Effects of the VIVIFRAIL Exercise Protocol on Circulatory and Intracellular Peripheral Mediators Bridging Mitochondrial Dynamics and Inflammation in Robust and Frail Older People

ABSTRACT Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs through a complex, yet poorly characterized network of multi‐organ interactions involving mitochondrial, inflammatory, and cell death/survival path...

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Published inAging cell Vol. 24; no. 6; pp. e70029 - n/a
Main Authors Limanaqi, Fiona, Ferri, Evelyn, Ogno, Pasquale, Guerini, Franca Rosa, Mihali, Gabriela Alexandra, Lucchi, Tiziano, Clerici, Mario, Fenoglio, Chiara, D'Andrea, Laura, Marcello, Elena, Biasin, Mara, Arosio, Beatrice
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.06.2025
John Wiley and Sons Inc
Subjects
Aged
Aged, 80 and over
Aging
Analysis
Apoptosis
ccf‐mtDNA
Cell death
Cell survival
Chronic illnesses
cytokines
Down-regulation
Exercise
Exercise - physiology
Female
Frail Elderly
Frailty
Gene expression
Gerontology
Humans
inflammaging
Inflammation
Inflammation - blood
Inflammation - metabolism
Interleukin 10
Kinases
Leukocytes (mononuclear)
Leukocytes, Mononuclear - metabolism
Male
Mitochondria
Mitochondria - metabolism
Mitochondrial DNA
Mitochondrial Dynamics - physiology
mitophagy
Older people
peripheral blood cells
Peripheral blood mononuclear cells
Physical activity
RNA
United States > US
Wisconsin
inflammaging
mitophagy
mitochondria
ccf‐mtDNA
apoptosis
exercise
cytokines
peripheral blood cells
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Abstract ABSTRACT Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs through a complex, yet poorly characterized network of multi‐organ interactions involving mitochondrial, inflammatory, and cell death/survival pathways. Here, we comprehensively evaluated the 12‐week VIVIFRAIL multicomponent exercise protocol in physically frail (n = 16, mean age 81.4 ± 5.6) and robust (n = 50, mean‐age 73.6 ± 4.7) old individuals. Before (T0) and after (T1) the protocol, functional outcomes were assessed alongside a detailed exploratory analysis of mitochondrial, inflammatory, apoptotic, and neuro‐muscular mediators concerning their plasmatic/serum concentrations, and/or mRNA expression from peripheral blood mononuclear cells (PBMCs). Besides significant functional improvements across both groups, our findings highlighted unique and overlapping modulations of key biological pathways. Both groups showed refined mitochondrial integrity/turnover (upregulated mt‐ND1, downregulated TFAM, and ULK1), anti‐inflammatory responses (upregulated IL10, and TGF‐B, and downregulated IL6/IL10 mRNA ratio), as well as reduced cellular damage/apoptosis (reduced plasmatic ccf‐nDNA, downregulated BAX, and upregulated BCL‐2/BAX ratio). Plasmatic ccf‐mtDNA was significantly reduced in robust subjects, while plasmatic IL6 and IL6/IL10 ratio were reduced in frail subjects uniquely. Spearman correlations between physical improvements and biological pathway variations also suggested different adaptation mechanisms influenced not only by chronological age but also by frailty status. In conclusion, this study confirms the benefits of physical activity in the older population and provides novel insights into specific biological mediators of the mitochondria‐inflammation axis as key players in such effects. Moreover, our findings establish PBMCs as a valuable tool for monitoring the biological trajectories of aging and health‐promoting lifestyle interventions. Physical activity promotes functional improvements in both robust and physically frail older adults, driven by distinct adaptation mechanisms in the mitochondria‐inflammation axis that are influenced by age and frailty status.
