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Cited by 89Neuroinflammation and Neurodegeneration MechanismsAutophagy in Disease and TherapyPhagocytosis and Immune Regulation

Microglial phagocytosis dysfunction in stroke is driven by energy depletion and induction of autophagy

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Beccari, Sol, Sierra-Torre, Virginia, Valero, Jorge, Pereira-Iglesias, Marta, García-Zaballa, Mikel, Soria, Federico N., De Las Heras-Garcia, Laura, Carretero-Guillen, Alejandro +17 more·2023·Autophagy
DOI 10.1080/15548627.2023.2165313PMC PMC10283420

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Abstract

ABSTRACT Microglial phagocytosis is rapidly emerging as a therapeutic target in neurodegenerative and neurological disorders. An efficient removal of cellular debris is necessary to prevent buildup damage of neighbor neurons and the development of an inflammatory response. As the brain professional phagocytes, microglia are equipped with an array of mechanisms that enable them to recognize and degrade several types of cargo, including neurons undergoing apoptotic cell death. While microglia are very competent phagocytes of apoptotic cells under physiological conditions, here we report their dysfunction in mouse and monkey ( Macaca fascicularis and Callithrix jacchus ) models of stroke by transient occlusion of the medial cerebral artery (tMCAo). The impairment of both engulfment and degradation was related to energy depletion triggered by oxygen and nutrients deprivation (OND), which led to reduced process motility, lysosomal depletion, and the induction of a protective autophagy response in microglia. Basal autophagy, which is in charge of removing and recycling intracellular elements, was critical to maintain microglial physiology, including survival and phagocytosis, as we determined both in vivo and in vitro using knock-out models of autophagy genes and the autophagy inhibitor MRT68921. Notably, the autophagy inducer rapamycin partially prevented the phagocytosis impairment induced by tMCAo in vivo but not by OND in vitro. These results suggest a more complex role of microglia in stroke than previously acknowledged, classically related to the inflammatory response. In contrast, here we demonstrate the impairment of apoptotic cell phagocytosis, a microglial function critical for brain recovery. We propose that phagocytosis is a therapeutic target yet to be explored and provide evidence that it can be modulated in vivo using rapamycin, setting the stage for future therapies for stroke patients.

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  • Partial inhibition of mTOR can pause mouse blastocyst development, preserving stemness for weeks in culture.

    “Partial inhibition of mTOR, which mimics nutrient starvation and activates autophagy, can pause mouse blastocyst development, preserving “stemness” for weeks in culture.16”

    From The lysosome and proteostatic stress at the intersection of pediatric neurological disorders and adult neurodegenerative diseases (2025) · cites this paper as [16]

    The Results section, “Rapamycin prevents phagocytosis impairment” (page unavailable), discusses mTOR inhibition and autophagy in a mouse stroke model. Searches for blastocysts, stemness, and paused embryonic development found no passage in our copy addressing whether mTOR inhibition preserves mouse blastocysts for weeks in culture. (LLM, conf=0.78)

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Authors
Beccari, S., Sierra-Torre, V., Valero, J., Pereira-Iglesias, M., García-Zaballa, M., Soria, F. N., De Las Heras-Garcia, L., Carretero-Guillen, A., Capetillo-Zarate, E., Domercq, M., Huguet, P. R., Ramonet, D., Osman, A., Han, W., Dominguez, C., Faust, T. E., Touzani, O., Pampliega, O., Boya, P., Schafer, D., Mariño, G., Canet-Soulas, E., Blomgren, K., Plaza-Zabala, A., & Sierra, A.
Affiliations
  • University of the Basque Country (ES)
  • Glial Cell Biology Labb, Department of Biochemistry and Molecular Biology, Achucarro Basque Center for Neuroscience, 48940, Leioa, Bizkaia, Spain
  • Ikerbasque (ES)
  • Lyon 1 Université (FR)
  • Karolinska Institutet (SE)
  • University of Massachusetts Chan Medical School (US)
  • Centre National de la Recherche Scientifique (FR)
  • University of Fribourg (CH)
  • INSERM U1060 CarMeN, Université Claude Bernard Lyon 1 - IRIS team, CarMeN, bat. B13, gpt hosp. Est, 59 bld Pinel, 69500, Bron, Auvergne-Rhône-Alpes, France
  • Karolinska University Hospital (SE)
Corresponding author
Sierra, Amanda
ORCID
Venue
Autophagy
Publisher
Informa UK Limited
Published
2023-01-20
Volume
19
Issue
7
Pages
1952-1981
ISSN
  • 1554-8627 (ISSN-L)
  • 1554-8635
DOI
10.1080/15548627.2023.2165313
PMC
PMC10283420
OpenAlex
W4313892827
Cited by
89
References
13
Citations by year
2026: 20 · 2025: 30 · 2024: 33 · 2023: 6
FWCI
9.17
Type
journal article
Language
en
Open access
Licence
Locations
  • Autophagy (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Hispana (publishedVersion, other-oa)
  • HAL (submittedVersion, cc-by-nc-nd)
  • Communities in ADDI (University of the Basque Country) (submittedVersion, cc-by-nc-nd)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by-nc-nd)
  • Gredos (University of Salamanca) (submittedVersion, other-oa)
  • Hispana (submittedVersion, cc-by-nc-nd)
Funders
  • Basque Government (ELKARTEK KK-2020/00034;, PIBA 2020_1_0030)
  • Spanish Ministry of Science and Innovation (RYC-2016–20480, RTI2018-099267-B-I00, RYC-2013-12817, RTI2018–097948-A-100)
  • Tatiana Foundation (P-048-FTPGB 2018)
Topics
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
  • Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Keywords
microglial phagocytosis, stroke, energy depletion, macroautophagy, rapamycin, transient middle cerebral artery occlusion, microglial motility, neuroinflammation, therapeutic target, single-cell RNA sequencing, marmoset model
MeSH terms
Beclin-1, Animals, Autophagy, Oxygen, Phagocytosis, Microglia, Sirolimus, Stroke, Mice

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