Algorithm for biological second messenger analysis with dynamic regions of interest.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2023
Historique:
received: 26 09 2022
accepted: 29 03 2023
medline: 15 5 2023
pubmed: 11 5 2023
entrez: 11 5 2023
Statut: epublish

Résumé

Physiological function is regulated through cellular communication that is facilitated by multiple signaling molecules such as second messengers. Analysis of signal dynamics obtained from cell and tissue imaging is difficult because of intricate spatially and temporally distinct signals. Signal analysis tools based on static region of interest analysis may under- or overestimate signals in relation to region of interest size and location. Therefore, we developed an algorithm for biological signal detection and analysis based on dynamic regions of interest, where time-dependent polygonal regions of interest are automatically assigned to the changing perimeter of detected and segmented signals. This approach allows signal profiles to be rigorously and precisely tracked over time, eliminating the signal distortion observed with static methods. Integration of our approach with state-of-the-art image processing and particle tracking pipelines enabled the isolation of dynamic cellular signaling events and characterization of biological signaling patterns with distinct combinations of parameters including amplitude, duration, and spatial spread. Our algorithm was validated using synthetically generated datasets and compared with other available methods. Application of the algorithm to volumetric time-lapse hyperspectral images of cyclic adenosine monophosphate measurements in rat microvascular endothelial cells revealed distinct signal heterogeneity with respect to cell depth, confirming the utility of our approach for analysis of 5-dimensional data. In human tibial arteries, our approach allowed the identification of distinct calcium signal patterns associated with atherosclerosis. Our algorithm for automated detection and analysis of second messenger signals enables the decoding of signaling patterns in diverse tissues and identification of pathologic cellular responses.

Identifiants

pubmed: 37167308
doi: 10.1371/journal.pone.0284394
pii: PONE-D-22-26650
pmc: PMC10174521
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0284394

Subventions

Organisme : NHLBI NIH HHS
ID : K25 HL136869
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL066299
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL155288
Pays : United States
Organisme : NIH HHS
ID : S10 OD020149
Pays : United States

Informations de copyright

Copyright: © 2023 Knighten et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Jennifer M Knighten (JM)

Department of Physiology and Cell Biology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

Takreem Aziz (T)

Department of Physiology and Cell Biology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

Donald J Pleshinger (DJ)

Department of Pharmacology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

Naga Annamdevula (N)

Department of Pharmacology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

Thomas C Rich (TC)

Department of Pharmacology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.
Center for Lung Biology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

Mark S Taylor (MS)

Department of Physiology and Cell Biology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

Joel F Andrews (JF)

Bioimaging Core Facility, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

Christian T Macarilla (CT)

Department of Physiology and Cell Biology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

C Michael Francis (CM)

Department of Physiology and Cell Biology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.
Center for Lung Biology, University of South Alabama College of Medicine, Mobile, Alabama, United States of America.

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