Emergence of Microglia Bearing Senescence Markers During Paralysis Progression in a Rat Model of Inherited ALS
Open accessAbstract
Age is a recognized risk factor for amyotrophic lateral sclerosis (ALS), a paralytic disease characterized by progressive loss of motor neurons and neuroinflammation. A hallmark of aging is the accumulation of senescent cells. Yet, the pathogenic role of cellular senescence in ALS remains poorly understood. In rats bearing the ALS-linked SOD1G93A mutation, microgliosis contribute to motor neuron death, and its pharmacologic downregulation results in increased survival. Here, we have explored whether gliosis and motor neuron loss were associated with cellular senescence in the spinal cord during paralysis progression. In the lumbar spinal cord of symptomatic SOD1G93A rats, numerous cells displayed nuclear p16INK4a as well as loss of nuclear Lamin B1 expression, two recognized senescence-associated markers. The number of p16INK4a-positive nuclei increased by 4-fold while Lamin B1-negative nuclei increased by 1,2-fold, respect to non-transgenic or asymptomatic transgenic rats. p16INK4a-positive nuclei and Lamin B1-negative nuclei were typically localized in a subset of hypertrophic Iba1-positive microglia, occasionally exhibiting nuclear giant multinucleated cell aggregates and abnormal nuclear morphology. Next, we analyzed senescence markers in cell cultures of microglia obtained from the spinal cord of symptomatic SOD1G93A rats. Although microglia actively proliferated in cultures, a subset of them developed senescence markers after few days in vitro and subsequent passages. Senescent SOD1G93A microglia in culture conditions were characterized by large and flat morphology, senescence-associated beta-Galactosidase (SA-β-Gal) activity as well as positive labeling for p16INK4a, p53, matrix metalloproteinase-1 (MMP-1) and nitrotyrosine, suggesting a senescent-associated secretory phenotype (SASP). Remarkably, in the degenerating lumbar spinal cord other cell types, including ChAT-positive motor neurons and GFAP-expressing astrocytes, also displayed nuclear p16INK4a staining. These results suggest that cellular senescence is closely associated with inflammation and motor neuron loss occurring after paralysis onset in SOD1G93A rats. The emergence of senescent cells could mediate key pathogenic mechanisms in ALS.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
In a mouse model of ALS, gliosis and motor neuron loss were associated with increased senescence indicators.
“A mouse model of ALS also found gliosis and motor neuron loss was associated with increased senescence indicators [94].”
From Untangling senescent and damage‐associated microglia in the aging and diseased brain (2023) · cites this paper as [94]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Polazzi, E., Mengoni, I., Caprini, M., Peña‐Altamira, E., Kurtys, E., & Monti, B. (2012) · Neurosignals · doi:10.1159/000337115 · Cited by 9,023 · 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
Nitric Oxide and Peroxynitrite in Health and Disease
Pacher, P., Beckman, J. S., & Liaudet, L. (2007) · Physiological Reviews · doi:10.1152/physrev.00029.2006 · Cited by 6,390 · see citing works
Self-citationClearance 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 · cited 1× · see citing works
“Nuclear expression of p16INK4A is considered a robust molecular marker of cellular aging, as its expression increases in a variety of aged tissues (Baker et al., 2011).”
