Pathological angiogenesis in retinopathy engages cellular senescence and is amenable to therapeutic elimination via BCL-xL inhibition
Open accessAbstract
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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A subset of senescent endothelial cells in the retina highly express Col1a1 and can be specifically eliminated by a senolytic drug.
“They identified a subset of senescent endothelial cells in the retina, which highly express Col1a1, that can be specifically eliminated by a senolytic drug [41].”
From The heterogeneity of cellular senescence: insights at the single-cell level (2023) · cites this paper as [41]
Cites
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
Comprehensive Integration of Single-Cell Data
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019) · Cell · doi:10.1016/j.cell.2019.05.031 · Cited by 15,453 · see citing works
GSVA: gene set variation analysis for microarray and RNA-Seq data
Hänzelmann, S., Castelo, R., & Guinney, J. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-7 · Cited by 15,440 · see citing works
Near-optimal probabilistic RNA-seq quantification
Bray, N. L., Pimentel, H., Melsted, P., & Pachter, L. (2016) · Nature Biotechnology · doi:10.1038/nbt.3519 · Cited by 9,723 · see citing works
A biomarker that identifies senescent human cells in culture and in aging skin in vivo.
Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., & Pereira-Smith, O. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9363 · Cited by 7,477 · see citing works
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · see citing works
Lang, G. E., Vaiser, A., Snyder, W. B., & Lynn, J. R. (1974) · doi:10.1159/isbn.978-3-318-01439-6 · Cited by 5,583 · see citing works
Wong, W. L., Su, X., Li, X., Cheung, C. M. G., Klein, R., Cheng, C., & Wong, T. Y. (2014) · The Lancet Global Health · doi:10.1016/s2214-109x(13)70145-1 · Cited by 5,403 · see citing works
Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq
Tirosh, I., Izar, B., Prakadan, S. M., Wadsworth, M. H., Treacy, D., Trombetta, J. J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al. (2016) · Science · doi:10.1126/science.aad0501 · Cited by 4,944 · see citing works
Hafemeister, C., & Satija, R. (2019) · Genome Biology · doi:10.1186/s13059-019-1874-1 · Cited by 4,479 · see citing works
Cellular senescence: when bad things happen to good cells
Campisi, J., & d'Adda di Fagagna, F. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2233 · Cited by 4,441 · see citing works
Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt
Durinck, S., Spellman, P. T., Birney, E., & Huber, W. K. (2009) · Nature Protocols · doi:10.1038/nprot.2009.97 · Cited by 4,081 · see citing works
Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences
Soneson, C., Love, M. I., & Robinson, M. D. (2015) · F1000Research · doi:10.12688/f1000research.7563.1 · Cited by 3,929 · see citing works
Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders
Baker, D. J., Wijshake, T., Tchkonia, T., LeBrasseur, N. K., Childs, B. G., van de Sluis, B., Kirkland, J. L., & van Deursen, J. M. (2011) · Nature · doi:10.1038/nature10600 · Cited by 3,670 · see citing works
ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets
Souers, A. J., Leverson, J. D., Boghaert, E. R., Ackler, S. L., Catron, N. D., Chen, J., Dayton, B. D., Ding, H., Enschede, S. H., Fairbrother, W. J., et al. (2013) · Nature Medicine · doi:10.1038/nm.3048 · Cited by 3,058 · see citing works
Naturally occurring p16Ink4a-positive cells shorten healthy lifespan
Baker, D. J., Childs, B. G., Durik, M., Wijers, M. E., Sieben, C. J., Zhong, J., A. Saltness, R., Jeganathan, K. B., Verzosa, G. C., Pezeshki, A., et al. (2016) · Nature · doi:10.1038/nature16932 · Cited by 2,891 · see citing works
VEGF in signaling and disease: beyond discovery and development
Apte, R. S., Chen, D. S., & Ferrara, N. (2019) · Cell · doi:10.1016/j.cell.2019.01.021 · Cited by 2,721 · see citing works
The role of senescent cells in ageing
van Deursen, J. M. (2014) · Nature · doi:10.1038/nature13193 · Cited by 2,623 · see citing works
Cellular senescence in aging and age-related disease: from mechanisms to therapy
Childs, B. G., Durik, M., Baker, D. J., & van Deursen, J. M. (2015) · Nature Medicine · doi:10.1038/nm.4000 · Cited by 2,363 · see citing works
Regulation of apoptosis in health and disease: the balancing act of BCL-2 family proteins
Singh, R., Letai, A., & Sarosiek, K. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0089-8 · Cited by 2,111 · see citing works
Clearance of senescent cells by ABT263 rejuvenates aged hematopoietic stem cells in mice
Chang, J., Wang, Y., Shao, L., Laberge, R.-M., Demaria, M., Campisi, J., Janakiraman, K., Sharpless, N. E., Ding, S., Feng, W., et al. (2016) · Nature Medicine · doi:10.1038/nm.4010 · Cited by 1,819 · see citing works
Senescence in Health and Disease
He, S., & Sharpless, N. E. (2017) · Cell · doi:10.1016/j.cell.2017.05.015 · Cited by 1,766 · see citing works
Antonetti, D. A., Klein, R., & Gardner, T. W. (2012) · New England Journal of Medicine · doi:10.1056/nejmra1005073 · Cited by 1,659 · see citing works
Oxygen-induced retinopathy in the mouse.
