Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors
Abstract
A population of embryonic rat cortical cells cultured in the presence of FGF2 and having neuronal morphology expressed higher levels of reactive oxygen species (ROS) than did progenitor cells, astrocytes, and several cell lines of neuronal and non-neuronal origin. ROS were assessed using 5-(and-6)-chlormethyl-2',7'-dichlorodihydrofluorescein diacetate, acetyl ester (CM-H2DCF-DA), and high levels persisted in the presence of antioxidants or lowered levels of ambient oxygen. Greater than 95% of high ROS-producing cells, isolated by fluorescence-activated cell sorting, expressed the neuronal marker beta III tubulin. These cells did not incorporate BrdU or express nestin, unlike low ROS-producing cells, 99% of which exhibited both of these characteristics. Upon growth factor removal, low ROS-expressing cells differentiated into neurons and astrocytes and these neurons expressed high levels of ROS, indicating that ROS accumulation accompanies the differentiation of progenitors into neurons. ROS levels were decreased by added superoxide dismutase and catalase, suggesting that both superoxide and hydrogen peroxide contribute to the ROS signal. High ROS-expressing cells also contained higher levels of several mitochondrial respiratory chain components. Although ROS have been associated with conditions that lead to cell death, our results and recent studies on the role of ROS as regulators of signal pathways are consistent with the possibility that ROS play a role in the development of the neuronal phenotype. Moreover, the differential production of ROS provides a useful method to isolate from mixed populations cells that are highly enriched for either progenitor cells or neurons.
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?
Cellular ROS levels increase upon the differentiation of both neural and epithelial stem cells.
“Cellular ROS levels also increase upon the differentiation of both neural and epithelial stem cells 44–46.”
From Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes (2010) · cites this paper as [45]
Cites
Free Radicals in the Physiological Control of Cell Function
Dröge, W. (2002) · Physiological Reviews · doi:10.1152/physrev.00018.2001 · Cited by 9,855 · see citing works
Dauer, W., & Przedborski, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00568-3 · Cited by 5,469 · see citing works
Neurotrophins: Roles in Neuronal Development and Function
Huang, E. J., & Reichardt, L. F. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.677 · Cited by 4,394 · see citing works
Subventricular zone astrocytes are neural stem cells in the adult mammalian brain
Doetsch, F., Caillé, I., Lim, D. A., García-Verdugo, J. M., & Alvarez-Buylla, A. (1999) · Cell · doi:10.1016/s0092-8674(00)80783-7 · Cited by 3,898 · see citing works
Oxidative Stress, Glutamate, and Neurodegenerative Disorders
Coyle, J. T., & Puttfarcken, P. (1993) · Science · doi:10.1126/science.7901908 · Cited by 3,762 · see citing works
Paxinos, G. (1985) · Cited by 3,715 · see citing works
CNS stem cells express a new class of intermediate filament protein
Lendahl, U., Zimmerman, L. B., & McKay, R. D. G. (1990) · Cell · doi:10.1016/0092-8674(90)90662-x · Cited by 3,164 · see citing works
Alley, M. C., Scudiero, D. A., Monks, A. P., Hursey, M. L., Czerwiński, M., Fine, D. L., Abbott, B. J., Mayo, J. G., Shoemaker, R. H., & Boyd, M. R. (1988) · PubMed · Cited by 3,082 · see citing works
Handbook of fluorescent probes and research chemicals
Haugland, R. P. (1996) · Medical Entomology and Zoology · Cited by 2,793 · see citing works
LeBel, C. P., Ischiropoulos, H., & Bondy, S. C. (1992) · Chemical Research in Toxicology · doi:10.1021/tx00026a012 · Cited by 2,694 · see citing works
Scudiero, D. A., Shoemaker, R. H., Paull, K. D., Monks, A. P., Tierney, S., Nofziger, T. H., Currens, M. J., Seniff, D. A., & Boyd, M. R. (1988) · PubMed · Cited by 2,342 · see citing works