BackgroundCellular senescence: from physiology to pathology
Muñoz-Espín, D., & Serrano, M. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3823 · Cited by 2,818 · see citing works
Kiernan, M. C., Vucic, S., Cheah, B. C., Turner, M. R., Eisen, A., Hardiman, O., Burrell, J. R., & Zoing, M. C. (2011) · The Lancet · doi:10.1016/s0140-6736(10)61156-7 · Cited by 2,603 · 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
Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion
Rodier, F., Coppé, J.-P., Patil, C. K., Hoeijmakers, W. A. M., Muñoz, D. P., Raza, S. R., Freund, A., Campeau, E., Davalos, A. R., & Campisi, J. (2009) · Nature Cell Biology · doi:10.1038/ncb1909 · Cited by 2,232 · see citing works
Hardiman, O. M., Al‐Chalabi, A., Chiò, A., Corr, E. M., Logroscino, G., Robberecht, W., Shaw, P. J., Simmons, Z., & van den Berg, L. H. (2017) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2017.71 · Cited by 2,191 · see citing works
Cellular senescence and the senescent secretory phenotype: therapeutic opportunities
Tchkonia, T., Zhu, Y., van Deursen, J., Campisi, J., & Kirkland, J. L. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64098 · Cited by 1,774 · see citing works
Onset and Progression in Inherited ALS Determined by Motor Neurons and Microglia
Boillée, S., Yamanaka, K., Lobsiger, C. S., Copeland, N. G., Jenkins, N. A., Kassiotis, G., Kollias, G., & Cleveland, D. W. (2006) · Science · doi:10.1126/science.1123511 · Cited by 1,623 · see citing works
Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase
Ischiropoulos, H., Zhu, L., Chen, J., Tsai, M., Martin, J. C., Smith, C. D. L., & Beckman, J. S. (1992) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(92)90431-u · Cited by 1,495 · see citing works
Self-citationInflammatory networks during cellular senescence: causes and consequences.
Freund, A., Orjalo, A. V., Desprez, P.-Y., & Campisi, J. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.03.003 · Cited by 1,354 · see citing works
Clearance of senescent glial cells prevents tau-dependent pathology and cognitive decline
Bussian, T. J., Aziz, A., Meyer, C. F., Swenson, B. L., van Deursen, J. M., & Baker, D. J. (2018) · Nature · doi:10.1038/s41586-018-0543-y · Cited by 1,289 · see citing works
Lamin B1 loss is a senescence-associated biomarker
Freund, A., Laberge, R.-M., Demaria, M., & Campisi, J. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-10-0884 · Cited by 1,046 · see citing works
Dechat, T., Pfleghaar, K., Sengupta, K., Shimi, T., Shumaker, D. K., Solimando, L., & Goldman, R. D. (2008) · Genes & Development · doi:10.1101/gad.1652708 · Cited by 1,001 · see citing works
Kurz, D. J., Decary, S., Hong, Y., & Erusalimsky, J. D. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.20.3613 · Cited by 899 · see citing works
Howland, D., Liu, J., She, Y., Goad, B., Maragakis, N. J., Kim, B. B., Erickson, J., Kulik, J., DeVito, L., Psaltis, G. C., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.032539299 · Cited by 841 · see citing works
Senescence and aging: the critical roles of p53
Rufini, A., Tucci, P., Celardo, I., & Melino, G. (2013) · Oncogene · doi:10.1038/onc.2012.640 · Cited by 798 · see citing works
Astrocytes from familial and sporadic ALS patients are toxic to motor neurons
Haidet-Phillips, A. M., Hester, M. E., Miranda, C. J., Meyer, K., Braun, L., Frakes, A., Song, S., Likhite, S., Murtha, M. J., Foust, K. D., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1957 · Cited by 782 · see citing works
Microglia Induce Motor Neuron Death via the Classical NF-κB Pathway in Amyotrophic Lateral Sclerosis
Frakes, A. E., Ferraiuolo, L., Haidet-Phillips, A. M., Schmelzer, L., Braun, L., Miranda, C. J., Ladner, K. J., Bevan, A. K., Foust, K. D., Godbout, J. P., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.013 · Cited by 638 · see citing works
Jurk, D., Wang, C., Miwa, S., Maddick, M., Korolchuk, V., Tsolou, A., Gonos, E. S., Thrasivoulou, C., Jill Saffrey, M., Cameron, K., et al. (2012) · Aging Cell · doi:10.1111/j.1474-9726.2012.00870.x · Cited by 598 · see citing works
Tau protein aggregation is associated with cellular senescence in the brain
Musi, N., Valentine, J. M., Sickora, K. R., Baeuerle, E., Thompson, C. S., Shen, Q., & Orr, M. E. (2018) · Aging Cell · doi:10.1111/acel.12840 · Cited by 595 · see citing works
