Down-Regulation of miR-23a-3p Mediates Irradiation-Induced Neuronal Apoptosis
Open accessAbstract
Radiation-induced central nervous system toxicity is a significant risk factor for patients receiving cancer radiotherapy. Surprisingly, the mechanisms responsible for the DNA damage-triggered neuronal cell death following irradiation have yet to be deciphered. Using primary cortical neuronal cultures in vitro, we demonstrated that X-ray exposure induces the mitochondrial pathway of intrinsic apoptosis and that miR-23a-3p plays a significant role in the regulation of this process. Primary cortical neurons exposed to irradiation show the activation of DNA-damage response pathways, including the sequential phosphorylation of ATM kinase, histone H2AX, and p53. This is followed by the p53-dependent up-regulation of the pro-apoptotic Bcl2 family molecules, including the BH3-only molecules PUMA, Noxa, and Bim, leading to mitochondrial outer membrane permeabilization (MOMP) and the release of cytochrome c, which activates caspase-dependent apoptosis. miR-23a-3p, a negative regulator of specific pro-apoptotic Bcl-2 family molecules, is rapidly decreased after neuronal irradiation. By increasing the degradation of PUMA and Noxa mRNAs in the RNA-induced silencing complex (RISC), the administration of the miR-23a-3p mimic inhibits the irradiation-induced up-regulation of Noxa and Puma. These changes result in an attenuation of apoptotic processes such as MOMP, the release of cytochrome c and caspases activation, and a reduction in neuronal cell death. The neuroprotective effects of miR-23a-3p administration may not only involve the direct inhibition of pro-apoptotic Bcl-2 molecules downstream of p53 but also include the attenuation of secondary DNA damage upstream of p53. Importantly, we demonstrated that brain irradiation in vivo results in the down-regulation of miR-23a-3p and the elevation of pro-apoptotic Bcl2-family molecules PUMA, Noxa, and Bax, not only broadly in the cortex and hippocampus, except for Bax, which was up-regulated only in the hippocampus but also selectively in isolated neuronal populations from the irradiated brain. Overall, our data suggest that miR-23a-3p down-regulation contributes to irradiation-induced intrinsic pathways of neuronal apoptosis. These regulated pathways of neurodegeneration may be the target of effective neuroprotective strategies using miR-23a-3p mimics to block their development and increase neuronal survival after irradiation.
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?
miR-23a-3p was found downregulated in mice cortex, hippocampus, and neurons after brain radiation, while the expression of Bcl family members was upregulated, causing secondary DNA damage.
“The miR-23a-3p was found downregulated in mice cortex, hippocampus, and neurons after brain radiation, while the expression of Bcl family members was upregulated, causing secondary DNA damage.”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [139]
Results §2.1 reports miR-23a-3p down-regulation in irradiated mouse cortex, hippocampus, and isolated neurons, alongside increased expression of selected pro-apoptotic Bcl-2 family members. The claim’s causal ending is not supported: the Discussion describes irradiation-induced DNA damage as preceding activation of p53 and up-regulation of those molecules, which then promote apoptosis—not as damage caused by their up-regulation. Bax was also not up-regulated in the cortex. (LLM, conf=0.89)
Experimental — accuracy not yet measuredIntervention with overexpression of miR-23a-3p can protect nerves and attenuate the apoptotic process and neuronal cell death.
“intervention with overexpression of miR-23a-3p can protect nerves and attenuate the apoptotic process and neuronal cell death [139].”
From Recent advances of miR-23 in human diseases and growth development (2025) · cites this paper as [139]
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
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
The ATM–Chk2 and ATR–Chk1 Pathways in DNA Damage Signaling and Cancer
Smith, J., Tho, L. M., Xu, N., & Gillespie, D. A. (2010) · Advances in cancer research · doi:10.1016/b978-0-12-380888-2.00003-0 · Cited by 1,279 · see citing works
Radiation‐induced dementia in patients cured of brain metastases
DeAngelis, L. M., Delattre, J., & Posner, J. B. (1989) · Neurology · doi:10.1212/wnl.39.6.789 · Cited by 951 · see citing works
Rogakou, E., Nieves-Neira, W., Boon, C., Pommier, Y., & Bonner, W. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.13.9390 · Cited by 747 · see citing works
Extreme sensitivity of adult neurogenesis to low doses of X-irradiation.
