyclization of 6-fluorogeranylgeranyl diphosphate to 7-fluoroverticillenes. J Am Chem Soc 127(21):7834-7842.
11. Chow SY, Williams HJ, Huang Q, Nanda S, Scott AI (2005) Studies on taxadiene synthase: Interception of the cyclization cascade at the isocembrene stage with GGPP analogues. J Org Chem 70(24):9997-10003.
12. Chow SY, et al. (2007) Studies on taxadiene synthase: Interception of the cyclization cascade at the verticillene stage and rearrangement to phomactatriene. Tetrahedron 63(27):6204-6209.
13. Tokiwano T, et al. (2005) Proposed mechanism for diterpene synthases in the formation of phomactatriene and taxadiene. Org Biomol Chem 3(15):2713-2722.
14. Gutta P, Tantillo DJ (2007) A promiscuous proton in taxadiene biosynthesis? Org Lett 9(6):1069-1071.
15. Hong YJ, Tantillo DJ (2011) The taxadiene-forming carbocation cascade. J Am Chem Soc 133(45):18249-18256.
16. Kobayashi M, Kobayashi K, Nomura M, Munakata H (1990) Conformational study of the cembranoid sarcophytol A, a potent anti-Tumor-promoter. Chem Pharm Bull (Tokyo) 38(3):815-817.
17. Kobayashi M, Kondo K, Osabe K, Mitsuhashi H (1988) Marine terpenes and terpenoids. V. Oxidation of sarcophytol A, a potent anti-Tumor-promoter from the soft coral Sarcophyton glaucum. Chem Pharm Bull (Tokyo) 36(7):2331-2341.
18. Sugano M, et al. (1995) Phomactin E, F, and G: New phomactin-group PAF antagonists from a marine fungus Phoma sp. J Antibiot (Tokyo) 48(10):1188-1190
19. Sugano M, et al. (1996) Structure-Activity relationships of phomactin derivatives as platelet activating factor antagonists. J Med Chem 39(26):5281-5284.
20. Shen YC, et al. (2008) Cespihypotins Q-V, verticillene diterpenoids from Cespitularia hypotentaculata. J Nat Prod 71(12):1993-1997.
21. Major DT, WeitmanM(2012) Electrostatically guided dynamics-The root of fidelity in a promiscuous terpene synthase? J Am Chem Soc 134(47):19454-19462.
22. Christianson DW (2008) Unearthing the roots of the terpenome. Curr Opin Chem Biol 12(2):141-150.
23. Li R, et al. (2014) Reprogramming the chemodiversity of terpenoid cyclization by remolding the active site contour of epi-isozizaene synthase. Biochemistry 53(7): 1155-1168.
24. Zhou K, Peters RJ (2011) Electrostatic effects on (di)terpene synthase product outcome. Chem Commun (Camb) 47(14):4074-4080.
25. Srividya N, Davis EM, Croteau RB, Lange BM (2015) Functional analysis of (4S)-limonene synthase mutants reveals determinants of catalytic outcome in a model monoterpene synthase. Proc Natl Acad Sci USA 112(11):3332-3337.
26. Whittington DA, et al. (2002) Bornyl diphosphate synthase: Structure and strategy for carbocation manipulation by a terpenoid cyclase. Proc Natl Acad Sci USA 99(24): 15375-15380.
27. Shishova EY, Di Costanzo L, Cane DE, Christianson DW (2007) X-ray crystal structure of aristolochene synthase from Aspergillus terreus and evolution of templates for the cyclization of farnesyl diphosphate. Biochemistry 46(7):1941-1951.
28. Shishova EY, et al. (2008) X-ray crystallographic studies of substrate binding to aristolochene synthase suggest a metal ion binding sequence for catalysis. J Biol Chem 283(22):15431-15439.
29. Hyatt DC, et al. (2007) Structure of limonene synthase, a simple model for terpenoid cyclase catalysis. Proc Natl Acad Sci USA 104(13):5360-5365.
30. Hong YJ, Tantillo DJ (2009) A potential energy surface bifurcation in terpene biosynthesis. Nat Chem 1(5):384-389.
31. Hong YJ, Tantillo DJ (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(20):4589-4600.
32. Tantillo DJ (2011) Biosynthesis via carbocations: Theoretical studies on terpene formation. Nat Prod Rep 28(6):1035-1053.
33. Zhou K, et al. (2012) Insights into diterpene cyclization from structure of bifunctional abietadiene synthase from Abies grandis. J Biol Chem 287(9):6840-6850.
34. Keeling CI, Weisshaar S, Lin RPC, Bohlmann J (2008) Functional plasticity of paralogous diterpene synthases involved in conifer defense. Proc Natl Acad Sci USA 105(3): 1085-1090.