Smith, L. E. H., Wesolowski, E., McLellan, A., Kostyk, S. K., D’Amato, R. J., Sullivan, R., & D'Amore, P. A. (1994) · PubMed · Cited by 1,627 · see citing works
Cellular senescence mediates fibrotic pulmonary disease
Schafer, M. J., White, T. A., Iijima, K., Haak, A. J., Ligresti, G., Atkinson, E. J., Oberg, A. L., Birch, J., Salmonowicz, H., Zhu, Y., et al. (2017) · Nature Communications · doi:10.1038/ncomms14532 · Cited by 1,613 · see citing works
Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss
Lee, R. Y., Wong, T. Y., & Sabanayagam, C. (2015) · Eye and Vision · doi:10.1186/s40662-015-0026-2 · Cited by 1,588 · see citing works
Jeon, O. H., Kim, C., Laberge, R.-M., Demaria, M., Rathod, S., Vasserot, A. P., Chung, J. W., Kim, D. H., Poon, Y., David, N., et al. (2017) · Nature Medicine · doi:10.1038/nm.4324 · Cited by 1,515 · see citing works
Baar, M. P., Brandt, R. M. C., Putavet, D. A., Klein, J. D. D., Derks, K. W. J., Bourgeois, B. R. M., Stryeck, S., Rijksen, Y., van Willigenburg, H., Feijtel, D. A., et al. (2017) · Cell · doi:10.1016/j.cell.2017.02.031 · Cited by 1,454 · see citing works
Hellström, A., Smith, L. E. H., & Dammann, O. (2013) · The Lancet · doi:10.1016/s0140-6736(13)60178-6 · Cited by 1,309 · see citing works
Senescent intimal foam cells are deleterious at all stages of atherosclerosis
Childs, B. G., Baker, D. J., Wijshake, T., Conover, C. A., Campisi, J., & van Deursen, J. M. (2016) · Science · doi:10.1126/science.aaf6659 · Cited by 1,195 · see citing works
The Prevalence of Diabetic Retinopathy Among Adults in the United States
Kempen, J. H., O'Colmain, B. J., Leske, M. C., Sm, H., Klein, R., Moss, S. E., Taylor, H. R., & Hamman, R. F. (2004) · Archives of Ophthalmology · doi:10.1001/archopht.122.4.552 · Cited by 1,151 · see citing works
Zhu, Y., Tchkonia, T., Fuhrmann‐Stroissnigg, H., Dai, H. M., Ling, Y. Y., Stout, M. B., Pirtskhalava, T., Giorgadze, N., Johnson, K. O., Giles, C. B., et al. (2016) · Aging Cell · doi:10.1111/acel.12445 · Cited by 1,148 · see citing works
Diabetic retinopathy: current understanding, mechanisms, and treatment strategies
Duh, E. J., Sun, J. K., & Stitt, A. W. (2017) · JCI Insight · doi:10.1172/jci.insight.93751 · Cited by 1,057 · see citing works
Energy limitation as a selective pressure on the evolution of sensory systems
Niven, J. E., & Laughlin, S. B. (2008) · Journal of Experimental Biology · doi:10.1242/jeb.017574 · Cited by 1,056 · see citing works
Directed elimination of senescent cells by inhibition of BCL-W and BCL-XL
Yosef, R., Pilpel, N., Tokarsky-Amiel, R., Biran, A., Ovadya, Y., Cohen, S., Vadai, E., Dassa, L., Shahar, E., Condiotti, R., et al. (2016) · Nature Communications · doi:10.1038/ncomms11190 · Cited by 1,032 · see citing works
Connor, K. M., SanGiovanni, J. P., Löfqvist, C., Aderman, C. M., Chen, J., Higuchi, A., Hong, S., Pravda, E. A., Majchrzak, S. F., Carper, D. A., et al. (2007) · Nature Medicine · doi:10.1038/nm1591 · Cited by 687 · see citing works
Mechanisms and Management of Retinopathy of Prematurity
Hartnett, M. E., & Penn, J. S. (2012) · New England Journal of Medicine · doi:10.1056/nejmra1208129 · Cited by 645 · see citing works
The Mouse Retina as an Angiogenesis Model
Stahl, A., Connor, K. M., Sapieha, P. S., Chen, J., Dennison, R. J., Krah, N. M., Seaward, M. R., Willett, K. L., Aderman, C. M., Guerin, K. I., et al. (2010) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.10-5176 · Cited by 610 · see citing works
Self-citationSecretion of vascular endothelial growth factor by primary human fibroblasts at senescence
Coppé, J.-P., Kauser, K., Campisi, J., & Beauséjour, C. M. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m603307200 · Cited by 604 · see citing works
Self-citationRisk of geographic atrophy in the comparison of age-related macular degeneration treatments trials
Grunwald, J. E., Daniel, E., Huang, J., Ying, G.-S., Maguire, M. G., Toth, C. A., Jaffe, G. J., Fine, S. L., Blodi, B., Klein, M. L., et al. (2014) · Ophthalmology · doi:10.1016/j.ophtha.2013.08.015 · Cited by 590 · see citing works
Tissue damage and senescence provide critical signals for cellular reprogramming in vivo
Mosteiro, L., Pantoja, C., Alcazar, N., Marión, R. M., Chondronasiou, D., Rovira, M., Fernandez-Marcos, P. J., Muñoz-Martin, M., Blanco-Aparicio, C., Pastor, J., et al. (2016) · Science · doi:10.1126/science.aaf4445 · Cited by 589 · see citing works
Molecular Classification and Comparative Taxonomics of Foveal and Peripheral Cells in Primate Retina
Peng, Y., Shekhar, K., Yan, W., Herrmann, D., Sappington, A., Bryman, G. S., van Zyl, T. A., Do, M. T. H., Regev, A., & Sanes, J. R. (2019) · Cell · doi:10.1016/j.cell.2019.01.004 · Cited by 465 · see citing works
Energy metabolism of rabbit retina as related to function: high cost of Na+ transport
Ames, A., Li, Y., Heher, E., & Kimble, C. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-03-00840.1992 · Cited by 458 · see citing works
Energy metabolism of the visual system
Wong‐Riley, M. T. T. (2010) · Eye and Brain · doi:10.2147/eb.s9078 · Cited by 456 · see citing works
Current Epidemiology of Diabetic Retinopathy and Diabetic Macular Edema
Ding, J., & Wong, T. Y. (2012) · Current Diabetes Reports · doi:10.1007/s11892-012-0283-6 · Cited by 445 · see citing works
