Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer’s disease
Open accessAbstract
Cell cycle events play a major role in the loss of neurons in advanced Alzheimer's disease (AD). It is currently unknown, however, whether the same is true for the neuronal losses in early disease stages. To explore this issue we analyzed brain autopsy material from individuals clinically categorized with mild cognitive impairment (MCI), many if not most of whom will progress to AD. Immunocytochemistry for three cell cycle-related proteins, proliferating cell nuclear antigen, cyclin D, and cyclin B, was performed on sections from hippocampus, basal nucleus of Meynert, and entorhinal cortex. The results obtained from MCI cases were compared with material from individuals diagnosed with AD and those without cognitive impairment. In both hippocampus and basal nucleus, there was a significant percentage of cell cycle immunopositive neurons in the MCI cases. These percentages were similar to those found in the AD cases but significantly higher than non-cognitively impaired controls. In entorhinal cortex, the density of cell cycle-positive neurons was greater in MCI than in AD. However, we observed large variations in the percentages of immunopositive neurons from individual to individual. These findings lend support to the hypothesis that both the mechanism of cell loss (a cell cycle-induced death) and the rate of cell loss (a slow atrophy over several months) are identical at all stages of the AD disease process. The implication of the findings for human clinical trials is discussed.
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?
There is growing evidence for an association between DNA damage and increased expression of cell-cycle markers in AD.
“There is also growing evidence for the association between DNA damage and increased expression of cell-cycle markers in AD [34], [38].”
From Repair of Oxidative DNA Damage, Cell-Cycle Regulation and Neuronal Death May Influence the Clinical Manifestation of Alzheimer’s Disease (2014) · cites this paper as [34]
In brains of people who died with MCI, the percentage of hippocampal neurons positive for cell-cycle proteins (PCNA, cyclin D and cyclin B) was very close to that found in individuals who died in advanced stages of AD (demented).
“Yang et al. [34] showed that in brains of people who died with MCI, the percentage of hippocampal neurons positive for cell-cycle proteins (PCNA, cyclin D and cyclin B) was very close to that found in individuals who died in advanced stages of AD (demented).”
From Repair of Oxidative DNA Damage, Cell-Cycle Regulation and Neuronal Death May Influence the Clinical Manifestation of Alzheimer’s Disease (2014) · cites this paper as [34]
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
Neuropathological stageing of Alzheimer-related changes.
Braak, H., & Braak, E. (1991) · Acta Neuropathologica · doi:10.1007/bf00308809 · Cited by 16,123 · see citing works
Alzheimer's Disease and Senile Dementia: Loss of Neurons in the Basal Forebrain
Whitehouse, P., Price, D., Struble, R., Clark, A., Coyle, J., & DeLong, M. R. (1982) · Science · doi:10.1126/science.7058341 · Cited by 3,627 · see citing works
Alzheimer's disease: cell-specific pathology isolates the hippocampal formation.
Hyman, B. T., Van Hoesen, G. W., Damasio, A. R., & Barnes, C. L. (1984) · Science · doi:10.1126/science.6474172 · Cited by 2,268 · cited 1× · see citing works
“This is evident both in the extent of neuronal loss and in the appearance of neurofibrillary tangles (Hyman et al., 1984, 1986; Arnold et al., 1991; Braak and Braak, 1991; Price et al., 1991; Kordower et al., 2001; Mitchell et al., 2002 ).”
BackgroundMild Cognitive Impairment Represents Early-Stage Alzheimer Disease
Morris, J. C., Storandt, M., Miller, J. P., McKeel, D. W., Price, J. L., Rubin, E. H., & Berg, L. (2001) · Archives of Neurology · doi:10.1001/archneur.58.3.397 · Cited by 1,833 · see citing works
Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease
Gómez-Isla, T., Price, J. L., McKeel Jr., D. W., Morris, J. C., Growdon, J. H., & Hyman, B. T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-14-04491.1996 · Cited by 1,796 · cited 2× · see citing works
“For example, several studies have shown an early loss of neurons in this region (Gomez-Isla et al., 1996; Kordower et al., 2001), a finding that is consistent with the early appearance of neurofibrillary tangles (Braak and Braak, 1991).”
