Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age

Organ function declines with age, and large-scale transcriptomic analyses have highlighted differential aging trajectories across tissues. The mechanism underlying shared and organ-selective functional changes across the lifespan, however, still remains poorly understood. Given the central role of m...

Full description

Saved in:
Bibliographic Details
Main Authors: Dylan C Sarver, Muzna Saqib, Fangluo Chen, G William Wong
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/96926
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850122482982322176
author Dylan C Sarver
Muzna Saqib
Fangluo Chen
G William Wong
author_facet Dylan C Sarver
Muzna Saqib
Fangluo Chen
G William Wong
author_sort Dylan C Sarver
collection DOAJ
description Organ function declines with age, and large-scale transcriptomic analyses have highlighted differential aging trajectories across tissues. The mechanism underlying shared and organ-selective functional changes across the lifespan, however, still remains poorly understood. Given the central role of mitochondria in powering cellular processes needed to maintain tissue health, we therefore undertook a systematic assessment of respiratory activity across 33 different tissues in young (2.5 months) and old (20 months) mice of both sexes. Our high-resolution mitochondrial respiration atlas reveals: (1) within any group of mice, mitochondrial activity varies widely across tissues, with the highest values consistently seen in heart, brown fat, and kidney; (2) biological sex is a significant but minor contributor to mitochondrial respiration, and its contributions are tissue-specific, with major differences seen in the pancreas, stomach, and white adipose tissue; (3) age is a dominant factor affecting mitochondrial activity, especially across most brain regions, different fat depots, skeletal muscle groups, eyes, and different regions of the gastrointestinal tract; (4) age effects can be sex- and tissue-specific, with some of the largest effects seen in pancreas, heart, adipose tissue, and skeletal muscle; and (5) while aging alters the functional trajectories of mitochondria in a majority of tissues, some are remarkably resilient to age-induced changes. Altogether, our data provide the most comprehensive compendium of mitochondrial respiration and illuminate functional signatures of aging across diverse tissues and organ systems.
format Article
id doaj-art-bbc00e49006b410db17d596fde5c9eb2
institution OA Journals
issn 2050-084X
language English
publishDate 2024-12-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj-art-bbc00e49006b410db17d596fde5c9eb22025-08-20T02:34:49ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.96926Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and ageDylan C Sarver0Muzna Saqib1Fangluo Chen2G William Wong3https://orcid.org/0000-0002-5286-6506Department of Physiology, Johns Hopkins University School of Medicine, Baltimore, United States; Center for Metabolism and Obesity Research, Johns Hopkins University School of Medicine, Baltimore, United StatesDepartment of Physiology, Johns Hopkins University School of Medicine, Baltimore, United States; Center for Metabolism and Obesity Research, Johns Hopkins University School of Medicine, Baltimore, United StatesDepartment of Physiology, Johns Hopkins University School of Medicine, Baltimore, United States; Center for Metabolism and Obesity Research, Johns Hopkins University School of Medicine, Baltimore, United StatesDepartment of Physiology, Johns Hopkins University School of Medicine, Baltimore, United States; Center for Metabolism and Obesity Research, Johns Hopkins University School of Medicine, Baltimore, United StatesOrgan function declines with age, and large-scale transcriptomic analyses have highlighted differential aging trajectories across tissues. The mechanism underlying shared and organ-selective functional changes across the lifespan, however, still remains poorly understood. Given the central role of mitochondria in powering cellular processes needed to maintain tissue health, we therefore undertook a systematic assessment of respiratory activity across 33 different tissues in young (2.5 months) and old (20 months) mice of both sexes. Our high-resolution mitochondrial respiration atlas reveals: (1) within any group of mice, mitochondrial activity varies widely across tissues, with the highest values consistently seen in heart, brown fat, and kidney; (2) biological sex is a significant but minor contributor to mitochondrial respiration, and its contributions are tissue-specific, with major differences seen in the pancreas, stomach, and white adipose tissue; (3) age is a dominant factor affecting mitochondrial activity, especially across most brain regions, different fat depots, skeletal muscle groups, eyes, and different regions of the gastrointestinal tract; (4) age effects can be sex- and tissue-specific, with some of the largest effects seen in pancreas, heart, adipose tissue, and skeletal muscle; and (5) while aging alters the functional trajectories of mitochondria in a majority of tissues, some are remarkably resilient to age-induced changes. Altogether, our data provide the most comprehensive compendium of mitochondrial respiration and illuminate functional signatures of aging across diverse tissues and organ systems.https://elifesciences.org/articles/96926mitochondriarespiration atlassexaging
spellingShingle Dylan C Sarver
Muzna Saqib
Fangluo Chen
G William Wong
Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age
eLife
mitochondria
respiration atlas
sex
aging
title Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age
title_full Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age
title_fullStr Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age
title_full_unstemmed Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age
title_short Mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age
title_sort mitochondrial respiration atlas reveals differential changes in mitochondrial function across sex and age
topic mitochondria
respiration atlas
sex
aging
url https://elifesciences.org/articles/96926
work_keys_str_mv AT dylancsarver mitochondrialrespirationatlasrevealsdifferentialchangesinmitochondrialfunctionacrosssexandage
AT muznasaqib mitochondrialrespirationatlasrevealsdifferentialchangesinmitochondrialfunctionacrosssexandage
AT fangluochen mitochondrialrespirationatlasrevealsdifferentialchangesinmitochondrialfunctionacrosssexandage
AT gwilliamwong mitochondrialrespirationatlasrevealsdifferentialchangesinmitochondrialfunctionacrosssexandage