AbstractList Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age-related declines. This occurs through a complex, yet poorly characterized network of multi-organ interactions involving mitochondrial, inflammatory, and cell death/survival pathways. Here, we comprehensively evaluated the 12-week VIVIFRAIL multicomponent exercise protocol in physically frail (n = 16, mean age 81.4 ± 5.6) and robust (n = 50, mean-age 73.6 ± 4.7) old individuals. Before (T0) and after (T1) the protocol, functional outcomes were assessed alongside a detailed exploratory analysis of mitochondrial, inflammatory, apoptotic, and neuro-muscular mediators concerning their plasmatic/serum concentrations, and/or mRNA expression from peripheral blood mononuclear cells (PBMCs). Besides significant functional improvements across both groups, our findings highlighted unique and overlapping modulations of key biological pathways. Both groups showed refined mitochondrial integrity/turnover (upregulated mt-ND1, downregulated TFAM, and ULK1), anti-inflammatory responses (upregulated IL10, and TGF-B, and downregulated IL6/IL10 mRNA ratio), as well as reduced cellular damage/apoptosis (reduced plasmatic ccf-nDNA, downregulated BAX, and upregulated BCL-2/BAX ratio). Plasmatic ccf-mtDNA was significantly reduced in robust subjects, while plasmatic IL6 and IL6/IL10 ratio were reduced in frail subjects uniquely. Spearman correlations between physical improvements and biological pathway variations also suggested different adaptation mechanisms influenced not only by chronological age but also by frailty status. In conclusion, this study confirms the benefits of physical activity in the older population and provides novel insights into specific biological mediators of the mitochondria-inflammation axis as key players in such effects. Moreover, our findings establish PBMCs as a valuable tool for monitoring the biological trajectories of aging and health-promoting lifestyle interventions.Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age-related declines. This occurs through a complex, yet poorly characterized network of multi-organ interactions involving mitochondrial, inflammatory, and cell death/survival pathways. Here, we comprehensively evaluated the 12-week VIVIFRAIL multicomponent exercise protocol in physically frail (n = 16, mean age 81.4 ± 5.6) and robust (n = 50, mean-age 73.6 ± 4.7) old individuals. Before (T0) and after (T1) the protocol, functional outcomes were assessed alongside a detailed exploratory analysis of mitochondrial, inflammatory, apoptotic, and neuro-muscular mediators concerning their plasmatic/serum concentrations, and/or mRNA expression from peripheral blood mononuclear cells (PBMCs). Besides significant functional improvements across both groups, our findings highlighted unique and overlapping modulations of key biological pathways. Both groups showed refined mitochondrial integrity/turnover (upregulated mt-ND1, downregulated TFAM, and ULK1), anti-inflammatory responses (upregulated IL10, and TGF-B, and downregulated IL6/IL10 mRNA ratio), as well as reduced cellular damage/apoptosis (reduced plasmatic ccf-nDNA, downregulated BAX, and upregulated BCL-2/BAX ratio). Plasmatic ccf-mtDNA was significantly reduced in robust subjects, while plasmatic IL6 and IL6/IL10 ratio were reduced in frail subjects uniquely. Spearman correlations between physical improvements and biological pathway variations also suggested different adaptation mechanisms influenced not only by chronological age but also by frailty status. In conclusion, this study confirms the benefits of physical activity in the older population and provides novel insights into specific biological mediators of the mitochondria-inflammation axis as key players in such effects. Moreover, our findings establish PBMCs as a valuable tool for monitoring the biological trajectories of aging and health-promoting lifestyle interventions.
Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs through a complex, yet poorly characterized network of multi‐organ interactions involving mitochondrial, inflammatory, and cell death/survival pathways. Here, we comprehensively evaluated the 12‐week VIVIFRAIL multicomponent exercise protocol in physically frail (n = 16, mean age 81.4 ± 5.6) and robust (n = 50, mean‐age 73.6 ± 4.7) old individuals. Before (T0) and after (T1) the protocol, functional outcomes were assessed alongside a detailed exploratory analysis of mitochondrial, inflammatory, apoptotic, and neuro‐muscular mediators concerning their plasmatic/serum concentrations, and/or mRNA expression from peripheral blood mononuclear cells (PBMCs). Besides significant functional improvements across both groups, our findings highlighted unique and overlapping modulations of key biological pathways. Both groups showed refined mitochondrial integrity/turnover (upregulated mt‐ND1, downregulated TFAM, and ULK1), anti‐inflammatory responses (upregulated IL10, and TGF‐B, and downregulated IL6/IL10 mRNA ratio), as well as reduced cellular damage/apoptosis (reduced plasmatic ccf‐nDNA, downregulated BAX, and upregulated BCL‐2/BAX ratio). Plasmatic ccf‐mtDNA was significantly reduced in robust subjects, while plasmatic IL6 and IL6/IL10 ratio were reduced in frail subjects uniquely. Spearman correlations between physical improvements and biological pathway variations also suggested different adaptation mechanisms influenced not only by chronological age but also by frailty status. In conclusion, this study confirms the benefits of physical activity in the older population and provides novel insights into specific biological mediators of the mitochondria‐inflammation axis as key players in such effects. Moreover, our findings establish PBMCs as a valuable tool for monitoring the biological trajectories of aging and health‐promoting lifestyle interventions.
