Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytes

Abstract Background Oocyte quality decreases with aging, thereby increasing errors in fertilization, chromosome segregation, and embryonic cleavage. Oocyte appearance also changes with aging, suggesting a functional relationship between oocyte quality and appearance. However, no methods are availabl...

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Main Authors: Momoko Imakubo, Jun Takayama, Hatsumi Okada, Shuichi Onami
Format: Article
Language:English
Published: BMC 2021-02-01
Series:BMC Bioinformatics
Subjects:
Online Access:https://doi.org/10.1186/s12859-021-03990-3
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spelling doaj-b18ea917dbe7490d95592ac10a221d482021-02-21T12:49:43ZengBMCBMC Bioinformatics1471-21052021-02-0122112110.1186/s12859-021-03990-3Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytesMomoko Imakubo0Jun Takayama1Hatsumi Okada2Shuichi Onami3Department of Computational Science, Graduate School of System Informatics, Kobe UniversityLaboratory for Developmental Dynamics, RIKEN Quantitative Biology CenterLaboratory for Developmental Dynamics, RIKEN Center for Biosystems Dynamics ResearchDepartment of Computational Science, Graduate School of System Informatics, Kobe UniversityAbstract Background Oocyte quality decreases with aging, thereby increasing errors in fertilization, chromosome segregation, and embryonic cleavage. Oocyte appearance also changes with aging, suggesting a functional relationship between oocyte quality and appearance. However, no methods are available to objectively quantify age-associated changes in oocyte appearance. Results We show that statistical image processing of Nomarski differential interference contrast microscopy images can be used to quantify age-associated changes in oocyte appearance in the nematode Caenorhabditis elegans. Max–min value (mean difference between the maximum and minimum intensities within each moving window) quantitatively characterized the difference in oocyte cytoplasmic texture between 1- and 3-day-old adults (Day 1 and Day 3 oocytes, respectively). With an appropriate parameter set, the gray level co-occurrence matrix (GLCM)-based texture feature Correlation (COR) more sensitively characterized this difference than the Max–min Value. Manipulating the smoothness of and/or adding irregular structures to the cytoplasmic texture of Day 1 oocyte images reproduced the difference in Max–min Value but not in COR between Day 1 and Day 3 oocytes. Increasing the size of granules in synthetic images recapitulated the age-associated changes in COR. Manual measurements validated that the cytoplasmic granules in oocytes become larger with aging. Conclusions The Max–min value and COR objectively quantify age-related changes in C. elegans oocyte in Nomarski DIC microscopy images. Our methods provide new opportunities for understanding the mechanism underlying oocyte aging.https://doi.org/10.1186/s12859-021-03990-3Oocyte agingCaenorhabditis elegansImage texture analysisStatistical image processingGray level co-occurrence matrixNomarski DIC microscopy
collection DOAJ
language English
format Article
sources DOAJ
author Momoko Imakubo
Jun Takayama
Hatsumi Okada
Shuichi Onami
spellingShingle Momoko Imakubo
Jun Takayama
Hatsumi Okada
Shuichi Onami
Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytes
BMC Bioinformatics
Oocyte aging
Caenorhabditis elegans
Image texture analysis
Statistical image processing
Gray level co-occurrence matrix
Nomarski DIC microscopy
author_facet Momoko Imakubo
Jun Takayama
Hatsumi Okada
Shuichi Onami
author_sort Momoko Imakubo
title Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytes
title_short Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytes
title_full Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytes
title_fullStr Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytes
title_full_unstemmed Statistical image processing quantifies the changes in cytoplasmic texture associated with aging in Caenorhabditis elegans oocytes
title_sort statistical image processing quantifies the changes in cytoplasmic texture associated with aging in caenorhabditis elegans oocytes
publisher BMC
series BMC Bioinformatics
issn 1471-2105
publishDate 2021-02-01
description Abstract Background Oocyte quality decreases with aging, thereby increasing errors in fertilization, chromosome segregation, and embryonic cleavage. Oocyte appearance also changes with aging, suggesting a functional relationship between oocyte quality and appearance. However, no methods are available to objectively quantify age-associated changes in oocyte appearance. Results We show that statistical image processing of Nomarski differential interference contrast microscopy images can be used to quantify age-associated changes in oocyte appearance in the nematode Caenorhabditis elegans. Max–min value (mean difference between the maximum and minimum intensities within each moving window) quantitatively characterized the difference in oocyte cytoplasmic texture between 1- and 3-day-old adults (Day 1 and Day 3 oocytes, respectively). With an appropriate parameter set, the gray level co-occurrence matrix (GLCM)-based texture feature Correlation (COR) more sensitively characterized this difference than the Max–min Value. Manipulating the smoothness of and/or adding irregular structures to the cytoplasmic texture of Day 1 oocyte images reproduced the difference in Max–min Value but not in COR between Day 1 and Day 3 oocytes. Increasing the size of granules in synthetic images recapitulated the age-associated changes in COR. Manual measurements validated that the cytoplasmic granules in oocytes become larger with aging. Conclusions The Max–min value and COR objectively quantify age-related changes in C. elegans oocyte in Nomarski DIC microscopy images. Our methods provide new opportunities for understanding the mechanism underlying oocyte aging.
topic Oocyte aging
Caenorhabditis elegans
Image texture analysis
Statistical image processing
Gray level co-occurrence matrix
Nomarski DIC microscopy
url https://doi.org/10.1186/s12859-021-03990-3
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