Li, J. Q., Welchowski, T., Schmid, M. C., Mauschitz, M. M., Holz, F. G., & Finger, R. P. (2019) · British Journal of Ophthalmology · doi:10.1136/bjophthalmol-2019-314422 · Cited by 383 · see citing works
Endothelial Notch1 Activity Facilitates Metastasis
Wieland, E., Rodríguez‐Vita, J., Liebler, S. S., Mogler, C., Moll, I., Herberich, S. E., Espinet, E., Herpel, E., Menuchin, A., Chang-Claude, J. C., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.01.007 · Cited by 315 · see citing works
Fibrosis and diseases of the eye
Friedlander, M. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31030 · Cited by 300 · see citing works
Targeting senescent cells in translational medicine
Pàez‐Ribes, M., González‐Gualda, E., Doherty, G. J., & Muñoz‐Espín, D. (2019) · EMBO Molecular Medicine · doi:10.15252/emmm.201810234 · Cited by 289 · see citing works
Neutrophil extracellular traps target senescent vasculature for tissue remodeling in retinopathy
Binet, F., Cagnone, G., Crespo-Garcia, S., Hata, M., Neault, M., Dejda, A., Wilson, A. M., Buscarlet, M., Mawambo, G. T., Howard, J. P., et al. (2020) · Science · doi:10.1126/science.aay5356 · Cited by 283 · see citing works
Self-citationABT-199 (venetoclax) and BCL-2 inhibitors in clinical development
Cang, S., Iragavarapu, C., Savooji, J., Song, Y., & Liu, D. (2015) · Journal of Hematology & Oncology · doi:10.1186/s13045-015-0224-3 · Cited by 282 · see citing works
Impaired Cholesterol Efflux in Senescent Macrophages Promotes Age-Related Macular Degeneration
Sene, A., Khan, A. A., Cox, D., Nakamura, R. E. I., Santeford, A., Kim, B. M., Sidhu, R., Onken, M. D., Harbour, J. W., Hagbi-Levi, S., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.03.009 · Cited by 277 · see citing works
Retinopathy of prematurity: understanding ischemic retinal vasculopathies at an extreme of life
Sapieha, P. S., Joyal, J., Rivera, J. C., Kermorvant‐Duchemin, E., Sennlaub, F., Hardy, P., Lachapelle, P., & Chemtob, S. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42142 · Cited by 264 · see citing works
Self-citationVascular Cell Senescence Contributes to Blood–Brain Barrier Breakdown
Yamazaki, Y., Baker, D. J., Tachibana, M., Liu, C.-C., van Deursen, J. M., Brott, T. G., Bu, G., & Kanekiyo, T. (2016) · Stroke · doi:10.1161/strokeaha.115.010835 · Cited by 263 · see citing works
Senescence-associated secretory phenotype contributes to pathological angiogenesis in retinopathy
Oubaha, M., Miloudi, K., Dejda, A., Guber, V., Mawambo, G., Germain, M.-A., Bourdel, G., Popovic, N., Rezende, F. A., Kaufman, R. J., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf9440 · Cited by 259 · see citing works
Self-citationSenolytic therapies for healthy longevity.
van Deursen, J. M. (2019) · Science · doi:10.1126/science.aaw1299 · Cited by 237 · see citing works
INCIDENCE OF ENDOPHTHALMITIS RELATED TO INTRAVITREAL INJECTION OF BEVACIZUMAB AND RANIBIZUMAB
Fintak, D. R., Shah, G. K., Blinder, K. J., Regillo, C. D., Pollack, J. S., Heier, J. S., Hollands, H., & Sharma, S. (2008) · Retina · doi:10.1097/iae.0b013e3181884fd2 · Cited by 215 · see citing works
Ritter, M. R., Banin, E., Moreno, S. K., Aguilar, E., Dorrell, M. I., & Friedlander, M. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29683 · Cited by 212 · see citing works
Fukushima, Y., Okada, M., Kataoka, H., Hirashima, M., Yoshida, Y., Mann, F., Gomi, F., Nishida, K., Nishikawa, S., & Uemura, A. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44900 · Cited by 207 · see citing works
Growth of Geographic Atrophy in the Comparison of Age-related Macular Degeneration Treatments Trials
Grunwald, J. E., Pistilli, M., Ying, G., Maguire, M. G., Daniel, E., & Martin, D. F. (2014) · Ophthalmology · doi:10.1016/j.ophtha.2014.11.007 · Cited by 204 · see citing works
Vascular senescence in cardiovascular and metabolic diseases
Katsuumi, G., Shimizu, I., Yoshida, Y., & Minamino, T. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00018 · Cited by 196 · see citing works
Cellular senescence in the glaucomatous outflow pathway
Liton, P. B., Challa, P., Stinnett, S. S., Luna, C., Epstein, D. L., & González, P. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.06.005 · Cited by 195 · see citing works
Ames, A. (1992) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y92-257 · Cited by 187 · see citing works
Ischemic neurons prevent vascular regeneration of neural tissue by secreting semaphorin 3A
Joyal, J., Sitaras, N., Binet, F., Rivera, J. C., Stahl, A., Zaniolo, K., Shao, Z., Polosa, A., Zhu, T., Hamel, D., et al. (2011) · Blood · doi:10.1182/blood-2010-10-311589 · Cited by 182 · see citing works
Self-citationPathological neoangiogenesis depends on oxidative stress regulation by ATM
Okuno, Y., Nakamura-Ishizu, A., Otsu, K., Suda, T., & Kubota, Y. (2012) · Nature Medicine · doi:10.1038/nm.2846 · Cited by 152 · see citing works
Retinal Oxygen Utilization Measured by Hyperbaric Blackout
ANDERSON, B., & Saltzman, H. A. (1964) · Archives of Ophthalmology · doi:10.1001/archopht.1964.00970020794009 · Cited by 151 · see citing works
Computer-aided quantification of retinal neovascularization
Stahl, A., Connor, K. M., Sapieha, P. S., Willett, K. L., Krah, N. M., Dennison, R. J., Chen, J., Guerin, K. I., & Smith, L. E. H. (2009) · Angiogenesis · doi:10.1007/s10456-009-9155-3 · Cited by 141 · see citing works
Self-citationSenescence-associated beta-galactosidase histochemistry for the primate eye.