ABSTRACT Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs through a complex, yet poorly characterized network of multi‐organ interactions involving mitochondrial, inflammatory, and cell death/survival pathways. Here, we comprehensively evaluated the 12‐week VIVIFRAIL multicomponent exercise protocol in physically frail (n = 16, mean age 81.4 ± 5.6) and robust (n = 50, mean‐age 73.6 ± 4.7) old individuals. Before (T0) and after (T1) the protocol, functional outcomes were assessed alongside a detailed exploratory analysis of mitochondrial, inflammatory, apoptotic, and neuro‐muscular mediators concerning their plasmatic/serum concentrations, and/or mRNA expression from peripheral blood mononuclear cells (PBMCs). Besides significant functional improvements across both groups, our findings highlighted unique and overlapping modulations of key biological pathways. Both groups showed refined mitochondrial integrity/turnover (upregulated mt‐ND1, downregulated TFAM, and ULK1), anti‐inflammatory responses (upregulated IL10, and TGF‐B, and downregulated IL6/IL10 mRNA ratio), as well as reduced cellular damage/apoptosis (reduced plasmatic ccf‐nDNA, downregulated BAX, and upregulated BCL‐2/BAX ratio). Plasmatic ccf‐mtDNA was significantly reduced in robust subjects, while plasmatic IL6 and IL6/IL10 ratio were reduced in frail subjects uniquely. Spearman correlations between physical improvements and biological pathway variations also suggested different adaptation mechanisms influenced not only by chronological age but also by frailty status. In conclusion, this study confirms the benefits of physical activity in the older population and provides novel insights into specific biological mediators of the mitochondria‐inflammation axis as key players in such effects. Moreover, our findings establish PBMCs as a valuable tool for monitoring the biological trajectories of aging and health‐promoting lifestyle interventions. Physical activity promotes functional improvements in both robust and physically frail older adults, driven by distinct adaptation mechanisms in the mitochondria‐inflammation axis that are influenced by age and frailty status.
ABSTRACT Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs through a complex, yet poorly characterized network of multi‐organ interactions involving mitochondrial, inflammatory, and cell death/survival pathways. Here, we comprehensively evaluated the 12‐week VIVIFRAIL multicomponent exercise protocol in physically frail (n = 16, mean age 81.4 ± 5.6) and robust (n = 50, mean‐age 73.6 ± 4.7) old individuals. Before (T0) and after (T1) the protocol, functional outcomes were assessed alongside a detailed exploratory analysis of mitochondrial, inflammatory, apoptotic, and neuro‐muscular mediators concerning their plasmatic/serum concentrations, and/or mRNA expression from peripheral blood mononuclear cells (PBMCs). Besides significant functional improvements across both groups, our findings highlighted unique and overlapping modulations of key biological pathways. Both groups showed refined mitochondrial integrity/turnover (upregulated mt‐ND1, downregulated TFAM, and ULK1), anti‐inflammatory responses (upregulated IL10, and TGF‐B, and downregulated IL6/IL10 mRNA ratio), as well as reduced cellular damage/apoptosis (reduced plasmatic ccf‐nDNA, downregulated BAX, and upregulated BCL‐2/BAX ratio). Plasmatic ccf‐mtDNA was significantly reduced in robust subjects, while plasmatic IL6 and IL6/IL10 ratio were reduced in frail subjects uniquely. Spearman correlations between physical improvements and biological pathway variations also suggested different adaptation mechanisms influenced not only by chronological age but also by frailty status. In conclusion, this study confirms the benefits of physical activity in the older population and provides novel insights into specific biological mediators of the mitochondria‐inflammation axis as key players in such effects. Moreover, our findings establish PBMCs as a valuable tool for monitoring the biological trajectories of aging and health‐promoting lifestyle interventions.
Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs through a complex, yet poorly characterized network of multi‐organ interactions involving mitochondrial, inflammatory, and cell death/survival pathways. Here, we comprehensively evaluated the 12‐week VIVIFRAIL multicomponent exercise protocol in physically frail ( n  = 16, mean age 81.4 ± 5.6) and robust ( n  = 50, mean‐age 73.6 ± 4.7) old individuals. Before (T0) and after (T1) the protocol, functional outcomes were assessed alongside a detailed exploratory analysis of mitochondrial, inflammatory, apoptotic, and neuro‐muscular mediators concerning their plasmatic/serum concentrations, and/or mRNA expression from peripheral blood mononuclear cells (PBMCs). Besides significant functional improvements across both groups, our findings highlighted unique and overlapping modulations of key biological pathways. Both groups showed refined mitochondrial integrity/turnover (upregulated mt‐ND1 , downregulated TFAM , and ULK1 ), anti‐inflammatory responses (upregulated IL10 , and TGF‐B , and downregulated IL6/IL10 mRNA ratio), as well as reduced cellular damage/apoptosis (reduced plasmatic ccf‐nDNA, downregulated BAX , and upregulated BCL‐2/BAX ratio). Plasmatic ccf‐mtDNA was significantly reduced in robust subjects, while plasmatic IL6 and IL6/IL10 ratio were reduced in frail subjects uniquely. Spearman correlations between physical improvements and biological pathway variations also suggested different adaptation mechanisms influenced not only by chronological age but also by frailty status. In conclusion, this study confirms the benefits of physical activity in the older population and provides novel insights into specific biological mediators of the mitochondria‐inflammation axis as key players in such effects. Moreover, our findings establish PBMCs as a valuable tool for monitoring the biological trajectories of aging and health‐promoting lifestyle interventions. Physical activity promotes functional improvements in both robust and physically frail older adults, driven by distinct adaptation mechanisms in the mitochondria‐inflammation axis that are influenced by age and frailty status.
