Autophagy maintains the metabolism and function of young and old stem cells

Ho, Theodore T.; Warr, Matthew R.; Adelman, Emmalee R.; Lansinger, Olivia M.; Flach, Johanna; Verovskaya, Evgenia V.; Figueroa, Maria E.; Passegué, Emmanuelle

doi:10.1038/nature21388

Cited by 897Hematopoietic Stem Cell TransplantationAutophagy in Disease and TherapyMesenchymal stem cell research

Autophagy maintains the metabolism and function of young and old stem cells

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Ho, Theodore T., Warr, Matthew R., Adelman, Emmalee R., Lansinger, Olivia M., Flach, Johanna, Verovskaya, Evgenia V., Figueroa, Maria E., Passegué, Emmanuelle·2017·Nature

DOI 10.1038/nature21388PMC PMC5344718

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Abstract

With age, haematopoietic stem cells lose their ability to regenerate the blood system, and promote disease development. Autophagy is associated with health and longevity, and is critical for protecting haematopoietic stem cells from metabolic stress. Here we show that loss of autophagy in haematopoietic stem cells causes accumulation of mitochondria and an activated metabolic state, which drives accelerated myeloid differentiation mainly through epigenetic deregulations, and impairs haematopoietic stem-cell self-renewal activity and regenerative potential. Strikingly, most haematopoietic stem cells in aged mice share these altered metabolic and functional features. However, approximately one-third of aged haematopoietic stem cells exhibit high autophagy levels and maintain a low metabolic state with robust long-term regeneration potential similar to healthy young haematopoietic stem cells. Our results demonstrate that autophagy actively suppresses haematopoietic stem-cell metabolism by clearing active, healthy mitochondria to maintain quiescence and stemness, and becomes increasingly necessary with age to preserve the regenerative capacity of old haematopoietic stem cells.

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During ageing, tissue regenerative functions decline, in part due to stem cell-intrinsic accumulation of damage, functional decay of niche cells and increased inflammation (inflammageing) through uncharacterized mechanisms.
“During ageing, tissue regenerative functions decline, in part due to stem cell-intrinsic accumulation of damage (for example, DNA damage, loss of proteostasis and oxidative damage), functional decay of niche cells and increased inflammation (inflammageing)4–9 through uncharacterized mechanisms.”
From Senescence atlas reveals an aged-like inflamed niche that blunts muscle regeneration (2023) · cites this paper as [7]
The Abstract (page not specified) says that ageing reduces tissue function alongside stem-cell activity and that aged hematopoietic stem cells lose regenerative ability. The Discussion and Extended Data (pages not specified) describe stem-cell-intrinsic metabolic changes and an adverse ageing bone-marrow environment. Our copy does not establish functional decay of niche cells or increased inflammation as contributors, and it identifies an autophagy mechanism rather than leaving the mechanism wholly uncharacterized. (LLM, conf=0.84)
Experimental — accuracy not yet measured
The functional heterogeneity of the HSC population rises with age.
“the functional heterogeneity of the HSC population increases with age.”
From Aging of hematopoietic stem cells (2018) · cites this paper as [33]
Individual HSCs in aged mice behave very differently from one another.
“individual HSCs behave very differently.”
From Aging of hematopoietic stem cells (2018) · cites this paper as [33]
Aged mice have an overall larger HSC pool.
“in aged mice that display an overall increase in HSC pool size”
From Aging of hematopoietic stem cells (2018) · cites this paper as [33]
A large fraction of aged HSCs have impaired autophagy.
“A large fraction of aged HSCs show impaired levels of autophagy.”
From Aging of hematopoietic stem cells (2018) · cites this paper as [33]

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Authors: Ho, T. T., Warr, M. R., Adelman, E. R., Lansinger, O. M., Flach, J., Verovskaya, E. V., Figueroa, M. E., & Passegué, E.
Affiliations: University of California, San Francisco (US)
University of Michigan (US)
ORCID: Ho, Theodore T.
Warr, Matthew R.
Adelman, Emmalee R.
Lansinger, Olivia M.
Flach, Johanna
Verovskaya, Evgenia V.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2017-03
Volume: 543
Issue: 7644
Pages: 205-210
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature21388
PMC: PMC5344718
OpenAlex: W2592615787
Cited by: 896
References: 42
Citations by year: 2026: 58 · 2025: 67 · 2024: 95 · 2023: 103 · 2022: 107 · 2021: 124 · 2020: 118 · 2019: 93 · 2018: 90 · 2017: 40
FWCI: 71.87
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institute on Aging (T32AG000114)
National Heart, Lung, and Blood Institute (R01HL126947)
National Cancer Institute (R01CA184014)
National Institute of General Medical Sciences (T32GM008284)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK063720)
Topics: Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
Keywords: autophagy, hematopoietic stem cells, cellular aging, stem cell self-renewal, mitochondrial accumulation, myeloid differentiation, epigenetic regulation, metabolic stress, regenerative capacity, stem cell quiescence
MeSH terms: Cell Self Renewal, Animals, Autophagy, Female, Hematopoiesis, Hematopoietic Stem Cells, Male, Mitochondria, Cellular Senescence, Myeloid Cells, Epigenesis, Genetic, Mice

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