Mishima, K., Handa, J. T., Aotaki-Keen, A. E., Lutty, G. A., Morse, L. S., & Hjelmeland, L. M. (1999) · PubMed · Cited by 126 · see citing works
P16INK4a Upregulation Mediated by SIX6 Defines Retinal Ganglion Cell Pathogenesis in Glaucoma
Skowronska‐Krawczyk, D., Zhao, L., Zhu, J., Weinreb, R. N., Cao, G., Luo, J., Flagg, K., Patel, S. H., Wen, C. H., Krupa, M., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.027 · Cited by 102 · see citing works
RPE cell senescence: A key contributor to age-related macular degeneration
Kozlowski, M. R. (2012) · Medical Hypotheses · doi:10.1016/j.mehy.2012.01.018 · Cited by 101 · see citing works
Ishikawa, K., Yoshida, S., Kobayashi, Y., Zhou, Y., Nakama, T., Nakao, S., Sassa, Y., Oshima, Y., Niiro, H., Akashi, K., et al. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-15589 · Cited by 91 · see citing works
Bai, L., Chen, J., McEachern, D., Liu, L., Zhou, H., Aguilar, A., & Wang, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099404 · Cited by 83 · see citing works
Binet, F., Mawambo, G., Sitaras, N., Tetreault, N., Lapalme, E., Favret, S., Cerani, A., Leboeuf, D., Tremblay, S., Rezende, F., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.02.003 · Cited by 80 · see citing works
Self-citationEnergy requirements of glutamatergic pathways in rabbit retina
Ames, A., & Li, Y. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04234.1992 · Cited by 61 · see citing works
Ras pathway inhibition prevents neovascularization by repressing endothelial cell sprouting
Westenskow, P. D., Kurihara, T., Aguilar, E., Scheppke, E. L., Moreno, S. K., Wittgrove, C. M., Marchetti, V., Michael, I. P., Anand, S., Nagy, A., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci70230 · Cited by 60 · see citing works
ClusterMap: compare multiple single cell RNA-Seq datasets across different experimental conditions
Gao, X., Hu, D., Gogol, M., & Li, H. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz024 · Cited by 47 · see citing works
Treatment of Proliferative Diabetic Retinopathy
Little, H. L. (1985) · Ophthalmology · doi:10.1016/s0161-6420(85)34059-9 · Cited by 22 · see citing works
Ye, L., Yuan, G., Xu, F., Sun, Y.-L., Chen, Z., Chen, M., Li, T., Sun, P., Li, S., & Sun, J. (2014) · Tumor Biology · doi:10.1007/s13277-014-2980-z · Cited by 22 · see citing works
Reducing Treatment Burden in AMD
Apte, R. S. (2020) · Cell · doi:10.1016/j.cell.2020.02.028 · Cited by 19 · see citing works
Assessment of Vascular Regeneration in the CNS Using the Mouse Retina
Miloudi, K., Dejda, A., Binet, F., Lapalme, E., Cerani, A., & Sapieha, P. S. (2014) · Journal of Visualized Experiments · doi:10.3791/51351 · Cited by 7 · see citing works
Self-citationAssessment of Vascular Regeneration in the CNS Using the Mouse Retina
Miloudi, K., Dejda, A., Binet, F., Lapalme, E., Cerani, A., & Sapieha, P. S. (2014) · Journal of Visualized Experiments · doi:10.3791/51351-v · Cited by 3 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Cellular senescence and senolytics: the path to the clinic
Chaib, S., Tchkonia, T., & Kirkland, J. L. (2022) · Nature Medicine · doi:10.1038/s41591-022-01923-y · Cited by 1,105 · see citing works
The metabolic roots of senescence: mechanisms and opportunities for intervention
Wiley, C. D., & Campisi, J. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00483-8 · Cited by 691 · see citing works
Mechanisms and consequences of endothelial cell senescence
Bloom, S. I., Islam, M. T., Lesniewski, L. A., & Donato, A. J. (2022) · Nature Reviews Cardiology · doi:10.1038/s41569-022-00739-0 · Cited by 512 · see citing works
Apoptotic cell death in disease—Current understanding of the NCCD 2023
Vitale, I., Pietrocola, F., Guilbaud, E., Aaronson, S. A., Abrams, J., Adam, D., Agostini, M., Agostinis, P., Alnemri, E. S., Altucci, L., et al. (2023) · Cell Death and Differentiation · doi:10.1038/s41418-023-01153-w · Cited by 359 · see citing works
Targeting angiogenesis in oncology, ophthalmology and beyond
Cao, Y., Langer, R., & Ferrara, N. (2023) · Nature Reviews Drug Discovery · doi:10.1038/s41573-023-00671-z · Cited by 333 · see citing works
The heterogeneity of cellular senescence: insights at the single-cell level
Cohn, R. L., Gasek, N. S., Kuchel, G. A., & Xu, M. (2023) · Trends in Cell Biology · doi:10.1016/j.tcb.2022.04.011 · Cited by 294 · see citing works
Senescence as a therapeutic target in cancer and age-related diseases
McHugh, D., Durán, I., & Gil, J. (2024) · Nature Reviews Drug Discovery · doi:10.1038/s41573-024-01074-4 · Cited by 199 · see citing works
Cellular Senescence in Cardiovascular Diseases: A Systematic Review
Hu, C., Zhang, X., Teng, T., Ma, Z., & Tang, Q. (2022) · Aging and Disease · doi:10.14336/ad.2021.0927 · Cited by 181 · see citing works
Role of Cellular Senescence in Type II Diabetes
Narasimhan, A., Flores, R. R., Robbins, P. D., & Niedernhofer, L. J. (2021) · Endocrinology · doi:10.1210/endocr/bqab136 · Cited by 133 · see citing works
Role of hypoxia in cellular senescence
