A new advanced cellular model of functional cholinergic-like neurons developed by reprogramming the human SH-SY5Y neuroblastoma cell line
Open accessAbstract
Modeling human neuronal properties in physiological and pathological conditions is essential to identify novel potential drugs and to explore pathological mechanisms of neurological diseases. For this purpose, we generated a three-dimensional (3D) neuronal culture, by employing the readily available human neuroblastoma SH-SY5Y cell line, and a new differentiation protocol. The entire differentiation process occurred in a matrix and lasted 47 days, with 7 days of pre-differentiation phase and 40 days of differentiation, and allowed the development of a 3D culture in conditions consistent with the physiological environment. Neurons in the culture were electrically active, were able to establish functional networks, and showed features of cholinergic neurons. Hence here we provide an easily accessible, reproducible, and suitable culture method that might empower studies on synaptic function, vesicle trafficking, and metabolism, which sustain neuronal activity and cerebral circuits. Moreover, this novel differentiation protocol could represent a promising cellular tool to study physiological cellular processes, such as migration, differentiation, maturation, and to develop novel therapeutic approaches.
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SH-SY5Y cell line failed to consistently replicate these properties by exhibiting limited electrophysiological functionality and weak or absent synaptic activity.
“In contrast, D'Aloia et al. (2024) found that the SH-SY5Y cell line failed to consistently replicate these properties by exhibiting limited electrophysiological functionality and weak or absent synaptic activity.”
From Primary cell cultures versus immortalized cell lines: critical comparative insights into biological fidelity and translational applications (2026) · cites this paper as D'Aloia et al. (2024)
The Introduction (page unavailable) says that most earlier studies of differentiated SH-SY5Y cells found only low-frequency induced action potentials, with faint spontaneous spiking reported by one group. But the Results report spontaneous activity in the authors’ 3D DMAP2 Mix cultures, rising to 37% of cells at 40 days. The claim captures a limitation of earlier culture conditions but overgeneralizes it to the cell line and the study’s findings. (LLM, conf=0.87)
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Cites
Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors
Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., & Yamanaka, S. (2007) · Cell · doi:10.1016/j.cell.2007.11.019 · Cited by 20,221 · see citing works
Neurotrophins and their receptors: A convergence point for many signalling pathways
Chao, M. V. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1078 · Cited by 2,298 · see citing works
Stem cells: past, present, and future
Zakrzewski, W., Dobrzyński, M., Szymonowicz, M. K., & Rybak, Z. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1165-5 · Cited by 1,886 · see citing works
Conserved cell types with divergent features in human versus mouse cortex
Hodge, R. D., Bakken, T. E., Miller, J. A., Smith, K. A., Barkan, E. R., Graybuck, L. T., Close, J. L., Long, B., Johansen, N., Penn, O., et al. (2019) · Nature · doi:10.1038/s41586-019-1506-7 · Cited by 1,775 · cited 1× · see citing works
“Speci fi cally, marked variations were observed in the proportions of neuronal and non-neuronal cells and in the transcription of genes associated with neuronal structure and activity [3].”
Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis
Christopherson, K. S., Ullian, E. M., Stokes, C. C. A., Mullowney, C. E., Hell, J. W., Agah, A., Lawler, J., Mosher, D. F., Bornstein, P., & Barres, B. A. (2005) · Cell · doi:10.1016/j.cell.2004.12.020 · Cited by 1,688 · see citing works
Modelling schizophrenia using human induced pluripotent stem cells
Brennand, K. J., Simone, A., Jou, J., Gelboin-Burkhart, C., Tran, N., Sangar, S., Li, Y., Mu, Y., Chen, G., Yu, D., et al. (2011) · Nature · doi:10.1038/nature09915 · Cited by 1,375 · see citing works
Marchetto, M. C. N., Carromeu, C., Acab, A., Yu, D., Yeo, G. W., Mu, Y., Chen, G., Gage, F. H., & Muotri, A. R. (2010) · Cell · doi:10.1016/j.cell.2010.10.016 · Cited by 1,329 · see citing works
Biedler, J. L., Helson, L., & Spengler, B. A. (1973) · PubMed · Cited by 1,295 · see citing works
Probing sporadic and familial Alzheimer’s disease using induced pluripotent stem cells
Israel, M. A., Yuan, S. H., Bardy, C., Reyna, S. M., Mu, Y., Herrera, C., Hefferan, M. P., Van Gorp, S., Nazor, K. L., Boscolo, F. S., et al. (2012) · Nature · doi:10.1038/nature10821 · Cited by 1,253 · see citing works
Considerations for the use of SH-SY5Y neuroblastoma cells in neurobiology
Kovalevich, J., & Langford, D. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-640-5_2 · Cited by 1,005 · see citing works
Encinas, M., Iglesias, M., Liu, Y., Wang, H., Muhaisen, A., Ceña, V., Gallego, C., & Comella, J. X. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0750991.x · Cited by 822 · see citing works
Tovar, K. R., & Westbrook, G. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-10-04180.1999 · Cited by 786 · see citing works
LRRK2 Mutant iPSC-Derived DA Neurons Demonstrate Increased Susceptibility to Oxidative Stress
Nguyen, H. N., Byers, B., Cord, B. J., Shcheglovitov, A., Byrne, J., Gujar, P., Kee, K., Schüle, B., Dolmetsch, R. E., Langston, J. W., et al. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.01.013 · Cited by 748 · see citing works
Zheng, X., Boyer, L., Jin, M., Mertens, J., Kim, Y., Ma, L., Ma, L., Hamm, M., Gage, F. H., & Hunter, T. (2016) · eLife · doi:10.7554/elife.13374 · Cited by 671 · cited 3× · see citing works
“In all the protocols described above, the culture medium was changed every 3 – 4 days by removing 30% of the total volume and adding fresh medium corresponding to 40% of the total volume.”
