Literature DB >> 25114240

A new tubulin-binding site and pharmacophore for microtubule-destabilizing anticancer drugs.

Andrea E Prota1, Katja Bargsten1, J Fernando Diaz2, May Marsh3, Carmen Cuevas4, Marc Liniger5, Christian Neuhaus5, Jose M Andreu2, Karl-Heinz Altmann5, Michel O Steinmetz6.   

Abstract

The recent success of antibody-drug conjugates (ADCs) in the treatment of cancer has led to a revived interest in microtubule-destabilizing agents. Here, we determined the high-resolution crystal structure of the complex between tubulin and maytansine, which is part of an ADC that is approved by the US Food and Drug Administration (FDA) for the treatment of advanced breast cancer. We found that the drug binds to a site on β-tubulin that is distinct from the vinca domain and that blocks the formation of longitudinal tubulin interactions in microtubules. We also solved crystal structures of tubulin in complex with both a variant of rhizoxin and the phase 1 drug PM060184. Consistent with biochemical and mutagenesis data, we found that the two compounds bound to the same site as maytansine and that the structures revealed a common pharmacophore for the three ligands. Our results delineate a distinct molecular mechanism of action for the inhibition of microtubule assembly by clinically relevant agents. They further provide a structural basis for the rational design of potent microtubule-destabilizing agents, thus opening opportunities for the development of next-generation ADCs for the treatment of cancer.

Entities:  

Keywords:  X-ray crystallography; drug mechanism; microtubule-targeting agents

Mesh:

Substances:

Year:  2014        PMID: 25114240      PMCID: PMC4183314          DOI: 10.1073/pnas.1408124111

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  34 in total

1.  Refined structure of alpha beta-tubulin at 3.5 A resolution.

Authors:  J Löwe; H Li; K H Downing; E Nogales
Journal:  J Mol Biol       Date:  2001-11-09       Impact factor: 5.469

2.  The promise of antibody-drug conjugates.

Authors:  Beverly A Teicher; James H Doroshow
Journal:  N Engl J Med       Date:  2012-11-08       Impact factor: 91.245

3.  Antibody-drug conjugates.

Authors:  Rachel S Zolot; Satarupa Basu; Ryan P Million
Journal:  Nat Rev Drug Discov       Date:  2013-04       Impact factor: 84.694

4.  Molecular mechanism of action of microtubule-stabilizing anticancer agents.

Authors:  Andrea E Prota; Katja Bargsten; Didier Zurwerra; Jessica J Field; José Fernando Díaz; Karl-Heinz Altmann; Michel O Steinmetz
Journal:  Science       Date:  2013-01-03       Impact factor: 47.728

5.  Total synthesis of the tubulin inhibitor WF-1360F based on macrocycle formation through ring-closing alkyne metathesis.

Authors:  Christian M Neuhaus; Marc Liniger; Martin Stieger; Karl-Heinz Altmann
Journal:  Angew Chem Int Ed Engl       Date:  2013-04-22       Impact factor: 15.336

6.  PM060184, a new tubulin binding agent with potent antitumor activity including P-glycoprotein over-expressing tumors.

Authors:  Marta Martínez-Díez; María José Guillén-Navarro; Benet Pera; Benjamin Pierre Bouchet; Juan Fernando Martínez-Leal; Isabel Barasoain; Carmen Cuevas; Jose M Andreu; Luis Francisco García-Fernández; J Fernando Díaz; Pablo Avilés; Carlos M Galmarini
Journal:  Biochem Pharmacol       Date:  2014-01-31       Impact factor: 5.858

7.  New interfacial microtubule inhibitors of marine origin, PM050489/PM060184, with potent antitumor activity and a distinct mechanism.

Authors:  Benet Pera; Isabel Barasoain; Areti Pantazopoulou; Angeles Canales; Ruth Matesanz; Javier Rodriguez-Salarichs; Luis F García-Fernandez; Victoria Moneo; Jesús Jiménez-Barbero; Carlos M Galmarini; Carmen Cuevas; Miguel A Peñalva; J Fernando Díaz; José M Andreu
Journal:  ACS Chem Biol       Date:  2013-08-01       Impact factor: 5.100

Review 8.  Antibody-drug conjugates in cancer therapy.

