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A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules

Plants are an excellent source of drug leads. However availability is limited by access to source species, low abundance and recalcitrance to chemical synthesis. Although plant genomics is yielding a wealth of genes for natural product biosynthesis, the translation of this genetic information into s...

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Autores principales: Reed, James, Stephenson, Michael J., Miettinen, Karel, Brouwer, Bastiaan, Leveau, Aymeric, Brett, Paul, Goss, Rebecca J.M., Goossens, Alain, O’Connell, Maria A., Osbourn, Anne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Academic Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5555447/
https://www.ncbi.nlm.nih.gov/pubmed/28687337
http://dx.doi.org/10.1016/j.ymben.2017.06.012
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author Reed, James
Stephenson, Michael J.
Miettinen, Karel
Brouwer, Bastiaan
Leveau, Aymeric
Brett, Paul
Goss, Rebecca J.M.
Goossens, Alain
O’Connell, Maria A.
Osbourn, Anne
author_facet Reed, James
Stephenson, Michael J.
Miettinen, Karel
Brouwer, Bastiaan
Leveau, Aymeric
Brett, Paul
Goss, Rebecca J.M.
Goossens, Alain
O’Connell, Maria A.
Osbourn, Anne
author_sort Reed, James
collection PubMed
description Plants are an excellent source of drug leads. However availability is limited by access to source species, low abundance and recalcitrance to chemical synthesis. Although plant genomics is yielding a wealth of genes for natural product biosynthesis, the translation of this genetic information into small molecules for evaluation as drug leads represents a major bottleneck. For example, the yeast platform for artemisinic acid production is estimated to have taken >150 person years to develop. Here we demonstrate the power of plant transient transfection technology for rapid, scalable biosynthesis and isolation of triterpenes, one of the largest and most structurally diverse families of plant natural products. Using pathway engineering and improved agro-infiltration methodology we are able to generate gram-scale quantities of purified triterpene in just a few weeks. In contrast to heterologous expression in microbes, this system does not depend on re-engineering of the host. We next exploit agro-infection for quick and easy combinatorial biosynthesis without the need for generation of multi-gene constructs, so affording an easy entrée to suites of molecules, some new-to-nature, that are recalcitrant to chemical synthesis. We use this platform to purify a suite of bespoke triterpene analogs and demonstrate differences in anti-proliferative and anti-inflammatory activity in bioassays, providing proof of concept of this system for accessing and evaluating medicinally important bioactives. Together with new genome mining algorithms for plant pathway discovery and advances in plant synthetic biology, this advance provides new routes to synthesize and access previously inaccessible natural products and analogs and has the potential to reinvigorate drug discovery pipelines.
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spelling pubmed-55554472017-08-22 A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules Reed, James Stephenson, Michael J. Miettinen, Karel Brouwer, Bastiaan Leveau, Aymeric Brett, Paul Goss, Rebecca J.M. Goossens, Alain O’Connell, Maria A. Osbourn, Anne Metab Eng Article Plants are an excellent source of drug leads. However availability is limited by access to source species, low abundance and recalcitrance to chemical synthesis. Although plant genomics is yielding a wealth of genes for natural product biosynthesis, the translation of this genetic information into small molecules for evaluation as drug leads represents a major bottleneck. For example, the yeast platform for artemisinic acid production is estimated to have taken >150 person years to develop. Here we demonstrate the power of plant transient transfection technology for rapid, scalable biosynthesis and isolation of triterpenes, one of the largest and most structurally diverse families of plant natural products. Using pathway engineering and improved agro-infiltration methodology we are able to generate gram-scale quantities of purified triterpene in just a few weeks. In contrast to heterologous expression in microbes, this system does not depend on re-engineering of the host. We next exploit agro-infection for quick and easy combinatorial biosynthesis without the need for generation of multi-gene constructs, so affording an easy entrée to suites of molecules, some new-to-nature, that are recalcitrant to chemical synthesis. We use this platform to purify a suite of bespoke triterpene analogs and demonstrate differences in anti-proliferative and anti-inflammatory activity in bioassays, providing proof of concept of this system for accessing and evaluating medicinally important bioactives. Together with new genome mining algorithms for plant pathway discovery and advances in plant synthetic biology, this advance provides new routes to synthesize and access previously inaccessible natural products and analogs and has the potential to reinvigorate drug discovery pipelines. Academic Press 2017-07 /pmc/articles/PMC5555447/ /pubmed/28687337 http://dx.doi.org/10.1016/j.ymben.2017.06.012 Text en © 2017 The Authors. International Metabolic Engineering Society. Published by Elsevier Inc. http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Reed, James
Stephenson, Michael J.
Miettinen, Karel
Brouwer, Bastiaan
Leveau, Aymeric
Brett, Paul
Goss, Rebecca J.M.
Goossens, Alain
O’Connell, Maria A.
Osbourn, Anne
A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules
title A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules
title_full A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules
title_fullStr A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules
title_full_unstemmed A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules
title_short A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules
title_sort translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like molecules
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5555447/
https://www.ncbi.nlm.nih.gov/pubmed/28687337
http://dx.doi.org/10.1016/j.ymben.2017.06.012
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