Coordinate Morphological and Biochemical Interconversion of Human Neuroblastoma Cells 2
Ross, R. A., Spengler, B. A., & Biedler, J. L. (1983) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/71.4.741 · Cited by 552 · see citing works
The Evolution of the Brain, the Human Nature of Cortical Circuits, and Intellectual Creativity
DeFelipe, J. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00029 · Cited by 527 · see citing works
Neuregulin and ErbB receptor signaling pathways in the nervous system
Buonanno, A., & Fischbach, G. D. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00210-5 · Cited by 505 · see citing works
Agholme, L., Lindström, T., Kågedal, K., Marcusson, J. O., & Hallbeck, M. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-091363 · Cited by 500 · see citing works
Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia
Corfas, G., Roy, K., & Buxbaum, J. D. (2004) · Nature Neuroscience · doi:10.1038/nn1258 · Cited by 388 · see citing works
Regulation of hippocampal transmitter release during development and long-term potentiation.
Bolshakov, V. Y., & Siegelbaum, S. (1995) · Science · doi:10.1126/science.7569903 · Cited by 385 · see citing works
Cellular and Molecular Mechanisms of Dendrite Growth
McAllister, A. K. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.963 · Cited by 382 · see citing works
Xie, H., Hu, L., & Li, G. (2010) · PubMed · Cited by 371 · see citing works
Dynamic Aspects of CNS Synapse Formation
McAllister, A. K. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112830 · Cited by 368 · see citing works
Neuromodulation by Extracellular ATP and P2X Receptors in the CNS
Khakh, B. S., & North, R. A. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.024 · Cited by 343 · see citing works
Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse
Chavis, P., & Westbrook, G. L. (2001) · Nature · doi:10.1038/35077101 · Cited by 332 · see citing works
Properties of synaptic transmission at single hippocampal synaptic boutons
Liu, G., & Tsien, R. W. (1995) · Nature · doi:10.1038/375404a0 · Cited by 302 · see citing works
Retinoic acid signaling and neuronal differentiation
Janesick, A., Wu, S. C., & Blumberg, B. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1815-9 · Cited by 295 · see citing works
Presgraves, S. P., Ahmed, T., Borwege, S., & Joyce, J. N. (2003) · Neurotoxicity Research · doi:10.1007/bf03033178 · Cited by 293 · see citing works
Morrison, H., Young, K., Qureshi, M., Rowe, R. K., & Lifshitz, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-13581-z · Cited by 276 · see citing works
Metabolic reprogramming during neuronal differentiation
Agostini, M., Romeo, F., Inoue, S., Niklison-Chirou, M. V., Elia, A., Dinsdale, D. D., Morone, N., Knight, R. A., Mak, T. W., & Melino, G. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.36 · Cited by 268 · see citing works
A Comparative View on Human Somatic Cell Sources for iPSC Generation
Raab, S., Klingenstein, M., Liebau, S., & Linta, L. (2014) · Stem Cells International · doi:10.1155/2014/768391 · Cited by 263 · see citing works
de Medeiros, L. M., Bastiani, M. A. D., Rico, E. P., Schönhofen, P., Pfaffenseller, B., Wollenhaupt-Aguiar, B., Grün, L. K., Barbé‐Tuana, F. M., Zimmer, E. R., Castro, M. A. A., et al. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1605-3 · Cited by 247 · see citing works
Arcangeli, A., Bianchi, L. K., Becchetti, A., Faravelli, L., Coronnello, M., Mini, E., Olivotto, M., & Wanke, E. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp021065 · Cited by 240 · see citing works
General Overview of Neuronal Cell Culture
Gordon, J., Amini, S., & White, M. K. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-640-5_1 · Cited by 212 · see citing works
The ethics of experimenting with human brain tissue
Farahany, N. A., Greely, H. T., Hyman, S. E., Christof Koch, A., Grady, C., Pașca, S. P., Šestan, N., Arlotta, P., Bernat, J. L., Ting, J. T., et al. (2018) · Nature · doi:10.1038/d41586-018-04813-x · Cited by 212 · see citing works
Hydrogel‐based three‐dimensional matrix for neural cells