Astrocyte Senescence as a Component of Alzheimer’s Disease
Bhat, R., Crowe, E. P., Bitto, A., Moh, M., Katsetos, C. D., Garcia, F. U., Johnson, F. B., Trojanowski, J. Q., Sell, C., & Torres, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045069 · Cited by 586 · see citing works
Chinta, S. J., Woods, G., Demaria, M., Rane, A., Zou, Y., McQuade, A., Rajagopalan, S., Limbad, C., Madden, D. T., Campisi, J., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.092 · Cited by 530 · see citing works
Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS
Liao, B., Zhao, W., Beers, D. R., Henkel-Tigges, J., & Appel, S. H. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.06.011 · Cited by 438 · see citing works
Analysis of amyotrophic lateral sclerosis as a multistep process: a population-based modelling study
Al‐Chalabi, A., Calvo, A., Chiò, A., Colville, S., Ellis, C., Hardiman, O. M., Heverin, M., Howard, R., Huisman, M. H. B., Keren, N., et al. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70219-4 · Cited by 421 · see citing works
Hall, B. M., Balan, V., Gleiberman, A. S., Strom, E., Krasnov, P., Virtuoso, L. P., Rydkina, E., Vujcic, S., Balan, K., Gitlin, I. I., et al. (2017) · Aging · doi:10.18632/aging.101268 · Cited by 407 · see citing works
Salminen, A., Ojala, J., Kaarniranta, K., Haapasalo, A., Hiltunen, M., & Soininen, H. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07738.x · Cited by 333 · see citing works
Cassina, P., Cassina, A., Pehar, M., Castellanos, R., Gandelman, M., de León, A., Robinson, K. M., Mason, R. P., Beckman, J. S., Barbeito, L., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5308-07.2008 · Cited by 310 · see citing works
Self-citationBrettschneider, J., Toledo, J. B., Van Deerlin, V. M., Elman, L., McCluskey, L., Lee, V. M.-Y., & Trojanowski, J. Q. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039216 · Cited by 268 · see citing works
ALS-specific cognitive and behavior changes associated with advancing disease stage in ALS
Crockford, C., Newton, J. L., Lonergan, K., Chiwera, T., Booth, T., Chandran, S., Colville, S., Heverin, M., Mays, I., Pal, S., et al. (2018) · Neurology · doi:10.1212/wnl.0000000000006317 · Cited by 264 · see citing works
Aging Microglia—Phenotypes, Functions and Implications for Age-Related Neurodegenerative Diseases
Spittau, B. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00194 · Cited by 258 · see citing works
Glial cells in amyotrophic lateral sclerosis
Philips, T., & Rothstein, J. D. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.05.015 · Cited by 255 · see citing works
Immunosenescence of microglia and macrophages: impact on the ageing central nervous system
Rawji, K. S., Mishra, M. K., Michaels, N. J., Rivest, S., Stys, P. K., & Yong, V. W. (2016) · Brain · doi:10.1093/brain/awv395 · Cited by 252 · see citing works
Expression of the cyclin-dependent kinase inhibitor p16 in Alzheimerʼs disease
Lars Rödel, T. A., Gärtner, U., & Holzer, M. (1996) · NeuroReport · doi:10.1097/00001756-199611250-00050 · Cited by 250 · see citing works
Microglia in the aging brain: relevance to neurodegeneration
Luo, X.-G., Ding, J.-Q., & Chen, S.-D. (2010) · Molecular Neurodegeneration · doi:10.1186/1750-1326-5-12 · Cited by 236 · see citing works
Pehar, M., Cassina, P., Vargas, M. R., Castellanos, R., Viera, L., Beckman, J. S., Estévez, Á. G., & Barbeito, L. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02357.x · Cited by 228 · see citing works
Self-citationLamin Dysfunction Mediates Neurodegeneration in Tauopathies
Frost, B., Bardai, F. H., & Feany, M. B. (2016) · Current Biology · doi:10.1016/j.cub.2015.11.039 · Cited by 226 · see citing works
Cell cycle arrest is not senescence
Blagosklonny, M. V. (2011) · Aging · doi:10.18632/aging.100281 · Cited by 217 · see citing works
Loss of TDP-43 causes age-dependent progressive motor neuron degeneration
Iguchi, Y., Katsuno, M., Niwa, J.-I., Takagi, S., Ishigaki, S., Ikenaka, K., Kawai, K., Watanabe, H., Yamanaka, K., Takahashi, R., et al. (2013) · Brain · doi:10.1093/brain/awt029 · Cited by 195 · see citing works
Díaz‐Amarilla, P., Olivera‐Bravo, S., Trías, E., Cragnolini, A. B., Palma, L. M., Cassina, P., Beckman, J. S., & Barbeito, L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110689108 · Cited by 186 · see citing works
Self-citationThe microglial-motoneuron dialogue in ALS.
