Non–cell autonomous effect of glia on motor neurons in an embryonic stem cell–based ALS model
Open accessAbstract
Here we report an in vitro model system for studying the molecular and cellular mechanisms that underlie the neurodegenerative disease amyotrophic lateral sclerosis (ALS). Embryonic stem cells (ESCs) derived from mice carrying normal or mutant transgenic alleles of the human SOD1 gene were used to generate motor neurons by in vitro differentiation. These motor neurons could be maintained in long-term coculture either with additional cells that arose during differentiation or with primary glial cells. Motor neurons carrying either the nonpathological human SOD1 transgene or the mutant SOD1(G93A) allele showed neurodegenerative properties when cocultured with SOD1(G93A) glial cells. Thus, our studies demonstrate that glial cells carrying a human SOD1(G93A) mutation have a direct, non-cell autonomous effect on motor neuron survival. More generally, our results show that ESC-based models of disease provide a powerful tool for studying the mechanisms of neural degeneration. These phenotypes displayed in culture could provide cell-based assays for the identification of new ALS drugs.
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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
Establishment in culture of pluripotential cells from mouse embryos
Evans, M. J., & Kaufman, M. H. (1981) · Nature · doi:10.1038/292154a0 · Cited by 8,623 · see citing works
Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J. P., Deng, H.-X., et al. (1993) · Nature · doi:10.1038/362059a0 · Cited by 7,062 · see citing works
Martin, G. R. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.12.7634 · Cited by 5,756 · see citing works
Manipulating the mouse embryo: A laboratory manual
Hogan, B., Costantini, F. D., & Lacy, E. (1986) · Cited by 4,467 · see citing works
Motor Neuron Degeneration in Mice that Express a Human Cu,Zn Superoxide Dismutase Mutation
Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H.-X., et al. (1994) · Science · doi:10.1126/science.8209258 · Cited by 4,143 · see citing works
Manipulating the mouse embryo: A laboratory manual
Johnson, M. (1986) · Trends in Genetics · doi:10.1016/0168-9525(86)90275-1 · Cited by 2,259 · see citing works
Directed differentiation of embryonic stem cells into motor neurons.
Wichterle, H., Lieberam, I., Porter, J. A., & Jessell, T. (2002) · Cell · doi:10.1016/s0092-8674(02)00835-8 · Cited by 1,792 · 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
Wong, P. C., Pardo, C. A., Borchelt, D., Lee, M. K., Copeland, N. G., Jenkins, N. A., Sisodia, S. S., Cleveland, D. W., & Price, D. L. (1995) · Neuron · doi:10.1016/0896-6273(95)90259-7 · Cited by 1,439 · see citing works
ALS: A Disease of Motor Neurons and Their Nonneuronal Neighbors
Boillée, S., Velde, C. V., & Cleveland, D. W. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.018 · Cited by 1,426 · see citing works
UNRAVELING THE MECHANISMS INVOLVED IN MOTOR NEURON DEGENERATION IN ALS
Bruijn, L. I., Miller, T. M., & Cleveland, D. W. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144244 · Cited by 1,371 · see citing works
Bruijn, L. I., Becher, M. W., Lee, M. K., Anderson, K. L., Jenkins, N. A., Copeland, N. G., Sisodia, S. S., Rothstein, J. D., Borchelt, D. R., Price, D. L., et al. (1997) · Neuron · doi:10.1016/s0896-6273(00)80272-x · Cited by 1,341 · see citing works
Banker, G. A., & Goslin, K. (1998) · Cited by 1,290 · see citing works
Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons
Nagai, M., Re, D. B., Nagata, T., Chalazonitis, A., Jessell, T. M., Wichterle, H., & Przedborski, S. (2007) · Nature Neuroscience · doi:10.1038/nn1876 · Cited by 1,220 · see citing works
Wild-Type Nonneuronal Cells Extend Survival of SOD1 Mutant Motor Neurons in ALS Mice
Clement, A. M., Nguyen, M. D., Roberts, E. A., Garcia, M. L., Boillée, S., Rule, M., McMahon, A. P., Doucette, W. T., Siwek, D. F., Ferrante, R. J., et al. (2003) · Science · doi:10.1126/science.1086071 · Cited by 1,101 · see citing works
The bHLH Transcription Factors OLIG2 and OLIG1 Couple Neuronal and Glial Subtype Specification
Zhou, Q., & Anderson, D. J. (2002) · Cell · doi:10.1016/s0092-8674(02)00677-3 · Cited by 1,059 · cited 1× · see citing works
