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Quantitative image analysis reveals distinct structural transitions during aging in Caenorhabditis elegans tissues.

Johnston J, Iser WB, Chow DK, Goldberg IG, Wolkow CA - PLoS ONE (2008)

Bottom Line: Such approaches are inadequate for the complex changes associated with aging.The processes that underlie these architectural changes may contribute to increased disease risk during aging, and may be targets for factors that alter the aging rate.This work further demonstrates that pattern analysis of an image series offers a novel and generally accessible approach for quantifying morphological changes and identifying structural biomarkers.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, NIA Intramural Research Program, National Institutes of Health, Baltimore, Maryland, United States of America.

ABSTRACT
Aging is associated with functional and structural declines in many body systems, even in the absence of underlying disease. In particular, skeletal muscles experience severe declines during aging, a phenomenon termed sarcopenia. Despite the high incidence and severity of sarcopenia, little is known about contributing factors and development. Many studies focus on functional aspects of aging-related tissue decline, while structural details remain understudied. Traditional approaches for quantifying structural changes have assessed individual markers at discrete intervals. Such approaches are inadequate for the complex changes associated with aging. An alternative is to consider changes in overall morphology rather than in specific markers. We have used this approach to quantitatively track tissue architecture during adulthood and aging in the C. elegans pharynx, the neuromuscular feeding organ. Using pattern recognition to analyze aged-grouped pharynx images, we identified discrete step-wise transitions between distinct morphologies. The morphology state transitions were maintained in mutants with pharynx neurotransmission defects, although the pace of the transitions was altered. Longitudinal measurements of pharynx function identified a predictive relationship between mid-life pharynx morphology and function at later ages. These studies demonstrate for the first time that adult tissues undergo distinct structural transitions reflecting postdevelopmental events. The processes that underlie these architectural changes may contribute to increased disease risk during aging, and may be targets for factors that alter the aging rate. This work further demonstrates that pattern analysis of an image series offers a novel and generally accessible approach for quantifying morphological changes and identifying structural biomarkers.

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Overview of whole-image analysis.(A) Anatomical description of the C. elegans pharynx during adulthood. Cartoon illustrates the pharynx's relative position in the head, and representative images of the terminal bulb from four different ages are shown. Bacteria are ingested through the stoma, or mouth, and concentrated in the corpus region. Concentrated bacteria are passed to the terminal bulb (outlined with a dashed line for clarity) for mechanical disruption in the grinder (G) before transfer to the intestine. Structural aging is evident in the terminal bulb between adult days 2–8 as deterioration of the striated muscle fibers and disorganization in the grinder. (B) Declines in survival and pump rate occur during normal aging in C. elegans. Shown are representative curves for adult survival and pump rate (relative to day 2) in a population of fem-1(hc17) animals at 25°C. (C) General outline for the procedures used in pattern analysis of pharynx images (see text). 85 training images were used for each age group. The resulting class distances form the basis for similarity measurements and age-score predictions.
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pone-0002821-g001: Overview of whole-image analysis.(A) Anatomical description of the C. elegans pharynx during adulthood. Cartoon illustrates the pharynx's relative position in the head, and representative images of the terminal bulb from four different ages are shown. Bacteria are ingested through the stoma, or mouth, and concentrated in the corpus region. Concentrated bacteria are passed to the terminal bulb (outlined with a dashed line for clarity) for mechanical disruption in the grinder (G) before transfer to the intestine. Structural aging is evident in the terminal bulb between adult days 2–8 as deterioration of the striated muscle fibers and disorganization in the grinder. (B) Declines in survival and pump rate occur during normal aging in C. elegans. Shown are representative curves for adult survival and pump rate (relative to day 2) in a population of fem-1(hc17) animals at 25°C. (C) General outline for the procedures used in pattern analysis of pharynx images (see text). 85 training images were used for each age group. The resulting class distances form the basis for similarity measurements and age-score predictions.

Mentions: To characterize age-associated morphological changes in the pharynx, we used DIC microscopy to image the pharynx terminal bulb region from adult animals in early adulthood through old age (Fig. 1A). The C. elegans pharynx is a neuromuscular organ responsible for ingestion and mechanical disruption of bacterial food. This tissue is well-suited for studies of aging. Its morphology is easily assessed by light microscopy and pharynx function can be measured by its pumping rate. During adult aging, the pharynx exhibits structural and functional declines (Fig. 1A, B) [8]. To characterize age-associated morphological changes in the pharynx, we used differential interference contrast (DIC) microscopy to image the pharynx terminal bulb region from adult animals in early adulthood through mid-life and older. To facilitate production of age-synchronized populations, animals used in this study carried the fem-1(hc17) mutation blocking spermatogenesis [9]. Although the fem-1(hc17) animals are sterile, they exhibit lifespan characteristics similar to the wildtype. The sterile fem-1(hc17) animals were used as the baseline for “normal” aging throughout this study.