BackgroundResultEffects of an Rb mutation in the mouse
Jacks, T., Fazeli, A., Schmitt, E. M., Bronson, R. T., Goodell, M. A., & Weinberg, R. A. (1992) · Nature · doi:10.1038/359295a0 · Cited by 1,755 · see citing works
Cyclin D1 is a nuclear protein required for cell cycle progression in G1
Baldin, V, Lukas, J., Marcote, M. J., Pagano, M., & Draetta, G. (1993) · Genes & Development · doi:10.1101/gad.7.5.812 · Cited by 1,614 · see citing works
Arnold, S. E., Hyman, B. T., Flory, J., Damasio, A. R., & Van Hoesen, G. W. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.103 · Cited by 1,380 · see citing works
Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease
West, M. J., Coleman, P. D., Flood, D. G., & Troncoso, J. C. (1994) · The Lancet · doi:10.1016/s0140-6736(94)92338-8 · Cited by 1,267 · cited 1× · see citing works
“It is generally considered that the cell loss in the CA1 region is greater than in the other CA fields (West et al., 1994).”
BackgroundMice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis
Lee, E. Y.-H. P., Chang, C.-Y., Hu, N., Wang, Y.-C. J., Lai, C., Herrup, K., Lee, W., & Bradley, A. (1992) · Nature · doi:10.1038/359288a0 · Cited by 1,264 · see citing works
Self-citationNatural history of mild cognitive impairment in older persons
Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Beckett, L. A., Aggarwal, N. T., Barnes, L. L., Fox, J. H., & Bach, J. (2002) · Neurology · doi:10.1212/wnl.59.2.198 · Cited by 1,037 · see citing works
Price, J. L., Davis, P. B., Morris, J. C., & White, D. L. (1991) · Neurobiology of Aging · doi:10.1016/0197-4580(91)90006-6 · Cited by 818 · see citing works
Perforant pathway changes and the memory impairment of Alzheimer's disease
Hyman, B. T., Van Hoesen, G. W., Kromer, L. J., & Damasio, A. R. (1986) · Annals of Neurology · doi:10.1002/ana.410200406 · Cited by 672 · see citing works
DNA Replication Precedes Neuronal Cell Death in Alzheimer's Disease
Yang, Y., Geldmacher, D., & Herrup, K. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02661.2001 · Cited by 607 · see citing works
Self-citationEctopic Cell Cycle Proteins Predict the Sites of Neuronal Cell Death in Alzheimer’s Disease Brain
Busser, J., Geldmacher, D. S., & Herrup, K. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-08-02801.1998 · Cited by 543 · see citing works
Self-citationAbnormal Alzheimer‐like phosphorylation of tau‐protein by cyclin‐dependent kinases cdk2 and cdk5
Baumann, K., Mandelkow, E., Biernat, J., Piwnica-Worms, H. M., & Mandelkow, E. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)80849-p · Cited by 479 · see citing works
The neuropathology of aminergic nuclei in Alzheimer's disease
Zweig, R. M., Ross, C. A., Hedreen, J. C., Steele, C., Cardillo, J. E., Whitehouse, P. J., Folstein, M. F., & Price, D. L. (1988) · Annals of Neurology · doi:10.1002/ana.410240210 · Cited by 446 · see citing works
Vincent, I. J., Jicha, G. A., Rosado, M., & Dickson, D. W. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03588.1997 · Cited by 444 · see citing works
Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease.
McShea, A., Harris, P. L. R., Webster, K. R., Wahl, A. F., & Smith, M. A. (1997) · Europe PMC (PubMed Central) · Cited by 422 · see citing works
Mitotic mechanisms in Alzheimer's disease?
Vincent, I., Rosado, M., & Davies, P. (1996) · The Journal of cell biology · doi:10.1083/jcb.132.3.413 · Cited by 386 · see citing works
Mild cognitive impairment: transition between aging and Alzheimer's disease.