Brewer, G. J., Torricelli, J. R., Evege, E. K., & Price, P. J. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490350513 · Cited by 2,094 · see citing works
Direct isolation of human central nervous system stem cells
Uchida, N., Buck, D. W., He, D., Reitsma, M. J., Masek, M., Phan, T. V., Tsukamoto, A. S., Gage, F. H., & Weissman, I. L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.26.14720 · Cited by 1,829 · see citing works
Astrocytes give rise to new neurons in the adult mammalian hippocampus
Seri, B., Garcı́a-Verdugo, J. M., McEwen, B. S., & Alvarez-Buylla, A. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07153.2001 · Cited by 1,495 · see citing works
ETIOLOGY AND PATHOGENESIS OF PARKINSON'S DISEASE
Olanow, C. W., & Tatton, W. G. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.123 · Cited by 1,394 · see citing works
Oxidant signals and oxidative stress
Finkel, T. (2003) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(03)00002-4 · Cited by 1,393 · see citing works
Banker, G. A., & Goslin, K. (1998) · Cited by 1,290 · see citing works
Mitochondria and neuronal survival
Nicholls, D. G., & Budd, S. L. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.1.315 · Cited by 1,243 · see citing works
Johe, K. K., Hazel, T. G., Müller, T. H., Dugich‐Djordjevic, M. M., & McKay, R. D. G. (1996) · Genes & Development · doi:10.1101/gad.10.24.3129 · Cited by 1,154 · see citing works
Royall, J. A., & Ischiropoulos, H. (1993) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1993.1222 · Cited by 1,123 · see citing works
Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate
Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T.-C., Hinks, J. A., Tonks, N. K., & Barford, D. (2003) · Nature · doi:10.1038/nature01680 · Cited by 951 · see citing works
Rothe, G., & Valet, G. (1990) · Journal of Leukocyte Biology · doi:10.1002/jlb.47.5.440 · Cited by 870 · see citing works
Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine
Bindokas, V. P., Jordán, J., Lee, C., & Miller, R. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-04-01324.1996 · Cited by 859 · see citing works
Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay
Cathcart, R., Schwiers, E., & Ames, B. N. (1983) · Analytical Biochemistry · doi:10.1016/0003-2697(83)90270-1 · Cited by 857 · see citing works
Reynolds, I., & Hastings, T. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03318.1995 · Cited by 777 · see citing works
Dugan, L. L., Sensi, S., Canzoniero, L. M. T., Handran, S. D., Rothman, S., Lin, T., Goldberg, M. P., & Choi, D. W. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06377.1995 · Cited by 762 · see citing works
Characterization of CNS Precursor Subtypes and Radial Glia
Hartfuss, E., Galli, R., Heins, N., & Götz, M. (2001) · Developmental Biology · doi:10.1006/dbio.2000.9962 · Cited by 755 · see citing works
Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis
Kasischke, K. A., Vishwasrao, H. D., Fisher, P. J., Zipfel, W. R., & Webb, W. W. (2004) · Science · doi:10.1126/science.1096485 · Cited by 742 · see citing works
Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain
Laywell, E. D., RAKIC, P. T., Kukekov, V. G., Holland, E. C., & Steindler, D. A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.250471697 · Cited by 722 · see citing works
Studer, L., CSETE, M. E., Lee, S., Kabbani, N., Walikonis, J., Wold, B. J., & McKay, R. D. G. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-19-07377.2000 · Cited by 709 · see citing works
Purification of a pluripotent neural stem cell from the adult mouse brain
Rietze, R. L., Valcanis, H., Brooker, G. J. F., Thomas, T., Voss, A. K., & Bartlett, P. F. (2001) · Nature · doi:10.1038/35089085 · Cited by 665 · see citing works
Brewer, G. J. (1995) · Journal of Neuroscience Research · doi:10.1002/jnr.490420510 · Cited by 546 · see citing works