Appel, S. H., Zhao, W., Beers, D. R., & Henkel-Tigges, J. (2011) · Europe PMC (PubMed Central) · Cited by 179 · see citing works
Pathogenesis of amyotrophic lateral sclerosis
Morgan, S. L., & Orrell, R. W. (2016) · British Medical Bulletin · doi:10.1093/bmb/ldw026 · Cited by 179 · see citing works
p53 isoforms regulate astrocyte-mediated neuroprotection and neurodegeneration
Turnquist, C., Horikawa, I., Foran, E., Major, E. O., Vojtěšek, B., Lane, D. P., Lü, X., Harris, B. T., & Harris, C. C. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.37 · Cited by 177 · see citing works
Activated Microglia Initiate Motor Neuron Injury by a Nitric Oxide and Glutamate-Mediated Mechanism
Zhao, W., Xie, W., Le, W., Beers, D. R., He, Y., Henkel-Tigges, J., Simpson, E. P., Yen, A. A., Xiao, Q., & Appel, S. H. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.9.964 · Cited by 169 · see citing works
Chinta, S. J., Lieu, C. A., DeMaria, M., Laberge, R. ‐., Campisi, J., & Andersen, J. K. (2013) · Journal of Internal Medicine · doi:10.1111/joim.12029 · Cited by 165 · see citing works
Telomere shortening in neurological disorders: an abundance of unanswered questions
Eitan, E., Hutchison, E. R., & Mattson, M. P. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.02.010 · Cited by 158 · see citing works
Trías, E., Ibarburu, S., Barreto‐Núñez, R., Babdor, J., Maciel, T. T., Guillo, M., Gros, L., Dubreuil, P. C., Díaz‐Amarilla, P., Cassina, P., et al. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0620-9 · Cited by 155 · see citing works
Self-citationTsai, M.-J., Hsu, C.-Y., & Sheu, C. (2017) · New England Journal of Medicine · doi:10.1056/nejmc1710379 · Cited by 152 · see citing works
Mast cells and neutrophils mediate peripheral motor pathway degeneration in ALS
Trías, E., King, P. H., Si, Y., Kwon, Y., Varela, V., Ibarburu, S., Kovacs, M., Moura, I. C., Beckman, J. S., Hermine, O., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.123249 · Cited by 139 · see citing works
Self-citationp53 Is Abnormally Elevated and Active in the CNS of Patients with Amyotrophic Lateral Sclerosis
Martin, L. J. (2000) · Neurobiology of Disease · doi:10.1006/nbdi.2000.0314 · Cited by 135 · see citing works
Prieur, A., Besnard, E., Babled, A., & Lemaitre, J.-M. (2011) · Nature Communications · doi:10.1038/ncomms1473 · Cited by 117 · see citing works
Key Aging-Associated Alterations in Primary Microglia Response to Beta-Amyloid Stimulation
Caldeira, C., Cunha, C., Vaz, A. R., Falcão, A. S., Barateiro, A., Seixas, E., Fernandes, A., & Brites, D. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00277 · Cited by 117 · see citing works
Revisiting oxidative damage in ALS: microglia, Nox, and mutant SOD1
Boillée, S., & Cleveland, D. W. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34613 · Cited by 95 · see citing works
Neuroinflammation in motor neuron disease
Endo, F., Komine, O., & Yamanaka, K. (2016) · Clinical and Experimental Neuroimmunology · doi:10.1111/cen3.12309 · Cited by 93 · see citing works
Age-Dependent TDP-43-Mediated Motor Neuron Degeneration Requires GSK3, hat-trick, and xmas-2
Sreedharan, J., Neukomm, L. J., Brown, R. H., & Freeman, M. R. (2015) · Current Biology · doi:10.1016/j.cub.2015.06.045 · Cited by 89 · see citing works
Fendrick, S. E., Xue, Q., & Streit, W. J. (2007) · Journal of Neuroinflammation · doi:10.1186/1742-2094-4-9 · Cited by 88 · see citing works
Neuroinflammation in motor neuron disease.