Mizumatsu, S., Monje, M., Morhardt, D. R., Rola, R., Palmer, T. D., & Fike, J. R. (2003) · PubMed · Cited by 657 · see citing works
Liu, D.-Z., Tian, Y., Ander, B. P., Xu, H., Stamova, B. S., Zhan, X., Turner, R. J., Jickling, G. C., & Sharp, F. R. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.186 · Cited by 496 · see citing works
Krol, J., Busskamp, V., Markiewicz, I., Stadler, M. B., Ribi, S., Richter, J., Duebel, J., Bicker, S., Fehling, H. J., Schübeler, D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.03.039 · Cited by 470 · see citing works
BH3-only proteins: Orchestrators of apoptosis
Shamas‐Din, A., Brahmbhatt, H., Leber, B. F., & Andrews, D. W. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.11.024 · Cited by 368 · see citing works
Loughery, J., Cox, M. L., Smith, L. M., & Meek, D. W. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku501 · Cited by 308 · see citing works
Effects of treatment on long‐term survivors with malignant astrocytomas
Imperato, J. P., Paleologos, N. A., & Vick, N. A. (1990) · Annals of Neurology · doi:10.1002/ana.410280614 · Cited by 254 · see citing works
Redell, J. B., Liu, Y., & Dash, P. K. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21945 · Cited by 214 · see citing works
Lithium Treatment Prevents Neurocognitive Deficit Resulting from Cranial Irradiation
Yazlovitskaya, E. M., Edwards, E., Thotala, D. K., Fu, A., Osusky, K. L., Whetsell, W. O., Boone, B. E., Shinohara, E. T., & Hallahan, D. E. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-2740 · Cited by 187 · see citing works
MicroRNAs in the ionizing radiation response and in radiotherapy
Metheetrairut, C., & Slack, F. J. (2013) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.01.002 · Cited by 185 · see citing works
The caspase‐activated DN ase: apoptosis and beyond
Larsen, B. D., & Sørensen, C. S. (2016) · FEBS Journal · doi:10.1111/febs.13970 · Cited by 180 · see citing works
p53-independent regulation of p21Waf1/Cip1 expression and senescence by Chk2.
Aliouat-Denis, C.-M., Dendouga, N., Van den Wyngaert, I., Goehlmann, H., Steller, U., van de Weyer, I., Van Slycken, N., Andries, L., Kass, S., Luyten, W., et al. (2005) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-05-0121 · Cited by 177 · see citing works
Molecular, Cellular and Functional Effects of Radiation-Induced Brain Injury: A Review
Bálentová, S., & Adamkov, M. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161126068 · Cited by 176 · see citing works
Proteins released from degenerating neurons are surrogate markers for acute brain damage
Siman, R., McIntosh, T. K., Soltesz, K., Chen, Z., Neumar, R. W., & Roberts, V. L. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.03.016 · Cited by 164 · see citing works
Chen, Q., Xu, J., Li, L., Li, H., Mao, S., Zhang, F., Zen, K., Cy, Z., & Zhang, Q. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.92 · Cited by 163 · see citing works
BOK and NOXA Are Essential Mediators of p53-dependent Apoptosis
Yakovlev, A. G., Giovanni, S. D., Wang, G., Liu, W., Stoica, B. A., & Faden, A. I. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313526200 · Cited by 162 · see citing works
Self-citationSabirzhanov, B. E., Zhao, Z., Stoica, B. A., Loane, D. J., Wu, J., Borroto, C., Dorsey, S. G., & Faden, A. I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1260-14.2014 · Cited by 152 · see citing works
Self-citationGobbel, G. T., Bellinzona, M., Vogt, A. R., Gupta, N. M., Fike, J. R., & Chan, P. H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00147.1998 · Cited by 148 · see citing works