Petersen, R. C. (2000) · PubMed · Cited by 383 · see citing works
Cell cycle markers in the hippocampus in Alzheimer's disease
Nagy, Z., Esiri, M. M., Cato, A.-M., & Smith, A. D. (1997) · Acta Neuropathologica · doi:10.1007/s004010050665 · Cited by 318 · see citing works
Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation.Preprint
Lee, E. Y., Hu, N., Yuan, S. F., Cox, L. A., Bradley, A., Lee, W., & Herrup, K. (1994) · Genes & Development · doi:10.1101/gad.8.17.2008 · Cited by 285 · see citing works
Self-citationPark, D. S., Morris, E. J., Greene, L. A., & Geller, H. M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-04-01256.1997 · Cited by 270 · see citing works
Cyclin-dependent Kinases Participate in Death of Neurons Evoked by DNA-damaging Agents
Park, D. S., Morris, E. J., Padmanabhan, J., Shelanski, M. L., Geller, H. M., & Greene, L. A. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.143.2.457 · Cited by 263 · 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
Mitchell, T. W., Mufson, E. J., Schneider, J. A., Cochran, E. J., Nissanov, J., Han, L., Bienias, J. L., Lee, V. M. ‐., Trojanowski, J. Q., Bennett, D. A., et al. (2002) · Annals of Neurology · doi:10.1002/ana.10086 · Cited by 249 · see citing works
Self-citationEntorhinal Cortex β-Amyloid Load in Individuals with Mild Cognitive Impairment
Mufson, E. J., Chen, E.-Y., Cochran, E. J., Beckett, L. A., Bennett, D. A., & Kordower, J. H. (1999) · Experimental Neurology · doi:10.1006/exnr.1999.7086 · Cited by 237 · see citing works
Self-citationThe induction of multiple cell cycle events precedes target-related neuronal death
Herrup, K., & Busser, J. C. (1995) · Development · doi:10.1242/dev.121.8.2385 · Cited by 220 · see citing works
Self-citationMufson, E. J., Ma, S. Y., Cochran, E. J., Bennett, D. A., Beckett, L., Jaffar, S., Saragovi, H. U., & Kordower, J. H. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001106)427:1 · Cited by 216 · see citing works
Self-citationFeddersen, R. M., Ehlenfeldt, R., Yunis, W. S., Clark, H. B., & Orr, H. T. (1992) · Neuron · doi:10.1016/0896-6273(92)90247-b · Cited by 206 · see citing works
Mufson, E. J., Ma, S. Y., Dills, J. L., Cochran, E. J., Leurgans, S. E., Wuu, J., Bennett, D. A., Jaffar, S., Gilmor, M. L., Levey, A. I., et al. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10122 · Cited by 197 · see citing works
Self-citationIs Mild Cognitive Impairment Prodromal for Vascular Dementia Like Alzheimer’s Disease?
Meyer, J. S., Xu, G., Thornby, J. A., Chowdhury, M. H., & Quach, M. (2002) · Stroke · doi:10.1161/01.str.0000024432.34557.10 · Cited by 195 · see citing works
Lew, J., & Wang, J. H.-C. (1995) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(00)88948-3 · Cited by 177 · see citing works
Stage-dependent and sector-specific neuronal loss in hippocampus during Alzheimer's disease
Rössler, M., Zarski, R., Bohl, J., & Ohm, T. (2002) · Acta Neuropathologica · doi:10.1007/s00401-001-0475-7 · Cited by 164 · see citing works
Al‐Ubaidi, M. R., Hollyfield, J. G., Overbeek, P. A., & Baehr, W. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.4.1194 · Cited by 148 · see citing works
AGING, MILD COGNITIVE IMPAIRMENT, AND ALZHEIMER'S DISEASE
Petersen, R. C. (2000) · Neurologic Clinics · doi:10.1016/s0733-8619(05)70226-7 · Cited by 141 · see citing works
Neuronal expression of cycline dependent kinase inhibitors of the INK4 family in Alzheimer's disease