Bellamkonda, R., Ranieri, J. P., Bouche, N., & Aebischer, P. (1995) · Journal of Biomedical Materials Research · doi:10.1002/jbm.820290514 · Cited by 202 · see citing works
Janke, R., Dodson, A. E., & Rine, J. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125544 · Cited by 192 · see citing works
Vitamin D in Neurological Diseases: A Rationale for a Pathogenic Impact
Moretti, R., Morelli, M. E., & Caruso, P. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082245 · Cited by 190 · see citing works
Ethical issues related to brain organoid research
Hyun, I., Scharf-Deering, J. C., & Lunshof, J. E. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146653 · Cited by 186 · see citing works
Dendritic DynamicsIn VivoChange during Neuronal Maturation
Wu, G., Zou, D., Rajan, I., & Cline, H. T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04472.1999 · Cited by 184 · see citing works
Complete morphologies of basal forebrain cholinergic neurons in the mouse
Wu, H., Williams, J., & Nathans, J. (2014) · eLife · doi:10.7554/elife.02444 · Cited by 167 · see citing works
Differentiation and survival influences of growth factors in human neuroblastoma
Påhlman, S., Hoehner, J., Nånberg, E., Hedborg, F., Fagerström, S., Gestblom, C., Johansson, I., Larsson, U., Lavenius, E., Örtoft, E., et al. (1995) · European Journal of Cancer · doi:10.1016/0959-8049(95)00033-f · Cited by 159 · see citing works
Uridine adenosine tetraphosphate: a novel endothelium- derived vasoconstrictive factor
Jankowski, V., Tölle, M., Vanholder, R. C., Schönfelder, G., van der Giet, M., Henning, L., Schlüter, H., Paul, M., Zidek, W., & Jankowski, J. (2005) · Nature Medicine · doi:10.1038/nm1188 · Cited by 153 · see citing works
Esper, R. M., Pankonin, M. S., & Loeb, J. A. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2005.11.006 · Cited by 152 · see citing works
The fate of the brain cholinergic neurons in neurodegenerative diseases
Pepeu, G., & Giovannini, M. G. (2017) · Brain Research · doi:10.1016/j.brainres.2017.06.023 · Cited by 144 · see citing works
The cytoskeleton and neurite initiation
Flynn, K. C. (2013) · BioArchitecture · doi:10.4161/bioa.26259 · Cited by 137 · see citing works
Lozovaya, N., Eftekhari, S., Cloarec, R., Gouty‐Colomer, L., Dufour, A., Riffault, B., Billon-Grand, M., Pons-Bennaceur, A., Oumar, N., Burnashev, N., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03802-y · Cited by 137 · see citing works
Sorting of Dendritic and Axonal Vesicles at the Pre-axonal Exclusion Zone
Farı́as, G. G., Guardia, C. M. A., Britt, D. J., Guo, X., & Bonifacino, J. S. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.074 · Cited by 126 · see citing works
PSD93 Regulates Synaptic Stability at Neuronal Cholinergic Synapses
Parker, M. J., Zhao, S., Bredt, D. S., Sanes, J. R., & Feng, G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3865-03.2004 · Cited by 118 · see citing works
Roles of mitochondria in neuronal development
Son, G., & Han, J. (2018) · BMB Reports · doi:10.5483/bmbrep.2018.51.11.226 · Cited by 117 · see citing works
Fumagalli, M., Lecca, D., Abbracchio, M. P., & Ceruti, S. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00941 · Cited by 116 · see citing works
Neuregulin-1β induces neurite extension and arborization in cultured hippocampal neurons
Gerecke, K. M., Wyss, J. M., & Carroll, S. L. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.08.001 · Cited by 114 · see citing works
Tosetti, P., Taglietti, V., & Toselli, M. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.2.648 · Cited by 110 · see citing works
New Insights Into Cholinergic Neuron Diversity
Ahmed, N. Y., Knowles, R., & Dehorter, N. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00204 · Cited by 108 · see citing works
Drug discovery and development for rare genetic disorders
Sun, W., Zheng, W., & Simeonov, A. (2017) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.38326 · Cited by 107 · see citing works
Ünal, Ç. T., Golowasch, J., & Záborszky, L. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00021 · Cited by 96 · see citing works
