Watching the release of a photopharmacological drug from tubulin using time-resolved serial crystallography.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
17 02 2023
Historique:
received: 15 08 2022
accepted: 02 02 2023
entrez: 22 2 2023
pubmed: 23 2 2023
medline: 25 2 2023
Statut: epublish

Résumé

The binding and release of ligands from their protein targets is central to fundamental biological processes as well as to drug discovery. Photopharmacology introduces chemical triggers that allow the changing of ligand affinities and thus biological activity by light. Insight into the molecular mechanisms of photopharmacology is largely missing because the relevant transitions during the light-triggered reaction cannot be resolved by conventional structural biology. Using time-resolved serial crystallography at a synchrotron and X-ray free-electron laser, we capture the release of the anti-cancer compound azo-combretastatin A4 and the resulting conformational changes in tubulin. Nine structural snapshots from 1 ns to 100 ms complemented by simulations show how cis-to-trans isomerization of the azobenzene bond leads to a switch in ligand affinity, opening of an exit channel, and collapse of the binding pocket upon ligand release. The resulting global backbone rearrangements are related to the action mechanism of microtubule-destabilizing drugs.

Identifiants

pubmed: 36807348
doi: 10.1038/s41467-023-36481-5
pii: 10.1038/s41467-023-36481-5
pmc: PMC9936131
doi:

Substances chimiques

Tubulin 0
Ligands 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

903

Informations de copyright

© 2023. The Author(s).

Références

iScience. 2020 Aug 29;23(9):101511
pubmed: 32920486
J Mol Biol. 2014 Apr 17;426(8):1848-60
pubmed: 24530796
Science. 2021 Aug 27;373(6558):
pubmed: 34446579
Chem Rev. 2018 Nov 14;118(21):10710-10747
pubmed: 29985590
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Acta Crystallogr D Biol Crystallogr. 2002 Nov;58(Pt 11):1948-54
pubmed: 12393927
Science. 2019 Jul 5;365(6448):61-65
pubmed: 31273117
Clin Ther. 2014 Oct 1;36(10):1465-79
pubmed: 25151572
Chem Soc Rev. 2011 Aug;40(8):4422-37
pubmed: 21483974
J Comput Chem. 2005 Dec;26(16):1701-18
pubmed: 16211538
Acta Crystallogr D Struct Biol. 2021 Oct 1;77(Pt 10):1218-1232
pubmed: 34605426
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):235-42
pubmed: 21460441
Curr Opin Struct Biol. 2019 Aug;57:23-30
pubmed: 30825844
Science. 2014 Dec 5;346(6214):1242-6
pubmed: 25477465
Int J Mol Sci. 2022 May 18;23(10):
pubmed: 35628467
Nature. 2020 Jul;583(7815):314-318
pubmed: 32499654
Angew Chem Int Ed Engl. 2021 Jun 7;60(24):13331-13342
pubmed: 33951246
Chem Rev. 2020 Dec 9;120(23):12788-12833
pubmed: 33006893
J Am Chem Soc. 2022 Mar 30;144(12):5614-5628
pubmed: 35290733
J Comput Aided Mol Des. 2013 Mar;27(3):221-34
pubmed: 23579614
J Am Chem Soc. 2014 Feb 12;136(6):2178-91
pubmed: 24456115
Nat Commun. 2014;5:3309
pubmed: 24525480
J Cell Biol. 2014 Nov 10;207(3):323-34
pubmed: 25385183
Acta Crystallogr A Found Adv. 2019 Sep 1;75(Pt 5):694-704
pubmed: 31475914
Gynecol Oncol Res Pract. 2018 Jan 5;5:1
pubmed: 29318022
Science. 2018 Jul 13;361(6398):
pubmed: 29903883
IUCrJ. 2021 Jun 30;8(Pt 4):532-543
pubmed: 34258002
J Chem Theory Comput. 2015 Aug 11;11(8):3696-713
pubmed: 26574453
J Appl Crystallogr. 2016 Mar 29;49(Pt 2):680-689
pubmed: 27047311
Cell. 2015 Jul 16;162(2):403-411
pubmed: 26165941
PLoS Comput Biol. 2012;8(10):e1002708
pubmed: 23093919
EMBO Mol Med. 2021 Nov 8;13(11):e13818
pubmed: 34661376
J Chem Theory Comput. 2012 Apr 10;8(4):1493-502
pubmed: 26596759
Mol Cell Endocrinol. 2019 May 15;488:36-51
pubmed: 30862498
J Chem Theory Comput. 2013 Sep 10;9(9):3878-88
pubmed: 26592383
J Vis Exp. 2019 Feb 28;(144):
pubmed: 30882786
Nat Rev Mol Cell Biol. 2018 Jul;19(7):451-463
pubmed: 29674711
Curr Opin Struct Biol. 2020 Dec;65:193-208
pubmed: 33049498
IUCrJ. 2021 Sep 09;8(Pt 6):878-895
pubmed: 34804542
Struct Dyn. 2018 Jan 08;4(6):061602
pubmed: 29376109
Nat Commun. 2021 Jul 22;12(1):4461
pubmed: 34294694
Methods Mol Biol. 2022;2430:349-374
pubmed: 35476344
Experientia. 1989 Feb 15;45(2):209-11
pubmed: 2920809
Trends Cell Biol. 2018 Oct;28(10):776-792
pubmed: 29871823
Science. 2019 Sep 13;365(6458):1167-1170
pubmed: 31515393
Nature. 2004 Mar 11;428(6979):198-202
pubmed: 15014504
Phys Rev Lett. 2008 Jan 18;100(2):020603
pubmed: 18232845
Nat Commun. 2017 Sep 14;8(1):542
pubmed: 28912485
IUCrJ. 2021 Sep 23;8(Pt 6):905-920
pubmed: 34804544
J Mol Biol. 2002 Jul 12;320(3):597-608
pubmed: 12096912
Cell Chem Biol. 2021 Feb 18;28(2):228-241.e6
pubmed: 33275880
Proc Natl Acad Sci U S A. 2012 Jul 24;109(30):12011-6
pubmed: 22778434
Curr Opin Struct Biol. 2012 Oct;22(5):651-9
pubmed: 23021004
Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13775-9
pubmed: 19666559
Curr Med Chem. 2022;29(20):3557-3585
pubmed: 34986762
Nat Methods. 2020 Jan;17(1):73-78
pubmed: 31740816
Phys Chem Chem Phys. 2016 Apr 21;18(15):10289-96
pubmed: 27020260
Nucleic Acids Res. 2015 Jul 1;43(W1):W443-7
pubmed: 25873628
Struct Dyn. 2020 Apr 01;7(2):024701
pubmed: 32266303
Sci Rep. 2017 Apr 6;7(1):703
pubmed: 28386083
J Comput Chem. 2003 Jul 15;24(9):1016-25
pubmed: 12759902