Arendt, T., Holzer, M., & Gärtner, U. (1998) · Journal of Neural Transmission · doi:10.1007/s007020050104 · Cited by 137 · see citing works
Alzheimer's disease and aging: Effects on perforant pathway perikarya and synapses
Lippa, C. F., Hamos, J. E., Pulaski-Salo, D., DeGennaro, L. J., & Drachman, D. A. (1992) · Neurobiology of Aging · doi:10.1016/0197-4580(92)90115-e · Cited by 122 · see citing works
Prosperi, E. (1997) · Springer eBooks · doi:10.1007/978-1-4615-5371-7_15 · Cited by 117 · see citing works
Popken, G. J., & Farel, P. B. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970915)386:1 · Cited by 117 · see citing works
Hoozemans, J. J. M., Brückner, M. K., Rozemüller, A. J. M., Veerhuis, R., Eikelenboom, P., & Arendt, T. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.8.678 · Cited by 116 · see citing works
Beta-amyloid activated microglia induce cell cycling and cell death in cultured cortical neurons
Wu, Q. (2000) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00219-0 · Cited by 93 · see citing works
Efficacy and Safety of OK-432 Sclerotherapy for Giant Cystic Hygroma in a Newborn
Samuel, M., McCarthy, L., & Boddy, S. A. (2000) · Fetal Diagnosis and Therapy · doi:10.1159/000020983 · Cited by 92 · see citing works
Fukutani, Y., Kobayashi, K., Nakamura, I., Watanabe, K., Isaki, K., & Cairns, N. J. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)12083-g · Cited by 88 · see citing works
In Vivo Viability of Postmitotic Purkinje Neurons Requires pRb Family Member Function
Feddersen, R. M., Clark, H. B., Yunis, W. S., & Orr, H. T. (1995) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1995.1014 · Cited by 70 · see citing works
Yu, P.-L., Fujimura, M., Okumiya, K., Kinoshita, M., Hasegawa, H., & Fujimiya, M. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990906)411:4 · Cited by 67 · see citing works
Role for peroxisome proliferator-activated receptor-gamma in Alzheimer's disease.
van Geel (2001) · Open Repository and Bibliography (University of Luxembourg) · doi:10.1002/1531-8249(20010201)49:2 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Querfurth, H. W., & LaFerla, F. M. (2010) · New England Journal of Medicine · doi:10.1056/nejmra0909142 · Cited by 4,569 · see citing works
The case for rejecting the amyloid cascade hypothesis
Herrup, K. (2015) · Nature Neuroscience · doi:10.1038/nn.4017 · Cited by 768 · see citing works
Self-citationYankner, B. A., Lu, T., & Loerch, P. (2008) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev.pathmechdis.2.010506.092044 · Cited by 677 · see citing works
Progesterone receptors: form and function in brain
Brinton, R. D., Thompson, R. F., Foy, M. R., Baudry, M., Wang, J., Finch, C. E., Morgan, T. E., Pike, C. J., Mack, W. J., Stanczyk, F. Z., et al. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.02.001 · Cited by 675 · see citing works
Taupin, P. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.08.002 · Cited by 645 · see citing works
Chong, Z. Z., Li, F., & Maiese, K. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.02.004 · Cited by 536 · see citing works
Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms
Andorfer, C., Acker, C. M., Kress, Y., Hof, P. R., Duff, K., & Davies, P. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4637-04.2005 · Cited by 511 · see citing works
“DOI:10.1523/JNEUROSCI.4637-04.2005 Copyright © 2005 Society for Neuroscience 0270-6474/05/255446-09$15.00/0 regions in which cell death is extensive (Lew et al., 1995; Busser et al., 1998; Yang et al., 2001, 2003; Herrup and Arendt, 2002).”