Gao, H., Nepovimová, E., Heger, Z., Valko, M., Wu, Q., Kuča, K., & Adam, V. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106841 · Cited by 130 · see citing works
New Dawn for Atherosclerosis: Vascular Endothelial Cell Senescence and Death
Bu, L.-L., Yuan, H., Xie, L., Guo, M.-H., Liao, D., & Zheng, X. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015160 · Cited by 129 · see citing works
Angiogenesis in adipose tissue and obesity
Corvera, S., Solivan-Rivera, J., & Yang, Z. (2022) · Angiogenesis · doi:10.1007/s10456-022-09848-3 · Cited by 125 · see citing works
Senescent Cells: A Therapeutic Target in Cardiovascular Diseases
Suda, M., Paul, K. H., Minamino, T., Miller, J. D., Lerman, A., Ellison, G. M., Tchkonia, T., & Kirkland, J. L. (2023) · Cells · doi:10.3390/cells12091296 · Cited by 116 · see citing works
Crespo‐Garcia, S., Fournier, F., Diaz-Marin, R., Klier, S. M., Ragusa, D., Masaki, L., Cagnone, G., Blot, G., Hafiane, I., Dejda, A., et al. (2024) · Nature Medicine · doi:10.1038/s41591-024-02802-4 · Cited by 108 · see citing works
Self-citationDiabetic retinopathy: Involved cells, biomarkers, and treatments
Ren, J., Zhang, S., Pan, Y., Jin, M., Li, J., Luo, Y., Sun, X., & Li, G. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.953691 · Cited by 100 · see citing works
Activated cGAS/STING signaling elicits endothelial cell senescence in early diabetic retinopathy
Liu, H., Ghosh, S., Vaidya, T. A., Bammidi, S., Huang, C., Shang, P., Nair, A. P., Chowdhury, O., Stepicheva, N. A., Strizhakova, A., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.168945 · Cited by 100 · see citing works
Becker, L. M., Chen, S.-H., Rodor, J., de Rooij, L. P. M. H., Baker, A. H., & Carmeliet, P. (2022) · Cardiovascular Research · doi:10.1093/cvr/cvac018 · Cited by 76 · see citing works
Recent advances in the treatment and delivery system of diabetic retinopathy
Wang, Z., Zhang, N., Lin, P., Xing, Y., & Yang, N. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1347864 · Cited by 68 · see citing works
Sun, D., Chen, S., Li, S., Wang, N., Zhang, S., Xu, L., Zhu, S., Li, H., Gu, Q., Xu, X., et al. (2022) · Redox Biology · doi:10.1016/j.redox.2022.102589 · Cited by 66 · see citing works
Mitochondria-targeted nanozymes eliminate oxidative damage in retinal neovascularization disease
Bai, X., Ge, M., Fan, K., Huang, X., Yan, X., Jiang, W., Jiang, B., & Yang, Z. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.08.026 · Cited by 61 · see citing works
Oxidative Stress-Induced Cellular Senescence in Aging Retina and Age-Related Macular Degeneration
Terao, R., Ahmed, T., Suzumura, A., & Terasaki, H. (2022) · Antioxidants · doi:10.3390/antiox11112189 · Cited by 59 · see citing works
The challenge of identifying senescent cells
Gil, J. (2023) · Nature Cell Biology · doi:10.1038/s41556-023-01267-w · Cited by 58 · see citing works
Terao, R., Lee, T. J., Colasanti, J. J., Pfeifer, C. W., Lin, J. B., Santeford, A. C., Hase, K., Yamaguchi, S., Du, D., Sohn, B. S., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114102 · Cited by 59 · see citing works
Sun, X., & Feinberg, M. W. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.693067 · Cited by 55 · see citing works
Long term high glucose exposure induces premature senescence in retinal endothelial cells
Bertelli, P. M., Pedrini, E., Hughes, D. W., McDonnell, S., Pathak, V., Peixoto, E., Guduric‐Fuchs, J., Stitt, A. W., & Medina, R. J. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.929118 · Cited by 57 · see citing works
Pathophysiology of Retinopathy of Prematurity
Hartnett, M. E. (2023) · Annual Review of Vision Science · doi:10.1146/annurev-vision-093022-021420 · Cited by 54 · see citing works
Fan, Y., Zhang, W., Huang, X., Fan, M., Shi, C., Zhao, L., Pi, G., Zhang, H., & Ni, S. (2024) · Nature Communications · doi:10.1038/s41467-024-47317-1 · Cited by 47 · see citing works
CD44 connects autophagy decline and ageing in the vascular endothelium
Zhang, L., Yang, P., Chen, J., Chen, Z., Liu, Z., Feng, G., Sha, F., Li, Z., Xu, Z., Huang, Y., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41346-y · Cited by 45 · see citing works
He, X., Wen, S., Tang, X., Wen, Z., Zhang, R. H., Li, S., Gao, R. B., Wang, J., Zhu, Y., Fang, D., et al. (2024) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2024.03.011 · Cited by 44 · see citing works
Liu, Y., Liu, X., Chen, X., Yang, Z., Chen, J., Zhu, W., Li, Y., Wen, Y., Deng, C., Gu, C., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2311028121 · Cited by 43 · see citing works
Sreekumar, P. G., Reddy, S. T., Hinton, D. R., & Kannan, R. (2022) · Experimental Eye Research · doi:10.1016/j.exer.2021.108918 · Cited by 41 · see citing works
Senescent cells at the crossroads of aging, disease, and tissue homeostasis
Kuehnemann, C., & Wiley, C. D. (2023) · Aging Cell · doi:10.1111/acel.13988 · Cited by 41 · see citing works
Senescent endothelial cells: a potential target for diabetic retinopathy
Liao, Y.-L., Fang, Y., Sun, J., & Dou, G. (2024) · Angiogenesis · doi:10.1007/s10456-024-09943-7 · Cited by 40 · see citing works
