skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Mechanism-Based Post-Translational Modification and Inactivation in Terpene Synthases

Journal Article · · ACS Chemical Biology
 [1];  [2];  [2];  [1]
  1. Howard Hughes Medical Institute, Jack H. Skirball Center for Chemical Biology & Proteomics, The Salk Institute for Biological Studies, La Jolla, California 92037, United States
  2. Department of Chemical Physiology, The Scripps Research Institute, La Jolla, California 92037, United States, Vincent J. Coates Mass Spectrometry Center, The Salk Institute of Biological Studies, La Jolla, California 92037, United States

Terpenes are ubiquitous natural chemicals with diverse biological functions spanning all three domains of life. In specialized metabolism, the active sites of terpene synthases (TPSs) evolve in shape and reactivity to direct the biosynthesis of a myriad of chemotypes for organismal fitness. As most terpene biosynthesis mechanistically involves highly reactive carbocationic intermediates, the protein surfaces catalyzing these cascade reactions possess reactive regions possibly prone to premature carbocation capture and potentially enzyme inactivation. Here, we show using proteomic and X-ray crystallographic analyses that cationic intermediates undergo capture by conserved active site residues leading to inhibitory self-alkylation. Furthermore, the level of cation-mediated inactivation increases with mutation of the active site, upon changes in the size and structure of isoprenoid diphosphate substrates, and alongside increases in reaction temperatures. TPSs that individually synthesize multiple products are less prone to self-alkylation then TPSs possessing relatively high product specificity. In total, the results presented suggest that mechanism-based alkylation represents an overlooked mechanistic pressure during the evolution of cation-derived terpene biosynthesis.

Research Organization:
Salk Inst. for Biological Studies, La Jolla, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
AC02-693-05CH11231; AC02-05CH11231
OSTI ID:
1221692
Alternate ID(s):
OSTI ID: 1345035
Journal Information:
ACS Chemical Biology, Journal Name: ACS Chemical Biology Vol. 10 Journal Issue: 11; ISSN 1554-8929
Publisher:
American Chemical SocietyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 15 works
Citation information provided by
Web of Science

References (44)

Toward Full Peptide Sequence Coverage by Dual Fragmentation Combining Electron-Transfer and Higher-Energy Collision Dissociation Tandem Mass Spectrometry journal October 2012
Crystal Structure of Pentalenene Synthase: Mechanistic Insights on Terpenoid Cyclization Reactions in Biology journal September 1997
Suicide substrates: mechanism-based enzyme inactivators journal January 1982
The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’ journal March 2010
Cloning and Bacterial Expression of a Sesquiterpene Cyclase from Hyoscyamus muticus and Its Molecular Comparison to Related Terpene Cyclases journal March 1995
Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases journal June 2006
Purification and characterization of the sesquiterpene cyclase patchoulol synthase from Pogostemon cablin journal October 1990
Production and quantification of sesquiterpenes in Saccharomyces cerevisiae, including extraction, detection and quantification of terpene products and key related metabolites journal July 2014
Artemisinins target the SERCA of Plasmodium falciparum journal August 2003
Trinuclear metal clusters in catalysis by terpenoid synthases journal May 2010
A single-vial analytical and quantitative gas chromatography–mass spectrometry assay for terpene synthases journal December 2004
Cation-pi Interactions in Chemistry and Biology: A New View of Benzene, Phe, Tyr, and Trp journal January 1996
One-Pot Enzymatic Synthesis of Merochlorin A and B journal August 2014
Enzymes of the Cyclooxygenase Pathways of Prostanoid Biosynthesis journal October 2011
Terpenoid synthase structures: a so far incomplete view of complex catalysis journal January 2012
The tobacco genome sequence and its comparison with those of tomato and potato journal May 2014
The fate of duplicated genes in a polyploid plant genome journal October 2012
Biosynthesis of the earthy odorant geosmin by a bifunctional Streptomyces coelicolor enzyme journal September 2007
The function of terpene natural products in the natural world journal June 2007
Evolving biosynthetic tangos negotiate mechanistic landscapes journal April 2008
Sterols and membrane dynamics journal September 2008
JLigand : a graphical tool for the CCP 4 template-restraint library journal March 2012
Emergence of terpene cyclization in Artemisia annua journal February 2015
Conformational Change and Ligand Binding in the Aristolochene Synthase Catalytic Cycle journal October 2013
Aristolochene Synthase. Mechanism-Based Inhibition of a Terpenoid Cyclase journal December 1994
High-Throughput Screening for Terpene-Synthase-Cyclization Activity and Directed Evolution of a Terpene Synthase journal March 2013
A High-Throughput Colorimetric Screening Assay for Terpene Synthase Activity Based on Substrate Consumption journal March 2014
Merochlorins A–D, Cyclic Meroterpenoid Antibiotics Biosynthesized in Divergent Pathways with Vanadium-Dependent Chloroperoxidases journal July 2012
A Multitasking Vanadium-Dependent Chloroperoxidase as an Inspiration for the Chemical Synthesis of the Merochlorins journal August 2014
Biosynthesis via carbocations: Theoretical studies on terpene formation journal January 2011
Citrus fruit flavor and aroma biosynthesis: isolation, functional characterization, and developmental regulation of Cstps1 , a key gene in the production of the sesquiterpene aroma compound valencene: Characterization and regulation of valencene synthase journal October 2003
Chemical wizardry? The generation of diversity in terpenoid biosynthesis journal January 2008
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Mechanistic Insights from the Binding of Substrate and Carbocation Intermediate Analogues to Aristolochene Synthase journal July 2013
Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases journal September 2008
Oxygenation of polyunsaturated fatty acids during prostaglandin biosynthesis by sheep vesicular glands journal August 1972
Designed divergent evolution of enzyme function journal February 2006
A Mutation in Para-Hydroxybenzoate-Polyprenyl Transferase (COQ2) Causes Primary Coenzyme Q10 Deficiency journal February 2006
Plant SILAC: Stable-Isotope Labelling with Amino Acids of Arabidopsis Seedlings for Quantitative Proteomics journal August 2013
Induced-Fit Mechanism in Class I Terpene Cyclases journal May 2014
The Rise of Chemodiversity in Plants journal June 2012
Structural Basis for Cyclic Terpene Biosynthesis by Tobacco 5-Epi-Aristolochene Synthase journal September 1997
CAAX Geranylgeranyl Transferase Transfers Farnesyl as Efficiently as Geranylgeranyl to RhoB journal April 1995
Xanthones from Hypericum roeperanum journal September 1996

Similar Records

Mechanism of Action and Inhibition of dehydrosqualene Synthase
Journal Article · Sat Dec 31 00:00:00 EST 2011 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1221692

Determinants of Selectivity for the Formation of Monocyclic and Bicyclic Products in Monoterpene Synthases
Journal Article · Wed Jun 08 00:00:00 EDT 2022 · ACS Catalysis · OSTI ID:1221692

Taxadiene Synthase Structure and Evolution of Modular Architecture in Terpene Biosynthesis
Journal Article · Sat Dec 31 00:00:00 EST 2011 · Nature · OSTI ID:1221692