“Glial cells are closely associated with motor neurons and both are derived from a common progenitor in vivo”
BackgroundBeers, D. R., Henkel, J. S., Xiao, Q., Zhao, W., Wang, J., Yen, A. A., Siklos, L., McKercher, S. R., & Appel, S. H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607423103 · Cited by 733 · see citing works
Requirement for the Homeobox Gene Hb9 in the Consolidation of Motor Neuron Identity
Arber, S., Han, B., Mendelsohn, M. M., Smith, M., Jessell, T. M., & Sockanathan, S. (1999) · Neuron · doi:10.1016/s0896-6273(01)80026-x · Cited by 607 · see citing works
Bignami, A., & Dahl, D. R. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901530104 · Cited by 491 · see citing works
Watanabe, M., Dykes‐Hoberg, M., Culotta, V., Price, D. L., Wong, P. C., & Rothstein, J. D. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2001.0443 · Cited by 432 · see citing works
Motoneuron Death Triggered by a Specific Pathway Downstream of Fas
Raoul, C., Estévez, Á. G., Nishimune, H., Cleveland, D. W., deLapeyrière, O., Henderson, C. E., Haase, G., & Pettmann, B. (2002) · Neuron · doi:10.1016/s0896-6273(02)00905-4 · Cited by 432 · see citing works
Role for glia in synaptogenesis
Ullian, E. M., Christopherson, K. S., & Barres, B. A. (2004) · Glia · doi:10.1002/glia.20082 · Cited by 370 · see citing works
Thaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J., & Pfaff, S. L. (1999) · Neuron · doi:10.1016/s0896-6273(01)80027-1 · Cited by 354 · see citing works
Pasinelli, P., Houseweart, M. K., Brown, R. H., & Cleveland, D. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240305897 · Cited by 344 · see citing works
Signaling between glia and neurons: focus on synaptic plasticity
Allen, N. J., & Barres, B. A. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.08.006 · Cited by 321 · see citing works
Nagai, M., Aoki, M., Miyoshi, I., Kato, M., Pasinelli, P., Kasai, N., Brown, R. H., & Itoyama, Y. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09246.2001 · Cited by 318 · see citing works
Wang, J., Slunt, H. H., Gonzales, V., Fromholt, D., Coonfield, M. L., Copeland, N. G., Jenkins, N. A., & Borchelt, D. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg312 · Cited by 306 · see citing works
(1998) · The MIT Press eBooks · doi:10.7551/mitpress/4913.001.0001 · Cited by 272 · see citing works
Therapeutic potential of embryonic stem cells.
Lerou, P., & Daley, G. (2005) · Blood reviews · doi:10.1016/j.blre.2005.01.005 · Cited by 228 · see citing works
Brown, R. H. (1997) · Archives of Neurology · doi:10.1001/archneur.1997.00550220050013 · Cited by 164 · see citing works
Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture
Ullian, E. M., Harris, B. T., Wu, A. W., Chan, J. R., & Barres, B. A. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2003.10.011 · Cited by 158 · see citing works
Ince, P. G., Tomkins, J., Slade, J. Y., Thatcher, N. M., & Shaw, P. J. (1998) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199810000-00002 · Cited by 142 · see citing works
Human embryonic stem cells as a cellular model for human disorders
Ben‐Nun, I. F., & Benvenisty, N. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.03.034 · Cited by 41 · see citing works
Genetic Disorders of Motor Neurons
Cole, N., & Siddique, T. (1999) · Seminars in Neurology · doi:10.1055/s-2008-1040855 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Astrocytes: Biology and pathology
Sofroniew, M. V., & Vinters, H. V. (2010) · Acta Neuropathologica · doi:10.1007/s00401-009-0619-8 · Cited by 5,196 · see citing works
The Blood-Brain Barrier in Health and Chronic Neurodegenerative Disorders
Zlokovic, B. V. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.003 · Cited by 3,280 · see citing works
Neurovascular pathways to neurodegeneration in Alzheimer’s disease and other disorders
Zlokovic, B. V. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3114 · Cited by 2,969 · see citing works
Reactive Astrocytes: Production, Function, and Therapeutic Potential
Liddelow, S. A., & Barres, B. A. (2017) · Immunity · doi:10.1016/j.immuni.2017.06.006 · Cited by 2,336 · see citing works
Disease-Specific Induced Pluripotent Stem Cells.
