Quantifying cooperative multisite binding in the hub protein LC8 through Bayesian inference Article Swipe
Aidan Estelle
,
August George
,
Elisar Barbar
,
Daniel M. Zuckerman
·
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1371/journal.pcbi.1011059
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1371/journal.pcbi.1011059
Multistep protein-protein interactions underlie most biological processes, but their characterization through methods such as isothermal titration calorimetry (ITC) is largely confined to simple models that provide little information on the intermediate, individual steps. In this study, we primarily examine the essential hub protein LC8, a small dimer that binds disordered regions of 100+ client proteins in two symmetrical grooves at the dimer interface. Mechanistic details of LC8 binding have remained elusive, hampered in part by ITC data analyses employing simple models that treat bivalent binding as a single event with a single binding affinity. We build on existing Bayesian ITC approaches to quantify thermodynamic parameters for multi-site binding interactions impacted by significant uncertainty in protein concentration. Using a two-site binding model, we identify positive cooperativity with high confidence for LC8 binding to multiple client peptides. In contrast, application of an identical model to the two-site binding between the coiled-coil NudE dimer and the intermediate chain of dynein reveals little evidence of cooperativity. We propose that cooperativity in the LC8 system drives the formation of saturated induced-dimer structures, the functional units of most LC8 complexes. In addition to these system-specific findings, our work advances general ITC analysis in two ways. First, we describe a previously unrecognized mathematical ambiguity in concentrations in standard binding models and clarify how it impacts the precision with which binding parameters are determinable in cases of high uncertainty in analyte concentrations. Second, building on observations in the LC8 system, we develop a system-agnostic heat map of practical parameter identifiability calculated from synthetic data which demonstrates that the ability to determine microscopic binding parameters is strongly dependent on both the parameters themselves and experimental conditions. The work serves as a foundation for determination of multi-step binding interactions, and we outline best practices for Bayesian analysis of ITC experiments.
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Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1371/journal.pcbi.1011059
- https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1011059&type=printable
- OA Status
- gold
- Cited By
- 15
- References
- 67
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4366601852
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4366601852Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1371/journal.pcbi.1011059Digital Object Identifier
- Title
-
Quantifying cooperative multisite binding in the hub protein LC8 through Bayesian inferenceWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2023Year of publication
- Publication date
-
2023-04-21Full publication date if available
- Authors
-
Aidan Estelle, August George, Elisar Barbar, Daniel M. ZuckermanList of authors in order
- Landing page
-
https://doi.org/10.1371/journal.pcbi.1011059Publisher landing page
- PDF URL
-
https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1011059&type=printableDirect link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
goldOpen access status per OpenAlex
- OA URL
-
https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1011059&type=printableDirect OA link when available
- Concepts
-
Cooperativity, Isothermal titration calorimetry, Cooperative binding, Dimer, Chemistry, Binding site, Plasma protein binding, Allosteric regulation, Biophysics, Biological system, Computational biology, Biology, Biochemistry, Organic chemistry, EnzymeTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
15Total citation count in OpenAlex
- Citations by year (recent)
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2025: 11, 2024: 3, 2023: 1Per-year citation counts (last 5 years)
- References (count)
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67Number of works referenced by this work
- Related works (count)
-
10Other works algorithmically related by OpenAlex
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