Belachew, S. M., Chittajallu, R., Aguirre, A. A., Yuan, X. Q., Kirby, M., Anderson, S. M., & Gallo, V. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200210110 · Cited by 489 · see citing works
Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons
Raps, S. P., Lai, J. C. K., Hertz, L., & Cooper, A. J. L. (1989) · Brain Research · doi:10.1016/0006-8993(89)91178-5 · Cited by 417 · see citing works
Makar, T. K., Nedergaard, M., Preuss, A. K., Gelbard, A. S., Perumal, A. S., & Cooper, A. J. L. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.62010045.x · Cited by 415 · see citing works
Fibroblast growth factors and their receptors in the central nervous system
Reuß, B., & Halbach, O. V. B. U. (2003) · Cell and Tissue Research · doi:10.1007/s00441-003-0756-7 · Cited by 412 · see citing works
Protein tyrosine phosphatases: mechanisms of catalysis and regulation
Denu, J. M., & Dixon, J. E. (1998) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(98)80095-1 · Cited by 403 · see citing works
Morrison, S. J., CSETE, M. E., Groves, A. K., Melega, W. P., Wold, B. J., & Anderson, D. J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-19-07370.2000 · Cited by 403 · see citing works
Smith, J., Ladi, E., Mayer-Pröschel, M., & Noble, M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.170209797 · Cited by 399 · see citing works
Role of Rac1 and Oxygen Radicals in Collagenase-1 Expression Induced by Cell Shape Change
Kheradmand, F., Werner, E., Tremble, P., Symons, M. H., & Werb, Z. (1998) · Science · doi:10.1126/science.280.5365.898 · Cited by 391 · see citing works
Rutherford, L. C., DeWan, A., Lauer, H. M., & Turrigiano, G. G. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-12-04527.1997 · Cited by 381 · see citing works
Brewer, G. J., & Cotman, C. W. (1989) · Brain Research · doi:10.1016/0006-8993(89)90144-3 · Cited by 376 · see citing works
A tripotential glial precursor cell is present in the developing spinal cord
Rao, M. S., Noble, M. A., & Mayer-Pröschel, M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3996 · Cited by 312 · see citing works
Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species
Brookes, P. S., Levonen, A.-L., Shiva, S., Sarti, P., & Darley-Usmar, V. M. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00901-2 · Cited by 298 · see citing works
2,7‐DICHLOROFLUORESCIN OXIDATION AND REACTIVE OXYGEN SPECIES: WHAT DOES IT MEASURE?
Jakubowski, W., & Bartosz, G. (2000) · Cell Biology International · doi:10.1006/cbir.2000.0556 · Cited by 292 · see citing works
Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition
Delaune, E. A., Lemaire, P., & Kodjabachian, L. (2004) · Development · doi:10.1242/dev.01582 · Cited by 290 · see citing works
Promotion and Attenuation of FGF Signaling Through the Ras-MAPK Pathway
Tsang, M., & Dawid, I. (2004) · Science's STKE · doi:10.1126/stke.2282004pe17 · Cited by 287 · see citing works
Annunziato, L. (2003) · Toxicology Letters · doi:10.1016/s0378-4274(02)00427-7 · Cited by 272 · see citing works
Neuronal cell death in nervous system development, disease, and injury (Review)
Martin, L. J. (2001) · International Journal of Molecular Medicine · doi:10.3892/ijmm.7.5.455 · Cited by 262 · see citing works
Werner, E., & Werb, Z. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200111028 · Cited by 252 · see citing works
Suzukawa, K., Miura, K., Mitsushita, J., Resau, J., Hirose, K., Crystal, R. G., & Kamata, T. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.18.13175 · Cited by 250 · see citing works
Gαi and Gαo are target proteins of reactive oxygen species
Nishida, M., Maruyama, Y., Tanaka, R., Kontani, K., Nagao, T., & Kurose, H. (2000) · Nature · doi:10.1038/35044120 · Cited by 245 · see citing works
Role of reactive oxygen species in hippocampal long‐term potentiation: Contributory or inhibitory?