Park, I.-H., Arora, N., Huo, H., Maherali, N., Ahfeldt, T., Shimamura, A., Lensch, M. W., Cowan, C., Hochedlinger, K., & Daley, G. Q. (2008) · Cell · doi:10.1016/j.cell.2008.07.041 · Cited by 2,196 · see citing works
Converging Mechanisms in ALS and FTD: Disrupted RNA and Protein Homeostasis
Ling, S.-C., Polymenidou, M., & Cleveland, D. W. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.033 · Cited by 1,811 · see citing works
Induced pluripotent stem cell technology: a decade of progress.
Shi, Y., Inoue, H., Wu, J. C., & Yamanaka, S. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.245 · Cited by 1,525 · see citing works
The Mystery and Magic of Glia: A Perspective on Their Roles in Health and Disease
Barres, B. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.013 · Cited by 1,352 · see citing works
Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons
Nagai, M., Re, D. B., Nagata, T., Chalazonitis, A., Jessell, T. M., Wichterle, H., & Przedborski, S. (2007) · Nature Neuroscience · doi:10.1038/nn1876 · Cited by 1,220 · see citing works
Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis
Yamanaka, K., Chun, S. J., Boillee, S., Fujimori-Tonou, N., Yamashita, H., Gutmann, D. H., Takahashi, R., Misawa, H., & Cleveland, D. W. (2008) · Nature Neuroscience · doi:10.1038/nn2047 · Cited by 1,140 · see citing works
Middeldorp, J., & Hol, E. M. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.01.005 · Cited by 1,080 · see citing works
Astrocyte reactivity and reactive astrogliosis: costs and benefits
Pekny, M., & Pekna, M. (2014) · Physiological Reviews · doi:10.1152/physrev.00041.2013 · Cited by 934 · 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
Minocycline selectively inhibits M1 polarization of microglia
Kobayashi, K., Imagama, S., Ohgomori, T., Hirano, K., Uchimura, K., Sakamoto, K., Hirakawa, A., Takeuchi, H., Suzumura, A., Ishiguro, N., et al. (2013) · Cell Death & Disease · doi:10.1038/cddis.2013.54 · Cited by 742 · see citing works
Chiu, I. M., Morimoto, E. T. A., Goodarzi, H., Liao, J. T., O’Keeffe, S., Phatnani, H. P., Muratet, M., Carroll, M. C., Levy, S., Tavazoie, S., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.018 · Cited by 651 · see citing works
Self-citationYamanaka, S. (2009) · Cell · doi:10.1016/j.cell.2009.03.034 · Cited by 659 · 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
Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease
Philips, T., & Robberecht, W. (2011) · The Lancet Neurology · doi:10.1016/s1474-4422(11)70015-1 · Cited by 646 · see citing works
Astrocyte–neuron metabolic relationships: for better and for worse
Allaman, I., Bélanger, M., & Magistretti, P. J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2010.12.001 · Cited by 639 · see citing works
Microglia and Central Nervous System–Associated Macrophages—From Origin to Disease Modulation
Prinz, M., Masuda, T., Wheeler, M. A., & Quintana, F. J. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-093019-110159 · Cited by 584 · see citing works
Pluripotent stem cells in disease modelling and drug discovery
Avior, Y., Sagi, I., & Benvenisty, N. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2015.27 · Cited by 592 · see citing works
Neurotoxic reactive astrocytes induce cell death via saturated lipids
Guttenplan, K. A., Weigel, M. K., Prakash, P., Wijewardhane, P. R., Hasel, P., Rufen-Blanchette, U., Münch, A. E., Blum, J. A., Fine, J., Neal, M. C., et al. (2021) · Nature · doi:10.1038/s41586-021-03960-y · Cited by 578 · see citing works
Lithium delays progression of amyotrophic lateral sclerosis
Fornai, F., Longone, P., Cafaro, L., Kastsiuchenka, O., Ferrucci, M., Manca, M. L., Lazzeri, G., Spalloni, A., Bellio, N., Lenzi, P., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708022105 · Cited by 550 · see citing works
Vargas, M. R., Johnson, D. A., Sirkis, D. W., Messing, A., & Johnson, J. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4099-08.2008 · Cited by 479 · see citing works
Lepore, A. C., Rauck, B., Dejea, C., Pardo, A. C., Rao, M. S., Rothstein, J. D., & Maragakis, N. J. (2008) · Nature Neuroscience · doi:10.1038/nn.2210 · Cited by 441 · see citing works
Astrocytes in Neurodegenerative Disease: Table 1.