Suhaili, S. H., Karimian, H., Stellato, M., Lee, T.-H., & Aguilar, M. (2017) · Biophysical Reviews · doi:10.1007/s12551-017-0308-0 · Cited by 115 · see citing works
Jimenez-Mateos, E. M., & Henshall, D. C. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.02.027 · Cited by 114 · see citing works
Proapoptotic BAX and BAK control multiple initiator caspases
Ruiz‐Vela, A., Opferman, J. T., Cheng, E. H. Y., & Korsmeyer, S. J. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400375 · Cited by 112 · see citing works
Koturbash, I., Zemp, F. J., Kolb, B. E., & Kovalchuk, O. (2010) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2010.05.007 · Cited by 110 · see citing works
Temporal Differences in MicroRNA Expression Patterns in Astrocytes and Neurons after Ischemic Injury
Ziu, M., Fletcher, L., Rana, S. R., Jimenez, D. F., & Digicaylioglu, M. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014724 · Cited by 106 · see citing works
Kempf, S. J., Casciati, A., Buratovic, S., Janik, D., von Toerne, C., Ueffing, M., Neff, F., Moertl, S., Stenerlöw, B., Saran, A., et al. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-57 · Cited by 102 · see citing works
Akhter, R., Sanphui, P., & Biswas, S. C. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.519355 · Cited by 99 · see citing works
Central Nervous System Responses to Simulated Galactic Cosmic Rays
Cekanaviciute, E., Rosi, S., & Costes, S. V. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113669 · Cited by 99 · see citing works
Tikka, T., Usenius, T., Tenhunen, M., Keinänen, R., & Koistinaho, J. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00543.x · Cited by 96 · see citing works
Emerging Roles of microRNAs in the Molecular Responses to Hypoxia
Crosby, M. E., Devlin, C. M., Glazer, P. M., Calin, G. A., & Ivan, M. (2009) · Current Pharmaceutical Design · doi:10.2174/138161209789649367 · Cited by 77 · see citing works
Radiation Exposure and Health Effects – is it Time to Reassess the Real Consequences?
Thomas, G. A. O., & Symonds, P. R. (2016) · Clinical Oncology · doi:10.1016/j.clon.2016.01.007 · Cited by 76 · see citing works
miR-711 upregulation induces neuronal cell death after traumatic brain injury
Sabirzhanov, B. E., Stoica, B. A., Zhao, Z., Loane, D. J., Wu, J., Dorsey, S. G., & Faden, A. I. (2015) · Cell Death and Differentiation · doi:10.1038/cdd.2015.132 · Cited by 76 · see citing works
Self-citationXu, S., Zhang, R., Niu, J., Cui, D., Xie, B., Zhang, B., Lu, K., Yu, W., Wang, X., & Zhang, Q. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms131216945 · Cited by 73 · see citing works
Jeong, J.-H., Kang, S., Park, K., Chang, H., Magae, J., & Chang, Y. (2010) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-09-1159 · Cited by 73 · see citing works
Thotala, D. K., Karvas, R. M., Engelbach, J. A., Garbow, J. R., Hallahan, A. N., DeWees, T. A., Laszlo, A., & Hallahan, D. E. (2015) · Oncotarget · doi:10.18632/oncotarget.5253 · Cited by 72 · see citing works
Bok is a genuine multi-BH-domain protein that triggers apoptosis in the absence of Bax and Bak
Einsele-Scholz, S., Malmsheimer, S., Bertram, K., Stehle, D., Johänning, J., Manz, M., Daniel, P. T., Gillissen, B. F., Schulze-Osthoff, K., & Essmann, F. (2016) · Journal of Cell Science · doi:10.1242/jcs.181727 · Cited by 65 · see citing works
Leucine-Rich Repeat Kinase 2 (LRRK2) phosphorylates p53 and induces p21WAF1/CIP1 expression
Ho, D. H., Kim, H. J., Kim, J., Sim, H., Ahn, H. M., Kim, J., Seo, H., Chung, K. C., Park, B.-J., Son, I., et al. (2015) · Molecular Brain · doi:10.1186/s13041-015-0145-7 · Cited by 62 · see citing works
Uo, T., Kinoshita, Y., & Morrison, R. S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3222-05.2007 · Cited by 61 · see citing works