Knapp, L. T., & Klann, E. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10371 · Cited by 223 · see citing works
Neuronal vulnerability in Parkinson’s disease
Hirsch, É. C., Faucheux, B. A., Damier, P., Prigent, A., & Agid, Y. (1997) · Journal of neural transmission. Supplementum · doi:10.1007/978-3-7091-6842-4_9 · Cited by 192 · see citing works
Signaling by reactive oxygen species in the nervous system
Maher, P. A., & Schubert, D. A. (2000) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000766 · Cited by 184 · see citing works
Redox Regulatory Mechanisms of Cellular Signal Transduction
Gabbita, S. P., Robinson, K. A., Stewart, C. A., Floyd, R. A., & Hensley, K. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1685 · Cited by 179 · see citing works
Fibroblast growth factors as regulators of central nervous system development and function
Dono, R. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00533.2002 · Cited by 177 · see citing works
The MTT assay underestimates the growth inhibitory effects of interferons
Jabbar, S., Twentyman, P., & Watson, J. V. S. (1989) · British Journal of Cancer · doi:10.1038/bjc.1989.306 · Cited by 177 · see citing works
Mitochondria and neuronal glutamate excitotoxicity
Nicholls, D. G., & Budd, S. L. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00123-6 · Cited by 171 · see citing works
Cell-Permeable Scavengers of Superoxide Prevent Long-Term Potentiation in Hippocampal Area CA1
Klann, E. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.452 · Cited by 165 · see citing works
Pagliacci, M. C., Spinozzi, F., Migliorati, G., Fumi, G., Smacchia, M. P., Grignani, F., Riccardi, C., & Nicoletti, I. (1993) · European Journal of Cancer · doi:10.1016/0959-8049(93)90297-s · Cited by 163 · see citing works
Maric, D., Marić, I., Chang, Y. H., et al. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00240.2003 · Cited by 154 · see citing works
Vergun, O. V., Sobolevsky, A. I., Yelshansky, M. V., et al. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0147j.x · Cited by 140 · see citing works
H2O2 Is a Novel, Endogenous Modulator of Synaptic Dopamine Release
Chen, B. T., Avshalumov, M. V., & Rice, M. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.6.2468 · Cited by 135 · see citing works
Castagné, V. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00012-x · Cited by 134 · see citing works
Rao, K. M. K., Padmanabhan, J., Dl, K., Cohen, H. J., Currie, M. S., & Weinberg, J. B. (1992) · Journal of Leukocyte Biology · doi:10.1002/jlb.51.5.496 · Cited by 133 · see citing works
Amoureux, M., Cunningham, B. A., Edelman, G. M., & Crossin, K. L. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03631.2000 · Cited by 132 · see citing works
Self-citationWhy are nigral catecholaminergic neurons more vulnerable than other cells in Parkinson's disease?