Senolytics in the treatment of diabetic retinopathy
Hassan, J. W., & Bhatwadekar, A. D. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.896907 · Cited by 39 · see citing works
Death-seq identifies regulators of cell death and senolytic therapies
Colville, A., Liu, J., Rodríguez-Mateo, C., Thomas, S. M., Ishak, H. D., Zhou, R., Klein, J. D. D., Morgens, D. W., Goshayeshi, A., Salvi, J. S., et al. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.08.008 · Cited by 36 · see citing works
Potential Clinical Implications of Senotherapies for Cardiovascular Disease
Suda, M., Katsuumi, G., Tchkonia, T., Kirkland, J. L., & Minamino, T. (2023) · Circulation Journal · doi:10.1253/circj.cj-23-0657 · Cited by 37 · see citing works
Iacobini, C., Vitale, M., Haxhi, J., Menini, S., & Pugliese, G. (2024) · Cells · doi:10.3390/cells13090763 · Cited by 38 · see citing works
Wen, Z., He, X., Wang, J., Wang, H., Li, T., Wen, S., Ren, Z., Cai, N., Yang, J., Li, M., et al. (2022) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2022.109213 · Cited by 34 · see citing works
Ryu, W., Park, C.-W., Kim, J., Lee, H., & Chung, H. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.2188 · Cited by 33 · see citing works
Bai, L., & Wang, Y. (2024) · Experimental Cell Research · doi:10.1016/j.yexcr.2024.114170 · Cited by 32 · see citing works
Immune response in retinal degenerative diseases – Time to rethink?
Xu, H., & Chen, M. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102350 · Cited by 32 · see citing works
A nutrigeroscience approach: Dietary macronutrients and cellular senescence
Calubag, M. F., Robbins, P. D., & Lamming, D. W. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.07.025 · Cited by 32 · see citing works
Single‐cell RNA sequencing in exploring the pathogenesis of diabetic retinopathy
Zhang, X. Y., Zhang, F., & Xu, X. (2024) · Clinical and Translational Medicine · doi:10.1002/ctm2.1751 · Cited by 29 · see citing works
Khan, A. H., Chowers, I., & Lotery, A. J. (2023) · Cells · doi:10.3390/cells12131708 · Cited by 31 · see citing works
Retinopathy of prematurity: Metabolic risk factors
Fu, Z., Nilsson, A., Hellström, A., & Smith, L. E. H. (2022) · eLife · doi:10.7554/elife.80550 · Cited by 29 · see citing works
α-Klotho prevents diabetic retinopathy by reversing the senescence of macrophages
Li, Q., Wang, P., Xu, M., Gong, Y., Wang, M., Luan, R., Liu, J., Li, X., Li, X., & Shao, Y. X. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01838-w · Cited by 30 · see citing works
Cellular senescence primes liver fibrosis regression through Notch‐EZH2
Song, P., Duan, J., Ding, J. H., Liu, J., Fang, Z., Xu, H., Li, Z., Du, W., Xu, M., Ling, Y., et al. (2023) · MedComm · doi:10.1002/mco2.346 · Cited by 25 · see citing works
Safety and Efficacy of Senolytic UBX1325 in Diabetic Macular Edema
Klier, S. M., Dananberg, J., Masaki, L., Bhisitkul, R. B., Khanani, A. M., Maturi, R. K., Salehi-Had, H., Mallinckrodt, C. H., Rathmell, J. M., Ghosh, A., et al. (2025) · NEJM Evidence · doi:10.1056/evidoa2400009 · Cited by 25 · see citing works
Self-citationLi, S., Sun, D., Chen, S., Zhang, S., Gu, Q., Shen, Y., Li, X., Xu, X., Wei, F., & Wang, N. (2024) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.65.1.14 · Cited by 27 · see citing works
A new clinical age of aging research
Zhang, Z., Yang, R., Zi, Z., & Liu, B. (2024) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2024.08.004 · Cited by 25 · see citing works
Zhang, Q., Huang, J., Chen, X., Li, L., Chen, L., Zhou, X., Zhao, X., Liu, M., Zhao, W., Yan, J., et al. (2025) · ACS Nano · doi:10.1021/acsnano.4c15759 · Cited by 24 · see citing works
Adipose tissue aging: An update on mechanisms and therapeutic strategies
Cai, Z., & He, B. (2022) · Metabolism · doi:10.1016/j.metabol.2022.155328 · Cited by 26 · see citing works
Innate immunity dysregulation in aging eye and therapeutic interventions
Das, S., Ahmad, Z., Suryawanshi, A. S., & Kumar, A. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101768 · Cited by 24 · see citing works
Fournier, F., Diaz-Marin, R., Pilon, F., Neault, M., Juneau, R., Girouard, G., Wilson, A. M., Larrivée, B., Mallette, F. A., Crespo‐Garcia, S., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2209973120 · Cited by 23 · see citing works
Self-citationDong, X., Song, Y., Liu, Y., Kou, X., Yang, T., Shi, S. X.-Y., He, K., Li, Y., Li, Z., Yao, X., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adi6626 · Cited by 22 · see citing works
Recent developments of neuroprotective agents for degenerative retinal disorders
Wu, J., Ou, K., Li, Y., Liu, L., Li, H., Cox, K. H. M., Liu, J., & Dick, A. D. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.335140 · Cited by 22 · see citing works
Zhang, H., Zhou, H., Shen, X. M., Lin, X., Zhang, Y., Sun, Y., Zhou, Y., Zhang, L., & Zhang, D. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1276707 · Cited by 24 · see citing works
The Role of Senescence-Associated Secretory Phenotype in Bone Loss