Phatnani, H., & Maniatis, T. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020628 · Cited by 420 · see citing works
Self-citationReactive astrocytes secrete lcn2 to promote neuron death
Bi, F., Huang, C., Tong, J., Qiu, G., Huang, B., Wu, Q., Li, F., Xu, Z., Bowser, R., Xia, X.-G., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218497110 · Cited by 371 · see citing works
Serio, A., Bilican, B., Barmada, S. J., Ando, D. M., Zhao, C., Siller, R., Burr, K., Haghi, G., Story, D., Nishimura, A. L., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300398110 · Cited by 345 · see citing works
Self-citationTam, O. H., Rozhkov, N. V., Shaw, R., Kim, D., Hubbard, I., Fennessey, S., Propp, N., Phatnani, H., Kwan, J., Sareen, D., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.09.066 · Cited by 327 · see citing works
Yamanaka, K., Boillee, S., Roberts, E. A., Garcia, M. L., McAlonis-Downes, M., Mikse, O. R., Cleveland, D. W., & Goldstein, L. S. B. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802556105 · Cited by 309 · see citing works
Modeling ALS with motor neurons derived from human induced pluripotent stem cells
Sances, S., Bruijn, L. I., Chandran, S., Eggan, K., Ho, R., Klim, J. R., Livesey, M. R., Lowry, E., Macklis, J. D., Rushton, D., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4273 · Cited by 289 · see citing works
Self-citationKnockout of reactive astrocyte activating factors slows disease progression in an ALS mouse model
Guttenplan, K. A., Weigel, M. K., Adler, D. I., Couthouis, J., Liddelow, S. A., Gitler, A. D., & Barres, B. A. (2020) · Nature Communications · doi:10.1038/s41467-020-17514-9 · Cited by 278 · see citing works
Membrane recruitment of endogenous LRRK2 precedes its potent regulation of autophagy
Schapansky, J., Nardozzi, J. D., Felizia, F., & LaVoie, M. J. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu138 · Cited by 226 · see citing works
Andrés, C. M. C., Pérez de la Lastra, J. M., Juan, C. A., Plou, F. J., & Pérez-Lebeña, E. (2022) · Stresses · doi:10.3390/stresses2030019 · Cited by 218 · see citing works
Papadeas, S. T., Kraig, S. E., O'Banion, C., Lepore, A. C., & Maragakis, N. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103141108 · Cited by 213 · see citing works
Human Stem Cell-Derived Spinal Cord Astrocytes with Defined Mature or Reactive Phenotypes
Roybon, L., Lamas, N. J., Garcia-Diaz, A., Yang, E. J., Sattler, R., Jackson-Lewis, V., Kim, Y. A., Kachel, C. A., Rothstein, J. D., Przedborski, S., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.021 · Cited by 208 · see citing works
Human glia can both induce and rescue aspects of disease phenotype in Huntington disease
Benraiss, A., Wang, S., Herrlinger, S., Li, X., Chandler-Militello, D., Mauceri, J., Burm, H. B., Toner, M., Osipovitch, M., Jim Xu, Q., et al. (2016) · Nature Communications · doi:10.1038/ncomms11758 · Cited by 199 · see citing works
Diverse functional roles of lipocalin-2 in the central nervous system
Jha, M. K., Lee, S., Park, D. H., Kook, H., Park, K.-G., Lee, I.-K., & Suk, K. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.006 · Cited by 195 · see citing works
Hester, M. E., Murtha, M. J., Song, S., Rao, M., Miranda, C. J., Meyer, K., Tian, J., Boulting, G., Schaffer, D. V., Zhu, M. X., et al. (2011) · Molecular Therapy · doi:10.1038/mt.2011.135 · Cited by 183 · see citing works
De Feo, D., Merlini, A., Laterza, C., & Martino, G. (2012) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328352ec45 · Cited by 181 · see citing works
In vivo genome editing improves motor function and extends survival in a mouse model of ALS
Gaj, T., Ojala, D. S., Ekman, F. K., Byrne, L. C., Limsirichai, P., & Schaffer, D. V. (2017) · Science Advances · doi:10.1126/sciadv.aar3952 · Cited by 185 · see citing works