Hirsch, É. C. (1992) · Annals of Neurology · doi:10.1002/ana.410320715 · Cited by 123 · see citing works
Kumar, M. J., Nicholls, D. G., & Andersen, J. K. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306378200 · Cited by 120 · see citing works
Free radicals in Parkinson's disease
Koutsilieri, E., Scheller, C., Grünblatt, E., Keinosuke, N. A. R. A., Li, J., & Riederer, P. F. (2002) · Journal of Neurology · doi:10.1007/s00415-002-1201-7 · Cited by 117 · see citing works
Reactive oxygen species and nitric oxide mediate plasticity of neuronal calcium signaling
Yermolaieva, O., Brot, N., Weissbach, H., Heinemann, S. H., & Hoshi, T. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.1.448 · Cited by 110 · see citing works
Participation of the mitochondrial genome in the differentiation of neuroblastoma cells
Vayssière, J., Cordeau‐Lossouarn, L., Larcher, J. C., Basseville, M., Gros, F., & Croizat, B. (1992) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/bf02631065 · Cited by 103 · see citing works
Electrophysiology of embryonic, adult and aged rat hippocampal neurons in serum-free culture
Evans, M. S., Collings, M. A., & Brewer, G. J. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(97)00159-3 · Cited by 98 · see citing works
Feeding active neurons: (re)emergence of a nursing role for astrocytes
Bouzier‐Sore, A., Merle, M., Magistretti, P. J., & Pellerin, L. (2002) · Journal of Physiology-Paris · doi:10.1016/s0928-4257(02)00016-5 · Cited by 93 · see citing works
A role for mitochondria as potential regulators of cellular life span
Xu, D. L., & Finkel, T. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)00464-3 · Cited by 89 · see citing works
Sporns, O., Edelman, G. M., & Crossin, K. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.2.542 · Cited by 88 · see citing works
Self-citationRole of Mitochondria in Neuronal Apoptosis
Gorman, A. M., Ceccatelli, S., & Orrenius, S. (2000) · Developmental Neuroscience · doi:10.1159/000017460 · Cited by 87 · see citing works
Biophysical basis of brain activity: implications for neuroimaging
Shulman, R. G., Hyder, F., & Rothman, D. L. (2002) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583502003803 · Cited by 79 · see citing works
Antioxidants are required during the early critical period, but not later, for neuronal survival
Perry, S. W., Norman, J. P., Stout, A., & Gelbard, H. A. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20272 · Cited by 79 · see citing works
Xie, C., Markesbery, W. R., & Lovell, M. A. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00268-3 · Cited by 78 · see citing works
Atkins, C. M., & Sweatt, J. D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07241.1999 · Cited by 74 · see citing works
Scanlon, J. M., & Reynolds, I. J. (1998) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1998.71062392.x · Cited by 74 · see citing works
Katoh, S., Mitsui, Y., Kitani, K., & Suzuki, T. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7514 · Cited by 66 · see citing works
Method for serum-free culture of late fetal and early postnatal rat brainstem neurons
Kivell, B. M., McDonald, F. J., & Miller, J. H. (2001) · Brain Research Protocols · doi:10.1016/s1385-299x(00)00037-4 · Cited by 64 · see citing works
Kamata, H., Tanaka, C., Yagisawa, H., & Hirata, H. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12806-8 · Cited by 63 · see citing works
Evolutionary conservation of key structures and binding functions of neural cell adhesion molecules.
Hoffman, S., Chuong, C., & Edelman, G. M. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.21.6881 · Cited by 46 · see citing works
Oxidative events in neuronal and glial cell-enriched fractions of rat cerebral cortex
Café, C., Torri, C., Bertorelli, L., Tartara, F., Tancioni, F., Gaetani, P., y Baena, R. R., & Marzatico, F. (1995) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(95)00086-d · Cited by 45 · see citing works
Katoh, S., Mitsui, Y., Kitani, K., et al. (1999) · Biochemical Journal · doi:10.1042/bj3380465 · Cited by 43 · see citing works
Role of neuron-glia interaction in the regulation of brain glucose utilization.
Pellerin, L., Bonvento, G., Chatton, J., Pierre, K., & Magistretti, P. J. (2002) · PubMed · Cited by 43 · see citing works
The role of the RE1 element in activation of the NR1 promoter during neuronal differentiation
Bai, G., Zhuang, Z.-Y., Liu, A., Chai, Y., & Hoffman, P. W. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01922.x · Cited by 38 · see citing works
Lee, J., Koh, H. C., Chang, M., et al. (2003) · Neuroreport · doi:10.1097/01.wnr.0000078542.07662.4b · Cited by 34 · see citing works
Mitochondrial maturation during neuronal differentiation in vivo and in vitro
Cordeau‐Lossouarn, L., Vayssière, J., Larcher, J.-C., Gros, F., & Croizat, B. (1991) · Biology of the Cell · doi:10.1016/0248-4900(91)90051-n · Cited by 29 · see citing works
Hasty, P. (2001) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00294-9 · Cited by 27 · see citing works
Lee, J., Koh, H. C., Chang, M., et al. (2003) · Neuroreport · doi:10.1097/00001756-200307180-00024 · Cited by 27 · see citing works
Cheung, N. S., Hickling, Y. M., & Beart, P. M. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00613-7 · Cited by 21 · see citing works
Role of neuron-glia interaction in the regulation of brain glucose utilization.