Zhu, R., Wan, H., Yang, H. S., Song, M., Chai, Y., & Yu, B. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.841612 · Cited by 21 · see citing works
Revisiting Retinal Degeneration Hallmarks: Insights from Molecular Markers and Therapy Perspectives
da Rosa, J. G. S., Disner, G. R., Pinto, F. J., Lima, C., & Lopes‐Ferreira, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713079 · Cited by 23 · see citing works
Li, C., Zhou, L., Sun, H., & Yang, M. S. (2024) · Clinical Interventions in Aging · doi:10.2147/cia.s463297 · Cited by 20 · see citing works
Obesity drives depot-specific vascular remodeling in male white adipose tissue
Hasan, S. S., John, D., Rudnicki, M., AlZaim, I., Eberhard, D., Moll, I., Taylor, J., Klein, C., von Heesen, M., Conradi, L., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-60910-2 · Cited by 20 · see citing works
Deletion of METTL14, a key methylation regulator, attenuates vascular ageing
Liu, X., Liu, H., Lin, Y., Lou, H., Feng, J., Sun, X., Wang, J., Dong, X., Liu, L., Sun, Z., et al. (2025) · European Heart Journal · doi:10.1093/eurheartj/ehaf476 · Cited by 19 · see citing works
Mechanical stimuli-induced CCL2 restores adult mouse cells to regenerate hair follicles
Wu, W., Zhou, W., Jiang, J., Wang, M., Zhang, J., Yang, J., Tang, Q., Liu, H., Liu, D., Xu, W., et al. (2023) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2023.03.002 · Cited by 19 · see citing works
Huang, Z., Xu, P., Hess, D. C., & Zhang, Q. (2024) · Translational Neurodegeneration · doi:10.1186/s40035-024-00457-2 · Cited by 18 · see citing works
Cellular Senescence: A Bridge Between Diabetes and Microangiopathy
Liu, J., Guo, B., Liu, Q., Zhu, G., Wang, Y., Wang, N., Yang, Y., & Fu, S. (2024) · Biomolecules · doi:10.3390/biom14111361 · Cited by 19 · see citing works
Does senescence play a role in age-related macular degeneration?
Malek, G., Campisi, J., Kitazawa, K., Webster, C. M., Lakkaraju, A., & Skowronska‐Krawczyk, D. (2022) · Experimental Eye Research · doi:10.1016/j.exer.2022.109254 · Cited by 18 · see citing works
Wang, S., Heng, K., Song, X., Zhai, J., Zhang, H., & Geng, Q. (2023) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202300330 · Cited by 18 · see citing works
Nanotechnology for vision restoration
Lanzani, G., Chiaravalli, G., Colombo, E., Manfredi, G., Marco, S. D., Vurro, V., & Benfenati, F. (2024) · Nature Reviews Bioengineering · doi:10.1038/s44222-024-00210-4 · Cited by 18 · see citing works
Endothelial protein C receptor promotes retinal neovascularization through heme catabolism
Song, H., Li, Q. X., Gui, X., Fang, Z., Zhou, W. S., Wang, M., Jiang, Y., Geng, A., Shen, X. P., Liu, Y., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-56810-0 · Cited by 17 · see citing works
Hata, M., Hata, M., Dejda, A., Pilon, F., Diaz-Marin, R., Fournier, F., Joyal, J., Cagnone, G., Ochi, Y., Crespo‐Garcia, S., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2411640121 · Cited by 17 · see citing works
Self-citationThe Role of Endothelial Senescence in the Pathogenesis of Diabetic Retinopathy
Gandhi, M., Haider, S., Chang, H. Z. Y., & Kazlauskas, A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26115211 · Cited by 16 · see citing works
Aging in Ocular Blood Vessels: Molecular Insights and the Role of Oxidative Stress
Cui, X., Buonfiglio, F., Pfeiffer, N., & Gericke, A. (2024) · Biomedicines · doi:10.3390/biomedicines12040817 · Cited by 16 · see citing works
Sun, D., Li, S., Chen, S., Zhang, S., Gu, Q., Shen, Y., Fang, W., & Wang, N. (2023) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-023-06160-8 · Cited by 15 · see citing works
The role of microRNAs in the pathophysiology of the aging eye
Tamaddon, M., Fazel, M., Rezaee, D., Khalilzad, M. A., Majidpoor, J., Ahmadieh, H., Fattahi, M.-D., Namakin, K., Suri, F., & Najafi, S. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102805 · Cited by 14 · see citing works
Zhu, H., Jiang, J., Yang, M., Zhao, M., He, Z., Tang, C., Song, C., Zhao, M., Akbar, A. N., Reddy, V. R., et al. (2024) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2024.06.002 · Cited by 15 · see citing works
Mechanisms of cellular senescence-induced vascular aging: evidence of senotherapeutic strategies
Mahoney, S. A., Bloom, S. I., Seals, D. R., Donato, A. J., Rossman, M. J., & Clayton, Z. S. (2025) · The Journal of Cardiovascular Aging · doi:10.20517/jca.2024.31 · Cited by 15 · see citing works
Nano-PROTACs for precision medicine: engineering strategies for enhanced targeting and potency
Yang, X., Wang, D., Li, C., Zhang, Y., Yang, J., Liu, M., Xing, D., Jiang, W., Xu, S., & Wang, C. (2026) · Journal of Nanobiotechnology · doi:10.1186/s12951-025-03985-9 · Cited by 13 · see citing works
HIF1α-dependent hypoxia response in myeloid cells requires IRE1α
Mawambo, G., Oubaha, M., Ichiyama, Y., Blot, G., Crespo‐Garcia, S., Dejda, A., Binet, F., Diaz-Marin, R., Sawchyn, C., Sergeev, M., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02793-y · Cited by 13 · see citing works