Kempf, S. J., Moertl, S., Sepe, S., von Toerne, C., Hauck, S. M., Atkinson, M. J., Mastroberardino, P. G., & Tapio, S. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00114 · Cited by 59 · see citing works
Nam, C., Doi, K., & Nakayama, H. (2010) · PubMed · doi:10.14670/hh-25.485 · Cited by 59 · see citing works
Exosomal miR-7 Mediates Bystander Autophagy in Lung after Focal Brain Irradiation in Mice
Cai, S., Shi, G.-S., Cheng, H., Zeng, Y.-N., Li, G. L., Zhang, M., Song, M. S., Zhou, P., Tian, Y., Cui, F., et al. (2017) · International Journal of Biological Sciences · doi:10.7150/ijbs.18890 · Cited by 59 · see citing works
Zhang, Y., Cheng, Z., Wang, C., Ma, H., Meng, W., & Zhao, Q. (2016) · Neurochemical Research · doi:10.1007/s11064-016-1967-0 · Cited by 56 · see citing works
Kempf, S. J., Buratovic, S., von Toerne, C., Moertl, S., Stenerlöw, B., Hauck, S. M., Atkinson, M. J., Eriksson, P., & Tapio, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110464 · Cited by 52 · see citing works
Using lithium as a neuroprotective agent in patients with cancer
Khasraw, M., Ashley, D. M., Wheeler, G., & Berk, M. (2012) · BMC Medicine · doi:10.1186/1741-7015-10-131 · Cited by 50 · see citing works
Gillissen, B. F., Richter, A. M., Richter, A., Preißner, R., Schulze‐Osthoff, K., Eßmann, F., & Daniel, P. T. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.754184 · Cited by 50 · see citing works
MiR-21 is Continually Elevated Long-Term in the Brain after Exposure to Ionizing Radiation
Shi, Y., Zhang, X., Tang, X., Wang, P., Wang, H., & Wang, Y. (2011) · Radiation Research · doi:10.1667/rr2764.1 · Cited by 47 · see citing works
Feng, X., Liu, S., Chen, D., Rosi, S., & Gupta, N. M. (2018) · eLife · doi:10.7554/elife.38865 · Cited by 44 · see citing works
Vauzour, D., Vafeiadou, K., Rice-Evans, C. A., Cadenas, E., & Spencer, J. P. E. (2007) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2007.09.021 · Cited by 35 · see citing works
Medical and policy considerations for nuclear and radiation accidents, incidents and terrorism
Gale, R. P. (2017) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000380 · Cited by 29 · see citing works
Ionizing radiation causes increased tau phosphorylation in primary neurons
Li, L., Wang, W., Welford, S. M., Zhang, T., Wang, X., & Zhu, X. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12769 · Cited by 26 · see citing works
Neuronal death is an active, caspase‐dependent process after moderate but not severe DNA damage
Gobbel, G. T., & Chan, P. H. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00070.x · Cited by 26 · see citing works
Mata-Garrido, J., Casafont, Í., Tapia, O., Berciano, M. T., & Lafarga, M. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0312-9 · Cited by 24 · see citing works
Tu, S., Liu, Z., Fu, J., Zhu, W., Luo, D., & Wan, F. (2012) · Cardiology · doi:10.1159/000338701 · Cited by 19 · see citing works
Differential Apoptosis Radiosensitivity of Neural Progenitors in Adult Mouse Hippocampus
Li, Y.-Q., Cheng, Z., & Wong, C. S. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060970 · Cited by 17 · see citing works
Treulen, F., Uribe, P., Boguen, R. E., & Villegas, J. (2015) · Molecular Human Reproduction · doi:10.1093/molehr/gav067 · Cited by 13 · see citing works
Al‐Khalaf, H. H., Hendrayani, S., & Aboussekhra, A. (2012) · Molecular Carcinogenesis · doi:10.1002/mc.20864 · Cited by 13 · see citing works
Flagged first, then by citations
1 of the 58 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Microglia as Therapeutic Target for Radiation-Induced Brain Injury