BackgroundInfluentialButterfield, D. A., Poon, H. F., St. Clair, D., Keller, J. N., Pierce, W. M., Klein, J. B., & Markesbery, W. R. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.11.002 · Cited by 377 · see citing works
Inflammaging as a prodrome to Alzheimer's disease
Giunta, B., Fernandez, F., Nikolic, W. V., Obregon, D., Rrapo, E., Town, T., & Tan, J. (2008) · Journal of Neuroinflammation · doi:10.1186/1742-2094-5-51 · Cited by 327 · see citing works
The pRb/E2F cell-cycle pathway mediates cell death in Parkinson's disease
Höglinger, G. U., Breunig, J. J., Depboylu, C., Rouaux, C., Michel, P. P., Alvarez-Fischer, D., Boutillier, A.-L., DeGregori, J., Oertel, W. H., Rakic, P., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611671104 · Cited by 276 · see citing works
Genomic integrity and the ageing brain
Chow, H.-M., & Herrup, K. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn4020 · Cited by 174 · see citing works
Self-citationAdult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells
Shivraj Sohur, U., Emsley, J. G., Mitchell, B. D., & Macklis, J. D. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1887 · Cited by 170 · see citing works
Spilsbury, A., Miwa, S., Attems, J., & Saretzki, G. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2925-14.2015 · Cited by 140 · see citing works
The DNA Damage Response in Neurons: Die by Apoptosis or Survive in a Senescence-Like State?
Fielder, E., von Zglinicki, T., & Jurk, D. (2017) · Journal of Alzheimer's Disease · doi:10.3233/jad-161221 · Cited by 126 · see citing works
Tanaka, H., Homma, H., Fujita, K., Kondo, K., Yamada, S., Jin, X., Waragai, M., Ohtomo, G., Iwata, A., Tagawa, K., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14353-6 · Cited by 119 · see citing works
Self-citationAre there roles for brain cell senescence in aging and neurodegenerative disorders?
Tan, F. C. C., Hutchison, E. R., Eitan, E., & Mattson, M. P. (2014) · Biogerontology · doi:10.1007/s10522-014-9532-1 · Cited by 116 · see citing works
Nuclear localization of Cdk5 is a key determinant in the postmitotic state of neurons
Zhang, J., Cicero, S. A., Wang, L., Romito-DiGiacomo, R. R., Yang, Y., & Herrup, K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711355105 · Cited by 113 · see citing works
Self-citationAerobic glycolysis in the primate brain: Reconsidering the implications for growth and maintenance
Bauernfeind, A. L., Barks, S. K., Duka, T., Grossman, L. I., Hof, P. R., & Sherwood, C. C. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0662-z · Cited by 105 · see citing works
The neuronal cell cycle as a mechanism of pathogenesis in Alzheimer's disease
Currais, A., Hortobágyi, T., & Soriano, S. (2009) · Aging · doi:10.18632/aging.100045 · Cited by 101 · see citing works
Silva, A. R. T., Santos, A. C. F., Farfel, J. M., Grinberg, L. T., Ferretti, R. E. L., Campos, A. H. J. F. M., Cunha, I. W., Begnami, M. D., Rocha, R. M., Carraro, D. M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099897 · Cited by 99 · see citing works
Cdk5 suppresses the neuronal cell cycle by disrupting the E2F1-DP1 complex
Zhang, J., Li, H., Yabut, O., Fitzpatrick, H., D'Arcangelo, G., & Herrup, K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5628-09.2010 · Cited by 96 · see citing works
Self-citationEvaluation of<sup>18</sup>F-UCB-H as a Novel PET Tracer for Synaptic Vesicle Protein 2A in the Brain
Warnock, G. I., Aerts, J., Bahri, M. A., Bretin, F., Lemaire, C., Giacomelli, F., Mievis, F., Mestdagh, N., Buchanan, T., Valade, A., et al. (2014) · Journal of Nuclear Medicine · doi:10.2967/jnumed.113.136143 · Cited by 85 · see citing works
Marlatt, M. W., Bauer, J., Aronica, E., van Haastert, E. S., Hoozemans, J. J. M., Joels, M., & Lucassen, P. J. (2014) · Neural Plasticity · doi:10.1155/2014/693851 · Cited by 83 · see citing works