Quantitative image analysis reveals distinct structural transitions during aging in Caenorhabditis elegans tissues.

Johnston J, Iser WB, Chow DK, Goldberg IG, Wolkow CA - PLoS ONE (2008)

Overview of whole-image analysis.(A) Anatomical description of the C. elegans pharynx during adulthood. Cartoon illustrates the pharynx's relative position in the head, and representative images of the terminal bulb from four different ages are shown. Bacteria are ingested through the stoma, or mouth, and concentrated in the corpus region. Concentrated bacteria are passed to the terminal bulb (outlined with a dashed line for clarity) for mechanical disruption in the grinder (G) before transfer to the intestine. Structural aging is evident in the terminal bulb between adult days 2–8 as deterioration of the striated muscle fibers and disorganization in the grinder. (B) Declines in survival and pump rate occur during normal aging in C. elegans. Shown are representative curves for adult survival and pump rate (relative to day 2) in a population of fem-1(hc17) animals at 25°C. (C) General outline for the procedures used in pattern analysis of pharynx images (see text). 85 training images were used for each age group. The resulting class distances form the basis for similarity measurements and age-score predictions.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2483734&req=5

pone-0002821-g001: Overview of whole-image analysis.(A) Anatomical description of the C. elegans pharynx during adulthood. Cartoon illustrates the pharynx's relative position in the head, and representative images of the terminal bulb from four different ages are shown. Bacteria are ingested through the stoma, or mouth, and concentrated in the corpus region. Concentrated bacteria are passed to the terminal bulb (outlined with a dashed line for clarity) for mechanical disruption in the grinder (G) before transfer to the intestine. Structural aging is evident in the terminal bulb between adult days 2–8 as deterioration of the striated muscle fibers and disorganization in the grinder. (B) Declines in survival and pump rate occur during normal aging in C. elegans. Shown are representative curves for adult survival and pump rate (relative to day 2) in a population of fem-1(hc17) animals at 25°C. (C) General outline for the procedures used in pattern analysis of pharynx images (see text). 85 training images were used for each age group. The resulting class distances form the basis for similarity measurements and age-score predictions.
Mentions: To characterize age-associated morphological changes in the pharynx, we used DIC microscopy to image the pharynx terminal bulb region from adult animals in early adulthood through old age (Fig. 1A). The C. elegans pharynx is a neuromuscular organ responsible for ingestion and mechanical disruption of bacterial food. This tissue is well-suited for studies of aging. Its morphology is easily assessed by light microscopy and pharynx function can be measured by its pumping rate. During adult aging, the pharynx exhibits structural and functional declines (Fig. 1A, B) [8]. To characterize age-associated morphological changes in the pharynx, we used differential interference contrast (DIC) microscopy to image the pharynx terminal bulb region from adult animals in early adulthood through mid-life and older. To facilitate production of age-synchronized populations, animals used in this study carried the fem-1(hc17) mutation blocking spermatogenesis [9]. Although the fem-1(hc17) animals are sterile, they exhibit lifespan characteristics similar to the wildtype. The sterile fem-1(hc17) animals were used as the baseline for “normal” aging throughout this study.

Bottom Line: Such approaches are inadequate for the complex changes associated with aging.The processes that underlie these architectural changes may contribute to increased disease risk during aging, and may be targets for factors that alter the aging rate.This work further demonstrates that pattern analysis of an image series offers a novel and generally accessible approach for quantifying morphological changes and identifying structural biomarkers.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, NIA Intramural Research Program, National Institutes of Health, Baltimore, Maryland, United States of America.

ABSTRACT
Aging is associated with functional and structural declines in many body systems, even in the absence of underlying disease. In particular, skeletal muscles experience severe declines during aging, a phenomenon termed sarcopenia. Despite the high incidence and severity of sarcopenia, little is known about contributing factors and development. Many studies focus on functional aspects of aging-related tissue decline, while structural details remain understudied. Traditional approaches for quantifying structural changes have assessed individual markers at discrete intervals. Such approaches are inadequate for the complex changes associated with aging. An alternative is to consider changes in overall morphology rather than in specific markers. We have used this approach to quantitatively track tissue architecture during adulthood and aging in the C. elegans pharynx, the neuromuscular feeding organ. Using pattern recognition to analyze aged-grouped pharynx images, we identified discrete step-wise transitions between distinct morphologies. The morphology state transitions were maintained in mutants with pharynx neurotransmission defects, although the pace of the transitions was altered. Longitudinal measurements of pharynx function identified a predictive relationship between mid-life pharynx morphology and function at later ages. These studies demonstrate for the first time that adult tissues undergo distinct structural transitions reflecting postdevelopmental events. The processes that underlie these architectural changes may contribute to increased disease risk during aging, and may be targets for factors that alter the aging rate. This work further demonstrates that pattern analysis of an image series offers a novel and generally accessible approach for quantifying morphological changes and identifying structural biomarkers.

Show MeSH
Related in: MedlinePlus