Liu, Q., Yan, H., Duan, M., Yang, Q., Ren, B., & Tang, F. R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158286 · Cited by 83 · see citing works
Pathological and Inflammatory Consequences of Aging
García‐Domínguez, M. (2025) · Biomolecules · doi:10.3390/biom15030404 · Cited by 75 · see citing works
MicroRNAs: protective regulators for neuron growth and development
Wu, Z., Liu, Z., Xiong, H.-H., Zhou, Z.-P., OuYang, L., XIE, F.-K., Tang, Y.-M., Wu, Z.-D., & Tang, Y. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.353481 · Cited by 38 · see citing works
Zheng, Z., Wang, B., Zhao, Q., Zhang, Y., Wei, J., Meng, L., Xin, Y., & Jiang, X. M. (2021) · European Radiology · doi:10.1007/s00330-021-08164-6 · Cited by 32 · see citing works
Qu, Y., Xu, Y., Jiang, Y., Yu, D., Jiang, X., & Zhao, L. (2021) · The FASEB Journal · doi:10.1096/fj.202001185rr · Cited by 31 · see citing works
Sheng, S., Zou, M., Yang, Y., Guan, M., Ren, S., Wang, X., Wang, L., & Xue, Y. (2021) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-021-00606-1 · Cited by 31 · see citing works
Lutsenko, I. А., Nikiforova, M. E., Кошенскова, К. А., Kiskin, M. A., Nelyubina, Y. V., Primakov, P. V., Fedin, M. V., Becker, O. B., Shender, V. О., Malyants, I. K., et al. (2021) · Russian Journal of Coordination Chemistry · doi:10.1134/s1070328421350013 · Cited by 27 · see citing works
Lutsenko, I. А., Kiskin, M. A., Кошенскова, К. А., Primakov, P. V., Хорошилов, А., Bekker, O. B., & Еременко, И. Л. (2021) · Russian Chemical Bulletin · doi:10.1007/s11172-021-3109-3 · Cited by 26 · see citing works
Sabirzhanov, B. E., Makarevich, O. D., Barrett, J. P., Jackson, I. L., Glaser, E. P., Faden, A. I., & Stoica, B. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155239 · Cited by 23 · see citing works
Self-citationISGylation is induced in neurons by demyelination driving ISG15-dependent microglial activation
Clarkson, B. D. S., Grund, E. M., David, K., Johnson, R. K., & Howe, C. L. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02618-4 · Cited by 21 · see citing works
Analysis of potential microRNA biomarkers for multiple sclerosis
Al-Temaimi, R. A., Alshammari, N., & Alroughani, R. (2024) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2024.104903 · Cited by 17 · see citing works
Malakoti, F., Alemi, F., Younesi, S., Majidinia, M., Yousefi, B., Morovat, P., Khelghati, N., Maleki, M., Karimian, A., & Asemi, Z. (2021) · DNA repair · doi:10.1016/j.dnarep.2020.103036 · Cited by 17 · see citing works
Cognitive dysfunction induced by cranial radiotherapy: mechanisms and therapeutic methods
Li, X., & Ding, Z. (2024) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2024.111106 · Cited by 16 · see citing works
Jin, M., Liu, Y., Hu, G., Li, X., Jia, N., Cui, X., Li, Z., Ai, L., Xie, M., Xue, F., et al. (2023) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2023.01.035 · Cited by 13 · see citing works
Zhou, Q., Yin, J., Tan, J., Li, S., Jiang, C., & He, Y. (2021) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2021.115800 · Cited by 12 · see citing works
Wu, C., Zhu, Q., Yao, Y., Shi, Z., Jin, C., & Chen, L. (2021) · Developmental Neuroscience · doi:10.1159/000521167 · Cited by 10 · see citing works
Tian, Q., Chen, C., Qiu, W., Wu, H., Zhou, L., Dai, Z., Li, Z., & Chen, S. (2021) · Stem Cells International · doi:10.1155/2021/5540149 · Cited by 10 · see citing works
Liu, L., Qin, T., Guo, L. T., Rong-Rong, H., Jing, Y., Lai, P., Xue, Y., & Ding, G. (2022) · International Journal of Radiation Biology · doi:10.1080/09553002.2022.2038806 · Cited by 10 · see citing works
Recent advances of miR-23 in human diseases and growth development
