Synthesis facilitates an understanding of the structural basis for translation inhibition by the lissoclimides

The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and analogue-oriented synthesis approaches provide a series of lissoclimide natural products and analogues that expand the structure–activity relationships (S...

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Veröffentlicht in:Nature chemistry Jg. 9; H. 11; S. 1140 - 1149
Hauptverfasser: Könst, Zef A., Szklarski, Anne R., Pellegrino, Simone, Michalak, Sharon E., Meyer, Mélanie, Zanette, Camila, Cencic, Regina, Nam, Sangkil, Voora, Vamsee K., Horne, David A., Pelletier, Jerry, Mobley, David L., Yusupova, Gulnara, Yusupov, Marat, Vanderwal, Christopher D.
Format: Journal Article
Sprache:Englisch
Veröffentlicht: London Nature Publishing Group UK 01.11.2017
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ISSN:1755-4330, 1755-4349, 1755-4349
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Abstract The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and analogue-oriented synthesis approaches provide a series of lissoclimide natural products and analogues that expand the structure–activity relationships (SARs) in this family. The semisynthesis approach yielded significant quantities of chlorolissoclimide (CL) to permit an evaluation against the National Cancer Institute's 60-cell line panel and allowed us to obtain an X-ray co-crystal structure of the synthetic secondary metabolite with the eukaryotic 80S ribosome. Although it shares a binding site with other imide-based natural product translation inhibitors, CL engages in a particularly interesting and novel face-on halogen– π interaction between the ligand's alkyl chloride and a guanine residue. Our analogue-oriented synthesis provides many more lissoclimide compounds, which were tested against aggressive human cancer cell lines and for protein synthesis inhibitory activity. Finally, computational modelling was used to explain the SARs of certain key compounds and set the stage for the structure-guided design of better translation inhibitors. Several natural and unnatural lissoclimide cytotoxins have been prepared via semi-synthesis and total synthesis. An X-ray co-crystal structure of chlorolissoclimide with the ribosome and evaluation of cytotoxicity and translation inhibition of new compounds in the series improves our understanding of the molecular basis for cytotoxicity.
AbstractList The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and analogue-oriented synthesis approaches provide a series of lissoclimide natural products and analogues that expand the structure-activity relationships (SARs) in this family. The semisynthesis approach yielded significant quantities of chlorolissoclimide (CL) to permit an evaluation against the National Cancer Institute's 60-cell line panel and allowed us to obtain an X-ray co-crystal structure of the synthetic secondary metabolite with the eukaryotic 80S ribosome. Although it shares a binding site with other imide-based natural product translation inhibitors, CL engages in a particularly interesting and novel face-on halogen-π interaction between the ligand's alkyl chloride and a guanine residue. Our analogue-oriented synthesis provides many more lissoclimide compounds, which were tested against aggressive human cancer cell lines and for protein synthesis inhibitory activity. Finally, computational modelling was used to explain the SARs of certain key compounds and set the stage for the structure-guided design of better translation inhibitors.
The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and analogue-oriented synthesis approaches provide a series of lissoclimide natural products and analogues that expand the structure-activity relationships (SARs) in this family. The semisynthesis approach yielded significant quantities of chlorolissoclimide (CL) to permit an evaluation against the National Cancer Institute's 60-cell line panel and allowed us to obtain an X-ray co-crystal structure of the synthetic secondary metabolite with the eukaryotic 80S ribosome. Although it shares a binding site with other imide-based natural product translation inhibitors, CL engages in a particularly interesting and novel face-on halogen-p interaction between the ligand's alkyl chloride and a guanine residue. Our analogue-oriented synthesis provides many more lissoclimide compounds, which were tested against aggressive human cancer cell lines and for protein synthesis inhibitory activity. Finally, computational modelling was used to explain the SARs of certain key compounds and set the stage for the structure-guided design of better translation inhibitors.
The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and analogue-oriented synthesis approaches provide a series of lissoclimide natural products and analogues that expand the structure–activity relationships (SARs) in this family. The semisynthesis approach yielded significant quantities of chlorolissoclimide (CL) to permit an evaluation against the National Cancer Institute's 60-cell line panel and allowed us to obtain an X-ray co-crystal structure of the synthetic secondary metabolite with the eukaryotic 80S ribosome. Although it shares a binding site with other imide-based natural product translation inhibitors, CL engages in a particularly interesting and novel face-on halogen– π interaction between the ligand's alkyl chloride and a guanine residue. Our analogue-oriented synthesis provides many more lissoclimide compounds, which were tested against aggressive human cancer cell lines and for protein synthesis inhibitory activity. Finally, computational modelling was used to explain the SARs of certain key compounds and set the stage for the structure-guided design of better translation inhibitors. Several natural and unnatural lissoclimide cytotoxins have been prepared via semi-synthesis and total synthesis. An X-ray co-crystal structure of chlorolissoclimide with the ribosome and evaluation of cytotoxicity and translation inhibition of new compounds in the series improves our understanding of the molecular basis for cytotoxicity.