Pellerin, L., Bonvento, G., Chatton, J. Y., et al. (2002) · IRIS · Cited by 20 · see citing works
Changes in the β-subunit of mitochondrial F1ATPase during neurogenesis
Vayssière, J., Larcher, J.-C., Gros, F., et al. (1987) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(87)91341-6 · Cited by 7 · see citing works
Changes in mitochondrial proteins during neuroblastoma differentiation
Vayssière, J., Berthelot, F., Croizat, B., et al. (1984) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(84)91269-5 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Association of reactive oxygen species levels and radioresistance in cancer stem cells
Diehn, M., Cho, R. W., Lobo, N. A., Kalisky, T., Dorie, M. J., Kulp, A. N., Qian, D., Lam, J. S., Ailles, L. E., Wong, M., et al. (2009) · Nature · doi:10.1038/nature07733 · Cited by 2,555 · see citing works
Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes
Hamanaka, R. B., & Chandel, N. S. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.04.002 · Cited by 1,011 · see citing works
Le Belle, J. E., Orozco, N. M., Paucar, A. A., Saxe, J. P., Mottahedeh, J., Pyle, A. D., Wu, H., & Kornblum, H. I. (2011) · Cell Stem Cell · doi:10.1016/j.stem.2010.11.028 · Cited by 789 · see citing works
Hamanaka, R. B., Glasauer, A., Hoover, P., Yang, S., Blatt, H., Mullen, A. R., Getsios, S., Gottardi, C. J., DeBerardinis, R. J., Lavker, R. M., et al. (2013) · Science Signaling · doi:10.1126/scisignal.2003638 · Cited by 315 · see citing works
Lampe, K. J., Namba, R. M., Silverman, T. R., Bjugstad, K. B., & Mahoney, M. J. (2009) · Biotechnology and Bioengineering · doi:10.1002/bit.22352 · Cited by 98 · see citing works
Reactive oxygen species and the neuronal fate
Kennedy, K. A. M., Sandiford, S. D. E., Skerjanc, I. S., & Li, S. S.-C. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0807-2 · Cited by 89 · see citing works
- Authors
- Tsatmali, M., Walcott, E. C., & Crossin, K. L.
- Affiliations
- Scripps Research Institute (US)
- Neurosciences Institute (US)
- Corresponding author
- Crossin, Kathryn L.
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2005-04
- Volume
- 1040
- Issue
- 1-2
- Pages
- 137-150
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2002030791
- Cited by
- 133
- References
- 98
- Citations by year
- 2025: 4 · 2023: 2 · 2022: 5 · 2021: 3 · 2020: 9 · 2019: 4 · 2018: 6 · 2017: 9 · 2016: 10 · 2015: 14 · 2014: 5 · 2013: 12 · 2012: 15
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- reactive oxygen species, neuronal differentiation, neural progenitor cells, newborn neurons, cortical development, FGF2, TUBB3, superoxide, hydrogen peroxide, mitochondrial respiratory chain, superoxide dismutase, catalase, astrocytes, cell isolation, oxidative stress signaling
- MeSH terms
- Animals, Animals, Newborn, Cell Differentiation, Cells, Cultured, Female, Neurons, Pregnancy, Stem Cells, Rats, Wistar, Reactive Oxygen Species, Mitochondrial Proteins, Rats
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