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Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin

Guanine nucleotides can flip between a North and South conformation in the ribose moiety. To test the enzymatic activity of GTPases bound to nucleotides in the two conformations, we generated methanocarba guanine nucleotides in the North or South envelope conformations, i.e., (N)-GTP and (S)-GTP, re...

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Autores principales: Toti, Kiran S., Jimah, John R., Salmaso, Veronica, Hinshaw, Jenny E., Jacobson, Kenneth A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9031165/
https://www.ncbi.nlm.nih.gov/pubmed/35454173
http://dx.doi.org/10.3390/biom12040584
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author Toti, Kiran S.
Jimah, John R.
Salmaso, Veronica
Hinshaw, Jenny E.
Jacobson, Kenneth A.
author_facet Toti, Kiran S.
Jimah, John R.
Salmaso, Veronica
Hinshaw, Jenny E.
Jacobson, Kenneth A.
author_sort Toti, Kiran S.
collection PubMed
description Guanine nucleotides can flip between a North and South conformation in the ribose moiety. To test the enzymatic activity of GTPases bound to nucleotides in the two conformations, we generated methanocarba guanine nucleotides in the North or South envelope conformations, i.e., (N)-GTP and (S)-GTP, respectively. With dynamin as a model system, we examined the effects of (N)-GTP and (S)-GTP on dynamin-mediated membrane constriction, an activity essential for endocytosis. Dynamin membrane constriction and fission activity are dependent on GTP binding and hydrolysis, but the effect of the conformational state of the GTP nucleotide on dynamin activity is not known. After reconstituting dynamin-mediated lipid tubulation and membrane constriction in vitro, we observed via cryo-electron microscopy (cryo-EM) that (N)-GTP, but not (S)-GTP, enables the constriction of dynamin-decorated lipid tubules. These findings suggest that the activity of dynamin is dependent on the conformational state of the GTP nucleotide. However, a survey of nucleotide ribose conformations associated with dynamin structures in nature shows almost exclusively the (S)-conformation. The explanation for this mismatch of (N) vs. (S) required for GTP analogues in a dynamin-mediated process will be addressed in future studies.
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spelling pubmed-90311652022-04-23 Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin Toti, Kiran S. Jimah, John R. Salmaso, Veronica Hinshaw, Jenny E. Jacobson, Kenneth A. Biomolecules Article Guanine nucleotides can flip between a North and South conformation in the ribose moiety. To test the enzymatic activity of GTPases bound to nucleotides in the two conformations, we generated methanocarba guanine nucleotides in the North or South envelope conformations, i.e., (N)-GTP and (S)-GTP, respectively. With dynamin as a model system, we examined the effects of (N)-GTP and (S)-GTP on dynamin-mediated membrane constriction, an activity essential for endocytosis. Dynamin membrane constriction and fission activity are dependent on GTP binding and hydrolysis, but the effect of the conformational state of the GTP nucleotide on dynamin activity is not known. After reconstituting dynamin-mediated lipid tubulation and membrane constriction in vitro, we observed via cryo-electron microscopy (cryo-EM) that (N)-GTP, but not (S)-GTP, enables the constriction of dynamin-decorated lipid tubules. These findings suggest that the activity of dynamin is dependent on the conformational state of the GTP nucleotide. However, a survey of nucleotide ribose conformations associated with dynamin structures in nature shows almost exclusively the (S)-conformation. The explanation for this mismatch of (N) vs. (S) required for GTP analogues in a dynamin-mediated process will be addressed in future studies. MDPI 2022-04-16 /pmc/articles/PMC9031165/ /pubmed/35454173 http://dx.doi.org/10.3390/biom12040584 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Toti, Kiran S.
Jimah, John R.
Salmaso, Veronica
Hinshaw, Jenny E.
Jacobson, Kenneth A.
Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin
title Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin
title_full Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin
title_fullStr Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin
title_full_unstemmed Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin
title_short Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin
title_sort synthesis and effect of conformationally locked carbocyclic guanine nucleotides on dynamin
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9031165/
https://www.ncbi.nlm.nih.gov/pubmed/35454173
http://dx.doi.org/10.3390/biom12040584
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