The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and analogue-oriented synthesis approaches provide a series of lissoclimide natural products and analogues that expand the structure-activity relationships (SARs) in this family. The semisynthesis approach yielded significant quantities of chlorolissoclimide (CL) to permit an evaluation against the National Cancer Institute's 60-cell line panel and allowed us to obtain an X-ray co-crystal structure of the synthetic secondary metabolite with the eukaryotic 80S ribosome. Although it shares a binding site with other imide-based natural product translation inhibitors, CL engages in a particularly interesting and novel face-on halogen-π interaction between the ligand's alkyl chloride and a guanine residue. Our analogue-oriented synthesis provides many more lissoclimide compounds, which were tested against aggressive human cancer cell lines and for protein synthesis inhibitory activity. Finally, computational modelling was used to explain the SARs of certain key compounds and set the stage for the structure-guided design of better translation inhibitors.The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and analogue-oriented synthesis approaches provide a series of lissoclimide natural products and analogues that expand the structure-activity relationships (SARs) in this family. The semisynthesis approach yielded significant quantities of chlorolissoclimide (CL) to permit an evaluation against the National Cancer Institute's 60-cell line panel and allowed us to obtain an X-ray co-crystal structure of the synthetic secondary metabolite with the eukaryotic 80S ribosome. Although it shares a binding site with other imide-based natural product translation inhibitors, CL engages in a particularly interesting and novel face-on halogen-π interaction between the ligand's alkyl chloride and a guanine residue. Our analogue-oriented synthesis provides many more lissoclimide compounds, which were tested against aggressive human cancer cell lines and for protein synthesis inhibitory activity. Finally, computational modelling was used to explain the SARs of certain key compounds and set the stage for the structure-guided design of better translation inhibitors.
The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semi-synthesis and analogue-oriented synthesis approaches have provided a series of lissoclimide natural products and analogues that expanded the structure-activity relationships in this family. The semi-synthesis approach yielded significant quantities of chlorolissoclimide that permitted evaluation against the NCI’s 60 cell line panel and allowed us to obtain an X-ray co-crystal structure of the synthetic secondary metabolite with the eukaryotic 80S ribosome. While it shares a binding site with other imide-based natural product translation inhibitors, chlorolissoclimide engages in a particularly interesting and novel face-on halogen-π interaction between the ligand’s alkyl chloride and a guanine residue. Our analogue-oriented synthesis provided many more lissoclimide compounds, which were tested against aggressive human cancer cell lines, and for protein synthesis inhibitory activity. Finally, computational modeling was used to explain the SAR of certain key compounds, setting the stage for structure-guided design of better translation inhibitors. Via semi-synthesis and total synthesis, we have made several natural and unnatural lissoclimide cytotoxins. An X-ray co-crystal structure of chlorolissoclimide with the ribosome and evaluation of cytotoxicity and translation inhibition of new compounds in the series improved our understanding of the molecular basis for cytotoxicity.
Author Könst, Zef A.
Yusupov, Marat
Michalak, Sharon E.
Nam, Sangkil
Mobley, David L.
Yusupova, Gulnara
Vanderwal, Christopher D.
Cencic, Regina
Szklarski, Anne R.
Pelletier, Jerry
Meyer, Mélanie
Pellegrino, Simone
Zanette, Camila
Horne, David A.
Voora, Vamsee K.