Norambuena, A., Wallrabe, H., McMahon, L., Silva, A., Swanson, E., Khan, S. S., Baerthlein, D., Kodis, E., Oddo, S., Mandell, J. W., et al. (2017) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.08.015 · Cited by 79 · see citing works
Munawara, U., Catanzaro, M., Xu, W., Tan, C., Hirokawa, K., Bosco, N., Dumoulin, D., Khalil, A., Larbi, A., Lévesque, S., et al. (2021) · Immunity & Ageing · doi:10.1186/s12979-021-00236-x · Cited by 74 · see citing works
Duque, A., Arellano, J. I., & Rakic, P. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01314-8 · Cited by 63 · see citing works
Curcumin attenuates glutamate-induced HT22 cell death by suppressing MAP kinase signaling
Suh, H.-W., Kang, S., & Kwon, K.-S. (2007) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-006-9365-6 · Cited by 66 · see citing works
Katsel, P., Tan, W., Fam, P., Purohit, D. P., & Haroutunian, V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068361 · Cited by 52 · see citing works
Swanson, D. J., & Goldowitz, D. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2010.11.018 · Cited by 40 · see citing works
Cdk5 and the non-catalytic arrest of the neuronal cell cycle
Zhang, J., & Herrup, K. (2008) · Cell Cycle · doi:10.4161/cc.7.22.7045 · Cited by 44 · see citing works
Self-citationSilva, A. R. T., Grinberg, L. T., Farfel, J. M., Diniz, B. S., Lima, L. A., Silva, P. J. S., Ferretti, R. E. L., Rocha, R. M., Filho, W. J., Carraro, D. M., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048751 · Cited by 40 · see citing works
Sanphui, P., Pramanik, S. K., Chatterjee, N., Moorthi, P., Banerji, B., & Biswas, S. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078842 · Cited by 38 · see citing works
Cdk5 Levels Oscillate during the Neuronal Cell Cycle
Zhang, J., Li, H., Zhou, T., Zhou, J., & Herrup, K. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.343152 · Cited by 34 · see citing works
Self-citationIbnidris, A., Robinson, J. N., Stubbs, M., Piumatti, G., Govia, I., & Albanese, E. (2022) · Systematic Reviews · doi:10.1186/s13643-022-02018-y · Cited by 30 · see citing works
Lopes, J. P., Blurton-Jones, M., Yamasaki, T. R., Agostinho, P., & LaFerla, F. M. (2009) · Journal of Alzheimer's Disease · doi:10.3233/jad-2009-0993 · Cited by 32 · see citing works
A nervous predisposition to unrepaired DNA double strand breaks
Reynolds, J. J., & Stewart, G. S. (2013) · DNA Repair · doi:10.1016/j.dnarep.2013.04.011 · Cited by 26 · see citing works
- Authors
- Yang, Y., Mufson, E. J., & Herrup, K.
- Affiliations
- University Hospitals of Cleveland (US)
- Rush University Medical Center (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-04-01
- Volume
- 23
- Issue
- 7
- Pages
- 2557-2563
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6742098
- OpenAlex
- W1485747833
- Cited by
- 483
- References
- 48
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 11 · 2023: 15 · 2022: 20 · 2021: 28 · 2020: 17 · 2019: 5 · 2018: 20 · 2017: 13 · 2016: 15 · 2015: 24 · 2014: 24 · 2013: 23 · 2012: 22
- FWCI
- 17.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Rare & Special e-Zone (The Hong Kong University of Science and Technology) (submittedVersion)
- Funders
- Blanchette Hooker Rockefeller Fund
- U.S. Public Health Service (A16668, A 09446)
- National Institute on Aging (AG-08012, AG 10161, AG-14449, P50AG008012, P01AG014449, P30AG010161)
- National Institute of Neurological Disorders and Stroke (R01NS020591, NS20591)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, neuronal cell death, cell cycle, mild cognitive impairment, proliferating cell nuclear antigen, cyclin D, cyclin B, hippocampus, basal ganglia, entorhinal cortex, brain atrophy, disease progression
- MeSH terms
- Aged, Alzheimer Disease, Cell Count, Cell Cycle, Cognition Disorders, Female, Hippocampus, Humans, Immunohistochemistry, Male, Neurons, Cyclins, Cell Death, Disease Progression, Entorhinal Cortex, Proliferating Cell Nuclear Antigen, Cyclin B, Basal Nucleus of Meynert, Cyclin D
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