Qian, X., Jiang, Y., Yang, Y., Zhang, Y., Xu, N., Xu, B., Pei, K., Yu, Z., & Wu, W. (2025) · Non-coding RNA Research · doi:10.1016/j.ncrna.2024.12.010 · Cited by 5 · see citing works
Wang, J., Parajuli, N., Wang, Q., Khalasawi, N., Peng, H., Zhang, J., Yin, C., Mi, Q., & Zhou, L. (2023) · Biology · doi:10.3390/biology12070925 · Cited by 3 · see citing works
Pathological Mechanisms of Irradiation‐Induced Neurological Deficits in the Developing Brain
Richard, S. A. (2025) · European Journal of Neuroscience · doi:10.1111/ejn.70070 · Cited by 2 · see citing works
Rahmi, U., Goenawan, H., Sylviana, N., Setiawan, I., Putri, S. T., Andriyani, S., Fitriana, L. A., & Murtiani, F. (2025) · Biomedical & Pharmacology Journal · doi:10.13005/bpj/3128 · Cited by 2 · see citing works
Interplay Between Key Molecular Signaling Pathways and Immune Players Following Brain Irradiation
Richard, S. A. (2025) · Mediators of Inflammation · doi:10.1155/mi/8833271 · Cited by 2 · see citing works
Novobilský, R., Kušnierová, P., Štěpán, D., Bártová, P., Stejskal, D., & Bar, M. (2025) · PLoS ONE · doi:10.1371/journal.pone.0333801 · Cited by 1 · see citing works
Tao, Q., Li, X., Xia, Y., Zheng, B., Yan, Y., Wang, S., & Jia, L. (2024) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2024.101858 · Cited by 1 · see citing works
Research Progress in the Regulation of Puma Expression by microRNA in Non-Neoplastic Diseases
田, 王. (2022) · Advances in Clinical Medicine · doi:10.12677/acm.2022.121104
Clarkson, B. D. S., Grund, E. M., David, K., Johnson, R. K., & Howe, C. L. (2022) · Figshare · doi:10.6084/m9.figshare.21366140
Issı, E. S., Onrat, S. T., Gönen, H. N., Acar, H., & Börü, Ü. T. (2026) · Diagnostics · doi:10.3390/diagnostics16060894
Jia, R., Zhu, T., Tian, X., Wang, S., Zhang, S., Fan, F., Wang, Y., Chai, Y., Chen, Z., Hu, Y., et al. (2026) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2026.1807959
Saçaki, C. S., Lührs, L., Dziedzic, D. S. M., da Rosa, N. N., Rosa, A. L. D., Souza, C., Irioda, A. C., Mogharbel, B. F., & de Carvalho, K. A. T. (2026) · Current Tissue Microenvironment Reports · doi:10.1007/s43152-026-00070-7
Xiao, J., Qi, S., Li, Y., Li, Y., & Tang, H. H. (2026) · Journal of Translational Medicine · doi:10.1186/s12967-026-08823-6
- Authors
- Sabirzhanov, B., Makarevich, O., Barrett, J., Jackson, I. L., Faden, A. I., & Stoica, B. A.
- Affiliations
- University of Maryland, Baltimore (US)
- Corresponding author
- Sabirzhanov, Boris
- Stoica, Bogdan A.
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2020-05-24
- Volume
- 21
- Issue
- 10
- Pages
- 3695
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC7279507
- OpenAlex
- W3028447208
- Cited by
- 31
- References
- 58
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 4 · 2023: 2 · 2022: 6 · 2021: 9 · 2020: 1
- FWCI
- 1.54
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Neurological Disorders and Stroke (R01 NS091191, R01 NS096002)
- United States (U.S.) Department of Veterans Affairs, Rehabilitation Research and Development Service (# 1I01 RX001993)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- miR-23a-3p, X-ray irradiation, central nervous system toxicity, mitochondrial apoptosis, p53, Bcl-2 family proteins, PUMA, Noxa, Bax, mitochondrial outer membrane permeabilization, cytochrome c release, caspase activation, DNA damage response, neuroprotection
- MeSH terms
- Bcl-2-Like Protein 11, Animals, DNA, DNA Damage, DNA Repair, Male, Neurons, Radiation, Ionizing, Signal Transduction, Tumor Suppressor Protein p53, Apoptosis, Proto-Oncogene Proteins c-bcl-2, Tumor Suppressor Proteins, MicroRNAs, Apoptosis Regulatory Proteins, Mice, Rats, Ataxia Telangiectasia Mutated Proteins
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