AuthorAffiliation c Department of Pharmaceutical Sciences, University of California, Irvine, CA 92697, United States
b Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), INSERM U964, CNRS UMR7104, Université de Strasbourg, 67404, Illkirch, France
a Department of Chemistry, 1102 Natural Sciences II, University of California, Irvine, CA 92697-2025, United States
e Department of Molecular Medicine, Beckman Research Institute, City of Hope Comprehensive Cancer Center, 1500 East Duarte Road, Duarte, California 91010, United States
d Department of Biochemistry, McGill University, Montréal, Québec H3G 1Y6, Canada
AuthorAffiliation_xml – name: e Department of Molecular Medicine, Beckman Research Institute, City of Hope Comprehensive Cancer Center, 1500 East Duarte Road, Duarte, California 91010, United States
– name: c Department of Pharmaceutical Sciences, University of California, Irvine, CA 92697, United States
– name: b Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), INSERM U964, CNRS UMR7104, Université de Strasbourg, 67404, Illkirch, France
– name: a Department of Chemistry, 1102 Natural Sciences II, University of California, Irvine, CA 92697-2025, United States
– name: d Department of Biochemistry, McGill University, Montréal, Québec H3G 1Y6, Canada
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  organization: Department of Chemistry, University of California
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  organization: Department of Chemistry, University of California
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  organization: Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), INSERM U964, CNRS UMR7104, Université de Strasbourg
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  organization: Department of Pharmaceutical Sciences, University of California
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  surname: Cencic
  fullname: Cencic, Regina
  organization: Department of Biochemistry, McGill University
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  surname: Nam
  fullname: Nam, Sangkil
  organization: Department of Molecular Medicine, Beckman Research Institute, City of Hope Comprehensive Cancer Center
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  givenname: Vamsee K.
  surname: Voora
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  organization: Department of Chemistry, University of California
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  organization: Department of Pharmaceutical Sciences, University of California
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  surname: Yusupova
  fullname: Yusupova, Gulnara
  organization: Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), INSERM U964, CNRS UMR7104, Université de Strasbourg
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  givenname: Marat
  surname: Yusupov
  fullname: Yusupov, Marat
  email: marat@igbmc.fr
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– sequence: 15
  givenname: Christopher D.
  surname: Vanderwal
  fullname: Vanderwal, Christopher D.
  email: cdv@uci.edu
  organization: Department of Chemistry, University of California
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29064494$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright Springer Nature Limited 2017
Copyright Nature Publishing Group Nov 2017
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Issue 11
Keywords CORE
DICHLOROLISSOCLIMIDE
PROTEIN
LACTIMIDOMYCIN
CYTOTOXIC DITERPENE ALKALOIDS
RIBOSOME
Language English
License Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
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European Research Council (ERC)
National Science Foundation
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content type line 14
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PMCID: PMC6021127
These authors contributed equally.
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0000-0001-5544-0597
0000-0002-9119-9136
0000-0001-6302-2774
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/6021127
PMID 29064494
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PublicationTitle Nature chemistry
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Snippet The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semisynthesis and...
The lissoclimides are unusual succinimide-containing labdane diterpenoids that were reported to be potent cytotoxins. Our short semi-synthesis and...
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StartPage 1140
SubjectTerms 631/535/1266
639/638/309/2420
639/638/549/977
Analogs
Analytical Chemistry
Animals
Antineoplastic Agents, Phytogenic - chemical synthesis
Antineoplastic Agents, Phytogenic - chemistry
Antineoplastic Agents, Phytogenic - pharmacology
Binding sites
Biochemistry
Biological Products - chemical synthesis
Biological Products - chemistry
Biological Products - pharmacology
Biotechnology
Cancer
Cell Line, Tumor
Cell Proliferation - drug effects
Chemistry
Chemistry, Multidisciplinary
Chemistry/Food Science
Computer applications
Crystal structure
Crystallography, X-Ray
Cytotoxins
Diterpenes
Diterpenes - chemical synthesis
Diterpenes - chemistry
Diterpenes - pharmacology
Drug Screening Assays, Antitumor
Eukaryotic Initiation Factors - antagonists & inhibitors
Eukaryotic Initiation Factors - metabolism
Guanine
Humans
Inhibitors
Inorganic Chemistry
Life Sciences
Metabolites
Mice
Models, Molecular
Molecular Conformation
Natural products
Organic Chemistry
Peptides, Cyclic
Physical Chemistry
Physical Sciences
Protein biosynthesis
Protein Biosynthesis - drug effects
Protein synthesis
Science & Technology
Semisynthesis
Structure-activity relationships
Succinimide
Succinimides - chemical synthesis
Succinimides - chemistry
Succinimides - pharmacology
Translation
Tumor cell lines
Title Synthesis facilitates an understanding of the structural basis for translation inhibition by the lissoclimides
URI https://link.springer.com/article/10.1038/nchem.2800
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https://pubmed.ncbi.nlm.nih.gov/PMC6021127
Volume 9
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