35. Nakano Y, et al. (2012) Characterization of the casbene synthase homolog from Jatropha. Plant Biotechnol 29:185-189.
36. Janke R, Görner C, Hirte M, Brück T, Loll B (2014) The first structure of a bacterial diterpene cyclase: CotB2. Acta Crystallogr D Biol Crystallogr 70(Pt 6):1528-1537.
37. Baer P, et al. (2014) Induced-fit mechanism in class I terpene cyclases. Angew Chem Int Ed Engl 53(29):7652-7656.
38. Rynkiewicz MJ, Cane DE, Christianson DW (2002) X-ray crystal structures of D100E trichodiene synthase and its pyrophosphate complex reveal the basis for terpene product diversity. Biochemistry 41(6):1732-1741.
39. Vedula LS, Cane DE, Christianson DW (2005) Role of arginine-304 in the diphosphatetriggered active site closure mechanism of trichodiene synthase. Biochemistry 44(38): 12719-12727.
40. Aaron JA, Lin X, Cane DE, Christianson DW (2010) Structure of epi-isozizaene synthase from Streptomyces coelicolor A3(2), a platform for new terpenoid cyclization templates. Biochemistry 49(8):1787-1797.
41. Cui H, Zhang ST, Yang HJ, Ji H, Wang XJ (2011) Gene expression profile analysis of tobacco leaf trichomes. BMC Plant Biol 11:76.
42. Drenth J, Jansonius JN, Koekoek R, Swen HM, Wolthers BG (1968) Structure of papain. Nature 218(5145):929-932.
43. Basar S, Koch A, KönigWA (2001) A verticillane-Type diterpene from Boswellia carterii essential oil. Flavour Fragrance J 16(5):315-318.
44. Xu M, Wilderman PR, Peters RJ (2007) Following evolution's lead to a single residue switch for diterpene synthase product outcome. Proc Natl Acad Sci USA 104(18): 7397-7401.
45. Morrone D, Xu M, Fulton DB, Determan MK, Peters RJ (2008) Increasing complexity of a diterpene synthase reaction with a single residue switch. J Am Chem Soc 130(16): 5400-5401.
46. Wilderman PR, Peters RJ (2007) A single residue switch converts abietadiene synthase into a pimaradiene specific cyclase. J Am Chem Soc 129(51):15736-15737.
47. Starks CM, Back K, Chappell J, Noel JP (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-Aristolochene synthase. Science 277(5333):1815-1820.
48. Lesburg CA, Caruthers JM, Paschall CM, Christianson DW (1998) Managing and manipulating carbocations in biology: Terpenoid cyclase structure and mechanism. Curr Opin Struct Biol 8(6):695-703.
49. Kirby J, et al. (2010) Cloning of casbene and neocembrene synthases from Euphorbiaceae plants and expression in Saccharomyces cerevisiae. Phytochemistry 71(13): 1466-1473.
50. Meguro A, Tomita T, Nishiyama M, Kuzuyama T (2013) Identification and characterization of bacterial diterpene cyclases that synthesize the cembrane skeleton. ChemBioChem 14(3):316-321.
51. Hong YJ, Tantillo DJ (2015) The energetic viability of an unexpected skeletal rearrangement in cyclooctatin biosynthesis. Org Biomol Chem 13(41):10273-10278.
52. Meguro A, et al. (2015) An unusual terpene cyclization mechanism involving a carboncarbon bond rearrangement. Angew Chem Int Ed Engl 54(14):4353-4356.
53. Görner C, Häuslein I, Schrepfer P, Eisenreich W, Brück T (2013) Targeted engineering of cyclooctat-9-en-7-ol synthase: A stereospecific access to two new non-natural fusicoccane-Type diterpenes. ChemCatChem 5(11):3289-3298.
54. Vedula LS, et al. (2005) Molecular recognition of the substrate diphosphate group governs product diversity in trichodiene synthase mutants. Biochemistry 44(16): 6153-6163.
55. Frisch MJ, et al. (2004) Gaussian 03, Revision (Gaussian, Inc., Wallingford, CT).
56. Krieger E, et al. (2009) Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 77(Suppl 9):114-122.
57. Jakalian A, Jack DB, Bayly CI (2002) Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation. J Comput Chem 23(16): 1623-1641.
58. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25(9):1157-1174.
59. Krieger E, Nielsen JE, Spronk CA, Vriend G (2006) Fast empirical pKa prediction by Ewald summation. J Mol Graph Model 25(4):481-486.
60. Trott O, Olson AJ (2010) AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455-461
61. Jung J, Lee B (2000) Protein structure alignment using environmental profiles. Protein Eng 13(8):535-543.