Komine, O., & Yamanaka, K. (2015) · Europe PMC (PubMed Central) · doi:10.18999/nagjms.77.4.537 · Cited by 87 · see citing works
Evidence for mast cells contributing to neuromuscular pathology in an inherited model of ALS
Trías, E., Ibarburu, S., Barreto‐Núñez, R., Varela, V., Moura, I. C., Dubreuil, P. C., Hermine, O., Beckman, J. S., & Barbeito, L. (2017) · JCI Insight · doi:10.1172/jci.insight.95934 · Cited by 80 · see citing works
Self-citationDas, M. M., & Svendsen, C. N. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.09.020 · Cited by 76 · see citing works
Lewis, K. E. A., Rasmussen, A. L., Bennett, W. R., King, A. E., West, A. K., Chung, R. S., & Chuah, M. I. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-55 · Cited by 75 · see citing works
In vitro evidence for senescent multinucleated melanocytes as a source for tumor-initiating cells
Leikam, C., Hufnagel, A., Otto, C., Murphy, D. J., Mühling, B., Kneitz, S., Nanda, I., Schmid, M., Wagner, T. U., Haferkamp, S., et al. (2015) · Cell Death and Disease · doi:10.1038/cddis.2015.71 · Cited by 74 · see citing works
Alzheimer's disease: An acquired neurodegenerative laminopathy
Frost, B. (2016) · Nucleus · doi:10.1080/19491034.2016.1183859 · Cited by 74 · see citing works
Lamoke, F., Shaw, S., Yuan, J., Ananth, S., Duncan, M. B., Martin, P. M., & Bartoli, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0139664 · Cited by 71 · see citing works
Markers of cellular senescence.
Carnero, A. (2013) · Methods in Molecular Biology · doi:10.1007/978-1-62703-239-1_4 · Cited by 68 · see citing works
Trías, E., Díaz‐Amarilla, P., Olivera‐Bravo, S., Isasi, E., Drechsel, D. A., Lopez, N. I., Bradford, C. S., Ireton, K. E., Beckman, J. S., & Barbeito, L. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00274 · Cited by 56 · see citing works
Self-citationThe p53 Transcriptional Network Influences Microglia Behavior and Neuroinflammation
Aloi, M. S., Su, W., & Garden, G. A. (2015) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v35.i5.40 · Cited by 34 · see citing works
Microglia: Senescence Impairs Clearance of Myelin Debris
Thériault, P., & Rivest, S. (2016) · Current Biology · doi:10.1016/j.cub.2016.06.066 · Cited by 34 · see citing works
Phenotypic heterogeneity of astrocytes in motor neuron disease
Trías, E., Barbeito, L., & Yamanaka, K. (2018) · Clinical and Experimental Neuroimmunology · doi:10.1111/cen3.12476 · Cited by 31 · see citing works
Self-citationJiménez, M., Díaz‐Amarilla, P., Isasi, E., Casanova, G., Barbeito, L., & Olivera‐Bravo, S. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2681-1 · Cited by 30 · see citing works
Self-citationSoon, C. P. W., Crouch, P. J., Turner, B. J., McLean, C., Laughton, K. M., Atkin, J. D., Masters, C. L., White, A. R., & Li, Q.-X. (2010) · Neuromuscular Disorders · doi:10.1016/j.nmd.2009.11.015 · Cited by 26 · see citing works
Thonhoff, J. R., Gao, J., Dunn, T. J., Ojeda, L. D., & Wu, P. (2012) · Europe PMC (PubMed Central) · Cited by 9 · see citing works
Ibarburu, S., Trías, E., Lago, N., et al. (2017) · NeuroImmunoModulation · doi:10.1159/000480639 · Cited by 9 · see citing works
Self-citationControlling the senescence-associated secretory phenotype