Auteurs

Maximilian Wranik (M)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Tobias Weinert (T)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Chavdar Slavov (C)

Institute of Physical and Theoretical Chemistry, Goethe University, Frankfurt am Main, Germany.

Tiziana Masini (T)

Computational & Chemical Biology, Istituto Italiano di Tecnologia, 16163, Genova, Italy.

Antonia Furrer (A)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Natacha Gaillard (N)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Dario Gioia (D)

Computational & Chemical Biology, Istituto Italiano di Tecnologia, 16163, Genova, Italy.

Marco Ferrarotti (M)

Computational & Chemical Biology, Istituto Italiano di Tecnologia, 16163, Genova, Italy.

Daniel James (D)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Hannah Glover (H)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Melissa Carrillo (M)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Demet Kekilli (D)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Robin Stipp (R)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Petr Skopintsev (P)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Steffen Brünle (S)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Tobias Mühlethaler (T)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

John Beale (J)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Dardan Gashi (D)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Karol Nass (K)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Dmitry Ozerov (D)

Scientific Computing, Theory and Data, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Philip J M Johnson (PJM)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Claudio Cirelli (C)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Camila Bacellar (C)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Markus Braun (M)

Institute of Physical and Theoretical Chemistry, Goethe University, Frankfurt am Main, Germany.

Meitian Wang (M)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Florian Dworkowski (F)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Chris Milne (C)

Photon Science Division, Paul Scherrer Institut, 5232, Villigen, Switzerland.

Andrea Cavalli (A)

Computational & Chemical Biology, Istituto Italiano di Tecnologia, 16163, Genova, Italy.
Department of Pharmacy and Biotechnology, University of Bologna, 40126, Bologna, Italy.

Josef Wachtveitl (J)

Institute of Physical and Theoretical Chemistry, Goethe University, Frankfurt am Main, Germany.

Michel O Steinmetz (MO)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland. michel.steinmetz@psi.ch.
Biozentrum, University of Basel, 4056, Basel, Switzerland. michel.steinmetz@psi.ch.

Jörg Standfuss (J)

Division of Biology and Chemistry, Paul Scherrer Institut, 5232, Villigen, Switzerland. joerg.standfuss@psi.ch.

Articles similaires

Receptor, Cannabinoid, CB1 Ligands Molecular Dynamics Simulation Protein Binding Thermodynamics
Crystallography, X-Ray DNA Protein Binding HMGA Proteins AT-Hook Motifs
Proteins Protein Binding Ligands Internet Databases, Protein

Human prolyl hydroxylase domain 2 reacts with O

Giorgia Fiorini, Stephen A Marshall, William D Figg et al.
1.00
Humans Ketoglutaric Acids Hypoxia-Inducible Factor-Proline Dioxygenases Oxygen Hypoxia-Inducible Factor 1, alpha Subunit

Classifications MeSH