Self-citationFraile‐Μartinez, O., León-Oliva, D. D., Boaru, D. L., Castro-Martinez, P. D., Montero, C. G., Barrena-Blázquez, S., García-García, J., García‐Honduvilla, N., Álvarez‐Mon, M., López-González, L., et al. (2024) · Frontiers in Genetics · doi:10.3389/fgene.2024.1345459 · Cited by 14 · see citing works
Wu, J., Liu, X., Liu, Y., Su, W., & Zhuo, Y. (2025) · Bioengineering · doi:10.3390/bioengineering12060563 · Cited by 13 · see citing works
New insights of potential biomarkers in diabetic retinopathy: integrated multi-omic analyses
Wang, X., Liu, W., Zheng, X., & Yang, M. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1595207 · Cited by 13 · see citing works
Senescent Cells: Dual Implications on the Retinal Vascular System
Habibi-Kavashkohie, M. R., Scorza, T., & Oubaha, M. (2023) · Cells · doi:10.3390/cells12192341 · Cited by 12 · see citing works
Liraglutide improves senescence and ameliorating diabetic sarcopenia via the YAP-TAZ pathway
Xu, Q., Qiu, X., Di, H., Li, Z., Liu, Z., & Liu, K. (2025) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2025.108975 · Cited by 13 · see citing works
Yang, B., Yang, K., Xi, R., Li, S., Chen, J., & Wu, Y. (2025) · Redox Biology · doi:10.1016/j.redox.2025.103716 · Cited by 12 · see citing works
Ramshekar, A., Bretz, C. A., & Hartnett, M. E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137354 · Cited by 11 · see citing works
Gao, X., Hu, Y., Zhang, Y., Huang, Y., Zhang, G., Zhang, X., Zhou, Y., & Zhang, D. (2025) · Science Advances · doi:10.1126/sciadv.adr2833 · Cited by 11 · see citing works
Emerging approaches in keloid scar healing: The synergistic role of nanoparticles and phytochemicals
Mercy, D. J., Girigoswami, K., & Girigoswami, A. (2025) · Chemical Engineering Journal · doi:10.1016/j.cej.2025.168048 · Cited by 11 · see citing works
Cellular senescence in pathologic retinal angiogenesis
Fu, Z., & Smith, L. E. H. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2021.03.010 · Cited by 11 · see citing works
Aging microvasculature: Effects on immune cell trafficking and inflammatory diseases
Reglero-Real, N., Rolas, L., & Nourshargh, S. (2025) · The Journal of Experimental Medicine · doi:10.1084/jem.20242154 · Cited by 11 · see citing works
Shen, W., Nie, Z., Wang, M., Zhang, H., Liu, Y., Zhu, H., Zhou, W., Zhang, L., Zhao, M., Zeng, H., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2501704122 · Cited by 10 · see citing works
Cholesterol Accumulation Promotes Photoreceptor Senescence and Retinal Degeneration
Terao, R., Sohn, B. S., Yamamoto, T., Lee, T. J., Colasanti, J. J., Pfeifer, C. W., Lin, J. B., Santeford, A. C., Yamaguchi, S., Yoshida, M., et al. (2024) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.65.10.29 · Cited by 10 · see citing works
The Ercc1−/Δ mouse model of XFE progeroid syndrome undergoes accelerated retinal degeneration
Narasimhan, A., Min, S.-H., Johnson, L. L., Roehrich, H., Cho, W., Her, T. K., Windschitl, C., O'Kelly, R. D., Angelini, L. A., Yousefzadeh, M. J., et al. (2024) · Aging Cell · doi:10.1111/acel.14419 · Cited by 10 · see citing works
SenMayo transcriptomic senescence panel highlights glial cells in the ageing mouse and human retina
Suresh, S., Karthik, G., Ouyang, J. F., Chrysostomou, V., Tang, S. A., Petretto, E. G., Crowston, J. G., & Bell, K. C. (2024) · npj Aging · doi:10.1038/s41514-024-00187-9 · Cited by 10 · see citing works
Yu, F., Yin, B.-F., Liu, M., Zhang, W., Zhao, Z., Wang, L., Li, X., Li, P., Li, Z., Xu, R.-X., et al. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04342-1 · Cited by 9 · see citing works
Teng, M. F., Wu, T.-J., Pritchard, K. A., Day, B. W., Naylor, S., & Teng, R. (2025) · Antioxidants · doi:10.3390/antiox14070844 · Cited by 9 · see citing works
Unveiling the link: aging and its impact on ocular diseases
Wang, K., Xie, Y., Lin, Y., Zhu, R., Gao, T., Han, Z., Yang, Z., Jiang, X., Chen, H., Wu, Z., et al. (2025) · Experimental Eye Research · doi:10.1016/j.exer.2025.110551 · Cited by 11 · see citing works
Liu, W., Fan, B., Fang, T., Li, H., Zhang, J., Liu, B., & Liu, Z. (2025) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2025.08.010 · Cited by 10 · see citing works
Zhou, Z., Feng, Z., Sun, X., Wang, Y., & Dou, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115516 · Cited by 9 · see citing works
Wang, Y., Ma, H., Yang, Q., Chen, K., Ye, H., Wang, X., Xia, J., Chen, X., Wang, X., Ye, S., et al. (2025) · Experimental Eye Research · doi:10.1016/j.exer.2025.110232 · Cited by 8 · see citing works
Insights into the therapeutic strategies for aging and aging-associated diseases
Dong, R., Wu, Q., Kan, J., Fu, C., Sorrentino, V., Chow, A., Lei, Y., Wu, D., Xu, Z., Du, J., et al. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02662-z · Cited by 9 · see citing works
- 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
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2021-04
- Volume
- 33
- Issue
- 4
- Pages
- 818-832.e7
- ISSN
- 1550-4131 (ISSN-L)
- 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
- Health Sciences › Medicine › Physiology › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review