Structural effects of protein aging: Terminal marking by deamidation in human triosephosphate isomerase
Abstract
Deamidation, the loss of the ammonium group of asparagine and glutamine to form aspartic and glutamic acid, is one of the most commonly occurring post-translational modifications in proteins. Since deamidation rates are encoded in the protein structure, it has been proposed that they can serve as molecular clocks for the timing of biological processes such as protein turnover, development and aging. Despite the importance of this process, there is a lack of detailed structural information explaining the effects of deamidation on the structure of proteins. Here, we studied the effects of deamidation on human triosephosphate isomerase (HsTIM), an enzyme for which deamidation of N15 and N71 has been long recognized as the signal for terminal marking of the protein. Deamidation was mimicked by site directed mutagenesis; thus, three mutants of HsTIM (N15D, N71D and N15D/N71D) were characterized. The results show that the N71D mutant resembles, structurally and functionally, the wild type enzyme. In contrast, the N15D mutant displays all the detrimental effects related to deamidation. The N15D/N71D mutant shows only minor additional effects when compared with the N15D mutation, supporting that deamidation of N71 induces negligible effects. The crystal structures show that, in contrast to the N71D mutant, where minimalmore »
- Authors:
-
- Univ. Nacional Autonoma de Mexico (Mexico)
- Instituto Nacional de Pediatria (Mexico)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- Instituto Nacional de Pediatria (Mexico)
- OSTI Identifier:
- 1178831
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 4; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; deamidation; crystal structure; sequence alignment; asparagine; multiple alignment calculation; phylogenetic analysis; protein structure; enzyme structure
Citation Formats
Torres-Larios, Alfredo, Enríquez-Flores, Sergio, Méndez, Sara -Teresa, Castillo-Villanueva, Adriana, Gómez-Manzo, Saúl, Velázquez, Gabriel López-, Marcial-Quino, Jaime, Torres-Arroyo, Angélica, García-Torres, Itzhel, Reyes-Vivas, Horacio, Oria-Hernández, Jesús, and de la Mora-de la Mora, Ignacio. Structural effects of protein aging: Terminal marking by deamidation in human triosephosphate isomerase. United States: N. p., 2015.
Web. doi:10.1371/journal.pone.0123379.
Torres-Larios, Alfredo, Enríquez-Flores, Sergio, Méndez, Sara -Teresa, Castillo-Villanueva, Adriana, Gómez-Manzo, Saúl, Velázquez, Gabriel López-, Marcial-Quino, Jaime, Torres-Arroyo, Angélica, García-Torres, Itzhel, Reyes-Vivas, Horacio, Oria-Hernández, Jesús, & de la Mora-de la Mora, Ignacio. Structural effects of protein aging: Terminal marking by deamidation in human triosephosphate isomerase. United States. https://doi.org/10.1371/journal.pone.0123379
Torres-Larios, Alfredo, Enríquez-Flores, Sergio, Méndez, Sara -Teresa, Castillo-Villanueva, Adriana, Gómez-Manzo, Saúl, Velázquez, Gabriel López-, Marcial-Quino, Jaime, Torres-Arroyo, Angélica, García-Torres, Itzhel, Reyes-Vivas, Horacio, Oria-Hernández, Jesús, and de la Mora-de la Mora, Ignacio. Fri .
"Structural effects of protein aging: Terminal marking by deamidation in human triosephosphate isomerase". United States. https://doi.org/10.1371/journal.pone.0123379. https://www.osti.gov/servlets/purl/1178831.
@article{osti_1178831,
title = {Structural effects of protein aging: Terminal marking by deamidation in human triosephosphate isomerase},
author = {Torres-Larios, Alfredo and Enríquez-Flores, Sergio and Méndez, Sara -Teresa and Castillo-Villanueva, Adriana and Gómez-Manzo, Saúl and Velázquez, Gabriel López- and Marcial-Quino, Jaime and Torres-Arroyo, Angélica and García-Torres, Itzhel and Reyes-Vivas, Horacio and Oria-Hernández, Jesús and de la Mora-de la Mora, Ignacio},
abstractNote = {Deamidation, the loss of the ammonium group of asparagine and glutamine to form aspartic and glutamic acid, is one of the most commonly occurring post-translational modifications in proteins. Since deamidation rates are encoded in the protein structure, it has been proposed that they can serve as molecular clocks for the timing of biological processes such as protein turnover, development and aging. Despite the importance of this process, there is a lack of detailed structural information explaining the effects of deamidation on the structure of proteins. Here, we studied the effects of deamidation on human triosephosphate isomerase (HsTIM), an enzyme for which deamidation of N15 and N71 has been long recognized as the signal for terminal marking of the protein. Deamidation was mimicked by site directed mutagenesis; thus, three mutants of HsTIM (N15D, N71D and N15D/N71D) were characterized. The results show that the N71D mutant resembles, structurally and functionally, the wild type enzyme. In contrast, the N15D mutant displays all the detrimental effects related to deamidation. The N15D/N71D mutant shows only minor additional effects when compared with the N15D mutation, supporting that deamidation of N71 induces negligible effects. The crystal structures show that, in contrast to the N71D mutant, where minimal alterations are observed, the N15D mutation forms new interactions that perturb the structure of loop 1 and loop 3, both critical components of the catalytic site and the interface of HsTIM. Based on a phylogenetic analysis of TIM sequences, we propose the conservation of this mechanism for mammalian TIMs.},
doi = {10.1371/journal.pone.0123379},
journal = {PLoS ONE},
number = 4,
volume = 10,
place = {United States},
year = {Fri Apr 17 00:00:00 EDT 2015},
month = {Fri Apr 17 00:00:00 EDT 2015}
}
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Succinimide and isoaspartate residues in the crystal structures of hen egg-white lysozyme complexed with tri-N-acetylchitotriose
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The E104D mutation increases the susceptibility of human triosephosphate isomerase to proteolysis. Asymmetric cleavage of the two monomers of the homodimeric enzyme
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Species-specific inhibition of Giardia lamblia triosephosphate isomerase by localized perturbation of the homodimer
journal, February 2008
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Evolution of enzyme function and the development of catalytic efficiency
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Role of Lys-12 in Catalysis by Triosephosphate Isomerase: A Two-Part Substrate Approach
journal, June 2010
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Deamidation of Asparagine to Aspartate Destabilizes Cu, Zn Superoxide Dismutase, Accelerates Fibrillization, and Mirrors ALS-Linked Mutations
journal, October 2013
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Initiation of the Reaction of Deamidation in Triosephosphate Isomerase: Investigations by Means of Molecular Dynamics Simulations
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Protein deamidation
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Controlled Deamidation of Peptides and Proteins: An Experimental Hazard and a Possible Biological Timer
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