Strzyz, P. J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.157 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ogrodnik, M., Evans, S. A., Fielder, E., Victorelli, S., Kruger, P., Salmonowicz, H., Weigand, B. M., Patel, A. D., Pirtskhalava, T., Inman, C. L., et al. (2021) · Aging Cell · doi:10.1111/acel.13296 · Cited by 405 · see citing works
Astrocyte Senescence and Alzheimer’s Disease: A Review
Han, X., Zhang, T., Liu, H., Mi, Y., & Gou, X. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00148 · Cited by 177 · see citing works
Similarities and interplay between senescent cells and macrophages
Behmoaras, J., & Gil, J. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202010162 · Cited by 158 · see citing works
Cellular senescence in aging and age-related diseases: Implications for neurodegenerative diseases
(2020) · International Review of Neurobiology · doi:10.1016/bs.irn.2020.03.019 · Cited by 114 · see citing works
Matsudaira, T., Nakano, S., Konishi, Y., Kawamoto, S., Uemura, K., Kondo, T., Sakurai, K., Ozawa, T., Hikida, T., Komine, O., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05027-2 · Cited by 98 · see citing works
Zhang, X., Pearsall, V. M., Carver, C. M., Atkinson, E. J., Clarkson, B. D. S., Grund, E. M., Baez-Faria, M., Pavelko, K. D., Kachergus, J. M., White, T. A., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33226-8 · Cited by 102 · see citing works
Senescent Microglia: The Key to the Ageing Brain?
Greenwood, E. K., & Brown, D. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094402 · Cited by 84 · see citing works
HIV TAT-mediated microglial senescence: Role of SIRT3-dependent mitochondrial oxidative stress
Thangaraj, A., Chivero, E. T., Tripathi, A., Singh, S., Niu, F., Guo, M.-L., Pillai, P., Periyasamy, P., & Buch, S. (2021) · Redox Biology · doi:10.1016/j.redox.2020.101843 · Cited by 76 · see citing works
Untangling senescent and damage‐associated microglia in the aging and diseased brain
Ng, P. Y., McNeely, T. L., & Baker, D. J. (2023) · The FEBS Journal · doi:10.1111/febs.16315 · Cited by 68 · see citing works
- Authors
- Trias, E., Beilby, P. R., Kovacs, M., Ibarburu, S., Varela, V., Barreto-Núñez, R., Bradford, S. C., Beckman, J. S., & Barbeito, L.
- Affiliations
- Oregon State University (US)
- Institut Pasteur de Montevideo (UY)
- Corresponding author
- Beckman, Joseph S.
- Barbeito, Luis
- Venue
- Frontiers in Aging Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2019-02-28
- Volume
- 11
- Pages
- 42-42
- ISSN
- 1663-4365 (ISSN-L)
- PMC
- PMC6403180
- OpenAlex
- W2918779335
- Cited by
- 85
- References
- 75
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 16 · 2023: 12 · 2022: 8 · 2021: 13 · 2020: 11 · 2019: 6
- FWCI
- 6.43
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Aging Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Agencia Nacional de Investigación e Innovación
- Amyotrophic Lateral Sclerosis Association
- U.S. Department of Defense
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Keywords
- amyotrophic lateral sclerosis, cellular senescence, microglia, p16INK4a, lamin B1, senescence-associated secretory phenotype, microglial activation, motor neuron degeneration, neuroinflammation, spinal cord, astrocytes, nitrotyrosine
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