Authors:  Eric L Sievers; Peter D Senter
Journal:  Annu Rev Med       Date:  2012-10-03       Impact factor: 13.739

9.  Isolation and first total synthesis of PM050489 and PM060184, two new marine anticancer compounds.

Authors:  María Jesús Martín; Laura Coello; Rogelio Fernández; Fernando Reyes; Alberto Rodríguez; Carmen Murcia; María Garranzo; Cristina Mateo; Francisco Sánchez-Sancho; Santiago Bueno; Carlos de Eguilior; Andrés Francesch; Simon Munt; Carmen Cuevas
Journal:  J Am Chem Soc       Date:  2013-06-26       Impact factor: 15.419

10.  Structural basis of tubulin tyrosination by tubulin tyrosine ligase.

Authors:  Andrea E Prota; Maria M Magiera; Marijn Kuijpers; Katja Bargsten; Daniel Frey; Mara Wieser; Rolf Jaussi; Casper C Hoogenraad; Richard A Kammerer; Carsten Janke; Michel O Steinmetz
Journal:  J Cell Biol       Date:  2013-01-28       Impact factor: 10.539

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  68 in total

Review 1.  Targeting and extending the eukaryotic druggable genome with natural products: cytoskeletal targets of natural products.

Authors:  April L Risinger; Lin Du
Journal:  Nat Prod Rep       Date:  2019-11-25       Impact factor: 13.423

2.  Design, synthesis, and structure-activity relationships of pyrimido[4,5-b]indole-4-amines as microtubule depolymerizing agents that are effective against multidrug resistant cells.

Authors:  Ravi Kumar Vyas Devambatla; Wei Li; Nilesh Zaware; Shruti Choudhary; Ernest Hamel; Susan L Mooberry; Aleem Gangjee
Journal:  Bioorg Med Chem Lett       Date:  2017-05-27       Impact factor: 2.823

3.  Structure based drug design and in vitro metabolism study: Discovery of N-(4-methylthiophenyl)-N,2-dimethyl-cyclopenta[d]pyrimidine as a potent microtubule targeting agent.

Authors:  Weiguo Xiang; Shruti Choudhary; Ernest Hamel; Susan L Mooberry; Aleem Gangjee
Journal:  Bioorg Med Chem       Date:  2018-04-04       Impact factor: 3.641

4.  Structures of potent anticancer compounds bound to tubulin.

Authors:  Dan E McNamara; Silvia Senese; Todd O Yeates; Jorge Z Torres
Journal:  Protein Sci       Date:  2015-05-27       Impact factor: 6.725

Review 5.  Current advances of tubulin inhibitors as dual acting small molecules for cancer therapy.

Authors:  Kinsie E Arnst; Souvik Banerjee; Hao Chen; Shanshan Deng; Dong-Jin Hwang; Wei Li; Duane D Miller
Journal:  Med Res Rev       Date:  2019-02-11       Impact factor: 12.944

Review 6.  Strategies and challenges for the next generation of antibody-drug conjugates.

Authors:  Alain Beck; Liliane Goetsch; Charles Dumontet; Nathalie Corvaïa
Journal:  Nat Rev Drug Discov       Date:  2017-03-17       Impact factor: 84.694

7.  A previously undescribed tubulin binder.

Authors:  Jessica J Field; Andrew B Waight; Peter D Senter
Journal:  Proc Natl Acad Sci U S A       Date:  2014-09-03       Impact factor: 11.205

8.  Synthesis and Biological Evaluation of Benzocyclooctene-based and Indene-based Anticancer Agents that Function as Inhibitors of Tubulin Polymerization.

Authors:  Christine A Herdman; Tracy E Strecker; Rajendra P Tanpure; Zhi Chen; Alex Winters; Jeni Gerberich; Li Liu; Ernest Hamel; Ralph P Mason; David J Chaplin; Mary Lynn Trawick; Kevin G Pinney
Journal:  Medchemcomm       Date:  2016-09-22       Impact factor: 3.597

9.  Gatorbulin-1, a distinct cyclodepsipeptide chemotype, targets a seventh tubulin pharmacological site.

Authors:  Susan Matthew; Qi-Yin Chen; Ranjala Ratnayake; Charles S Fermaintt; Daniel Lucena-Agell; Francesca Bonato; Andrea E Prota; Seok Ting Lim; Xiaomeng Wang; J Fernando Díaz; April L Risinger; Valerie J Paul; Maria Ángela Oliva; Hendrik Luesch
Journal:  Proc Natl Acad Sci U S A       Date:  2021-03-02       Impact factor: 11.205

10.  Biological Characterization of an Improved Pyrrole-Based Colchicine Site Agent Identified through Structure-Based Design.

Authors:  Cristina C Rohena; Nakul S Telang; Chenxiao Da; April L Risinger; James A Sikorski; Glen E Kellogg; John T Gupton; Susan L Mooberry
Journal:  Mol Pharmacol       Date:  2015-12-11       Impact factor: 4.436

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