Cited by 184Telomeres, Telomerase, and SenescenceRetinal Diseases and TreatmentsAngiogenesis and VEGF in Cancer

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Pathological angiogenesis in retinopathy engages cellular senescence and is amenable to therapeutic elimination via BCL-xL inhibition

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Crespo-Garcia, Sergio, Tsuruda, Pamela R., Dejda, Agnieszka, Ryan, Rathi D., Fournier, Frederik, Chaney, Shawnta Y., Pilon, Frederique, Dogan, Taner, Cagnone, Gael, Patel, Priyanka, Buscarlet, Manuel, Dasgupta, Sonali, Girouard, Gabrielle, Rao, Surabhi R., Wilson, Ariel M., O’Brien, Robert, Juneau, Rachel, Guber, Vera, Dubrac, Alexandre, Beausejour, Christian, Armstrong, Scott, Mallette, Frederick A., Yohn, Christopher B., Joyal, Jean-Sebastien, Marquess, Dan, Beltran, Pedro J., Sapieha, Przemyslaw·2021·Cell Metabolism

DOI 10.1016/j.cmet.2021.01.011

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Abstract

Attenuating pathological angiogenesis in diseases characterized by neovascularization such as diabetic retinopathy has transformed standards of care. Yet little is known about the molecular signatures discriminating physiological blood vessels from their diseased counterparts, leading to off-target effects of therapy. We demonstrate that in contrast to healthy blood vessels, pathological vessels engage pathways of cellular senescence. Senescent (p16 INK4A-expressing) cells accumulate in retinas of patients with diabetic retinopathy and during peak destructive neovascularization in a mouse model of retinopathy. Using either genetic approaches that clear p16 INK4A-expressing cells or small molecule inhibitors of the anti-apoptotic protein BCL-xL, we show that senolysis suppresses pathological angiogenesis. Single-cell analysis revealed that subsets of endothelial cells with senescence signatures and expressing Col1a1 are no longer detected in BCL-xL-inhibitor-treated retinas, yielding a retina conducive to physiological vascular repair. These findings provide mechanistic evidence supporting the development of BCL-xL inhibitors as potential treatments for neovascular retinal disease.

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Authors: Crespo-Garcia, S., Tsuruda, P. R., Dejda, A., Ryan, R. D., Fournier, F., Chaney, S. Y., Pilon, F., Dogan, T., Cagnone, G., Patel, P., Buscarlet, M., Dasgupta, S., Girouard, G., Rao, S. R., Wilson, A. M., O’Brien, R., Juneau, R., Guber, V., Dubrac, A., Beausejour, C., Armstrong, S., Mallette, F. A., Yohn, C. B., Joyal, J.-S., Marquess, D., Beltran, P. J., & Sapieha, P.
Affiliations: Unity Biotechnology (United States) (US)
Hôpital Maisonneuve-Rosemont (CA)
Centre Hospitalier Universitaire Sainte-Justine (CA)
Corresponding author: Tsuruda, Pamela R.
Sapieha, Przemyslaw
ORCID: Dejda, Agnieszka
Chaney, Shawnta Y.
Buscarlet, Manuel
Dasgupta, Sonali
Wilson, Ariel M.
Juneau, Rachel
Guber, Vera
Dubrac, Alexandre
Beausejour, Christian
Yohn, Christopher B.
Beltran, Pedro J.
Sapieha, Przemyslaw
Venue: Cell Metabolism
Publisher: Elsevier BV
Published: 2021-04
Volume: 33
Issue: 4
Pages: 818-832.e7
ISSN: 1550-4131 (ISSN-L)
DOI: 10.1016/j.cmet.2021.01.011
OpenAlex: W3126392088
Cited by: 182
References: 81
Citations by year: 2026: 21 · 2025: 55 · 2024: 44 · 2023: 30 · 2022: 28 · 2021: 4
FWCI: 17.10
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 370 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell Metabolism (publishedVersion)
PubMed (publishedVersion)
Funders: Université de Montréal
Canadian Diabetes Association (DI-3-18-5444-PS)
Canadian Institutes of Health Research (148460)
Fonds de Recherche du Québec - Santé
Canada Research Chairs
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: pathological angiogenesis, diabetic retinopathy, cellular senescence, BCL-XL inhibition, senolysis, p16INK4a, neovascularization, endothelial cells, COL1A1, anti-apoptotic therapy
MeSH terms: Collagen Type I, alpha 1 Chain, Animals, Disease Models, Animal, Female, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Neovascularization, Pathologic, Retinal Diseases, Tacrolimus, Cellular Senescence, Apoptosis, Cyclin-Dependent Kinase Inhibitor p16, Endothelial Cells, Flavonols, bcl-X Protein, Mice

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Pathological angiogenesis in retinopathy engages cellular senescence and is amenable to therapeutic elimination via BCL-xL inhibition

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