Audience Academic
Author Lucchi, Tiziano
Fenoglio, Chiara
D'Andrea, Laura
Guerini, Franca Rosa
Ferri, Evelyn
Biasin, Mara
Arosio, Beatrice
Limanaqi, Fiona
Marcello, Elena
Ogno, Pasquale
Mihali, Gabriela Alexandra
Clerici, Mario
AuthorAffiliation 6 Department of Biomedical, Surgical and Dental Sciences University of Milan Milan Italy
8 Department of Clinical Sciences and Community Health University of Milan Milan Italy
4 Asst Fatebenefratelli Sacco Milan Italia Italy
3 IRCCS Fondazione Don Carlo Gnocchi ONLUS Milan Italy
2 IRCCS Fondazione Ca' Granda Ospedale Maggiore Policlinico Milan Italy
5 Department of Pathophysiology and Transplantation University of Milan Milan Italy
7 Department of Pharmacological and Biomolecular Sciences “Rodolfo Paoletti” University of Milan Milan Italy
1 Department of Biomedical and Clinical Sciences University of Milan Milan Italy
AuthorAffiliation_xml – name: 2 IRCCS Fondazione Ca' Granda Ospedale Maggiore Policlinico Milan Italy
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/40033883$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2025 The Author(s). published by Anatomical Society and John Wiley & Sons Ltd.
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– notice: COPYRIGHT 2025 John Wiley & Sons, Inc.
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Issue 6
Keywords inflammaging
mitophagy
mitochondria
ccf‐mtDNA
apoptosis
exercise
cytokines
peripheral blood cells
Language English
License Attribution
2025 The Author(s). Aging Cell published by Anatomical Society and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Notes Fiona Limanaqi and Evelyn Ferri First authors equally contributed.
Mara Biasin and Beatrice Arosio Senior authors equally contributed.
Funding
This work was supported by Fondazione Cariplo, 2017‐0622, by grants from Fondazione Romeo and Enrica Invernizzi, and by the Italian Ministry of Health, under the Aging Network of Italian Research Hospitals (IRCCS), RCR‐2022‐23682286 (Ricerca Corrente Reti 2022).
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Funding: This work was supported by Fondazione Cariplo, 2017‐0622, by grants from Fondazione Romeo and Enrica Invernizzi, and by the Italian Ministry of Health, under the Aging Network of Italian Research Hospitals (IRCCS), RCR‐2022‐23682286 (Ricerca Corrente Reti 2022).
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Snippet ABSTRACT Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs...
Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs through a...
Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age-related declines. This occurs through a...
ABSTRACT Physical exercise has been associated with healthier aging trajectories, potentially preventing or mitigating age‐related declines. This occurs...
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SubjectTerms Aged
Aged, 80 and over
Aging
Analysis
Apoptosis
ccf‐mtDNA
Cell death
Cell survival
Chronic illnesses
cytokines
Down-regulation
Exercise
Exercise - physiology
Female
Frail Elderly
Frailty
Gene expression
Gerontology
Humans
inflammaging
Inflammation
Inflammation - blood
Inflammation - metabolism
Interleukin 10
Kinases
Leukocytes (mononuclear)
Leukocytes, Mononuclear - metabolism
Male
Mitochondria
Mitochondria - metabolism
Mitochondrial DNA
Mitochondrial Dynamics - physiology
mitophagy
Older people
peripheral blood cells
Peripheral blood mononuclear cells
Physical activity
RNA
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Title Effects of the VIVIFRAIL Exercise Protocol on Circulatory and Intracellular Peripheral Mediators Bridging Mitochondrial Dynamics and Inflammation in Robust and Frail Older People
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Facel.70029
https://www.ncbi.nlm.nih.gov/pubmed/40033883
https://www.proquest.com/docview/3217345627
https://www.proquest.com/docview/3173407381
https://pubmed.ncbi.nlm.nih.gov/PMC12151904
Volume 24
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