Amyotrophic Lateral Sclerosis: From Current Developments in the Laboratory to Clinical Implications
Cozzolino, M., Ferri, A., & Teresa Carrì, M. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2007.1760 · Cited by 156 · see citing works
Madill, M., McDonagh, K., Ma, J., Vajda, A., McLoughlin, P., O’Brien, T., Hardiman, O., & Shen, S. (2017) · Molecular Brain · doi:10.1186/s13041-017-0300-4 · Cited by 134 · see citing works
Tripathi, P., Rodriguez-Muela, N., Klim, J. R., de Boer, A. S., Agrawal, S., Sandoe, J., Lopes, C. S., Ogliari, K. S., Williams, L. A., Shear, M., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.06.008 · Cited by 123 · see citing works
Self-citationActivation of interferon signaling pathways in spinal cord astrocytes from an ALS mouse model
Wang, R., Yang, B., & Zhang, D. (2011) · Glia · doi:10.1002/glia.21167 · Cited by 115 · see citing works
Autophagy and amyotrophic lateral sclerosis: The multiple roles of lithium
Fornai, F., Longone, P., Ferrucci, M., Lenzi, P., Isidoro, C., Ruggieri, S., & Paparelli, A. (2008) · Autophagy · doi:10.4161/auto.5923 · Cited by 111 · see citing works
Primary cells and stem cells in drug discovery: emerging tools for high-throughput screening
Eglen, R., & Reisine, T. (2011) · ASSAY and Drug Development Technologies · doi:10.1089/adt.2010.0305 · Cited by 100 · see citing works
Glia in neurodegeneration: Drivers of disease or along for the ride?
Gleichman, A. J., & Carmichael, S. T. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104957 · Cited by 90 · see citing works
Harlan, B. A., Pehar, M., Sharma, D. R., Beeson, G., Beeson, C. C., & Vargas, M. R. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.698779 · Cited by 94 · see citing works
Qiang, L., Fujita, R., & Abeliovich, A. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.002 · Cited by 59 · see citing works
Thams, S., Lowry, E. R., Larraufie, M.-H., Spiller, K. J., Li, H., Williams, D. J., Hoang, P., Jiang, E., Williams, L. A., Sandoe, J., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2018.10.010 · Cited by 51 · see citing works
Self-citationCould sirtuin activities modify ALS onset and progression?
Tang, B. L. (2017) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-016-0452-2 · Cited by 24 · see citing works
- Authors
- Di Giorgio, F. P., Carrasco, M. A., Siao, M. C., Maniatis, T., & Eggan, K.
- Affiliations
- Harvard University (US)
- Corresponding author
- Maniatis, Tom
- Eggan, Kevin
- Venue
- Nature Neuroscience
- Published
- 2007-04-15
- Volume
- 10
- Issue
- 5
- Pages
- 608-614
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3139463
- OpenAlex
- W1993064034
- Cited by
- 799
- References
- 35
- Citations by year
- 2026: 13 · 2025: 14 · 2024: 29 · 2023: 26 · 2022: 30 · 2021: 26 · 2020: 36 · 2019: 25 · 2018: 32 · 2017: 51 · 2016: 34 · 2015: 51 · 2014: 51 · 2013: 68 · 2012: 69
- FWCI
- 43.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Harvard University
- National Institute of Neurological Disorders and Stroke (R01NS043915)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD046732)
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- amyotrophic lateral sclerosis, glial cells, motor neurons, non-cell autonomous neurodegeneration, SOD1 mutations, SOD1 G93A, embryonic stem cells, in vitro disease model, motor neuron survival, drug screening
- MeSH terms
- Amyotrophic Lateral Sclerosis, Analysis of Variance, Animals, Cell Differentiation, Cell Survival, Cells, Cultured, Disease Models, Animal, Embryo, Mammalian, Flow Cytometry, Humans, Mice, Transgenic, Motor Neurons, Nerve Tissue Proteins, Neuroglia, Stem Cells, Superoxide Dismutase, Time Factors, Coculture Techniques, Reverse Transcriptase Polymerase Chain Reaction, Green Fluorescent Proteins, 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 ›
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