Neural Stem Cells and Methods for Their Generation From Induced Pluripotent Stem Cells in vitro
Galiakberova, A. A., & Dashinimaev, E. B. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00815 · Cited by 95 · see citing works
Uracil nucleotides: From metabolic intermediates to neuroprotection and neuroinflammation
Lecca, D., & Ceruti, S. (2008) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.12.009 · Cited by 92 · see citing works
Induced pluripotent stem cells for neural drug discovery
Farkhondeh, A., Li, R., Gorshkov, K., Chen, K. G., Might, M., Rodems, S. M., Lo, D. C., & Zheng, W. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.01.007 · Cited by 90 · see citing works
Dravid, A., Raos, B. J., Svirskis, D. M., & O’Carroll, S. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-03442-1 · Cited by 90 · see citing works
Tonge, P. D., & Andrews, P. W. (2010) · Differentiation · doi:10.1016/j.diff.2010.04.001 · Cited by 85 · see citing works
Nucleotide-sugar transporters: structure, function and roles in vivo
Handford, M. G., Rodríguez-Furlán, C., & Orellana, A. (2006) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2006000900002 · Cited by 83 · see citing works
A Neuron, Microglia, and Astrocyte Triple Co-culture Model to Study Alzheimer’s Disease
Luchena, C., Zuazo-Ibarra, J., Valero, J., Matute, C., Alberdi, E. M., & Capetillo‐Zarate, E. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.844534 · Cited by 82 · see citing works
Karasmanis, E. P., Phan, C.-T., Angelis, D., Kesisova, I. A., Hoogenraad, C. C., McKenney, R. J., & Spiliotis, E. T. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.06.013 · Cited by 81 · see citing works
Martorana, F., Gaglio, D., Bianco, M. R., Aprea, F., Virtuoso, A., Bonanomi, M., Alberghina, L., Papa, M., & Colangelo, A. M. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0429-9 · Cited by 80 · see citing works
TIGAR promotes neural stem cell differentiation through acetyl-CoA-mediated histone acetylation
Zhou, W., Zhao, T., Du, J., Ji, G., Li, X., Ji, S., Tian, W., Wang, X., & Hao, A. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1434-3 · Cited by 76 · see citing works
Knowing a Nascent Synapse When You See It
Ahmari, S. E., & Smith, S. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00685-2 · Cited by 72 · see citing works
A novel method of neural differentiation of PC12 cells by using Opti-MEM as a basic induction medium
Hu, R., Cao, Q., Sun, Z., Chen, J., Zheng, Q., & Xiao, F. (2017) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2017.3195 · Cited by 72 · see citing works
Luchicchi, A., Bloem, B., Viaña, J. N. M., Mansvelder, H. D., & Role, L. W. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00024 · Cited by 70 · see citing works
Rapid Neuromodulation of Layer 1 Interneurons in Human Neocortex
Poorthuis, R. B., Muhammad, K., Wang, M., Verhoog, M. B., Junek, S., Wrana, A., Mansvelder, H. D., & Letzkus, J. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.111 · Cited by 70 · see citing works
Liu, Q., Telezhkin, V., Jiang, W., Gu, Y., Wang, Y., Hong, W., Tian, W., Yarova, P., Zhang, G., Lee, S. M., et al. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-00954-3 · Cited by 70 · see citing works
Hromádková, L., Bezděková, D., Pala, J., Schedin‐Weiss, S., Tjernberg, L. O., Höschl, C., & Ovsepian, S. V. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118737 · Cited by 69 · see citing works
Scheibe, R. J., & Wagner, J. A. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)37086-3 · Cited by 60 · see citing works
Majumder, P., Trujillo, C. A., Lopes, C. G., Resende, R., Gomes, K. N., Yuahasi, K., Britto, L., & Ulrich, H. (2007) · Purinergic Signalling Purinergic Signalling · doi:10.1007/s11302-007-9074-y · Cited by 59 · see citing works
Jakobsson, A., Ottosson, M., Zalis, M. C., O’Carroll, D. C., Johansson, U. E., & Johansson, F. (2017) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2016.12.023 · Cited by 55 · see citing works
Mohrmann, R., Leßmann, V., & Gottmann, K. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00835-7 · Cited by 46 · see citing works
RalGPS2 is involved in tunneling nanotubes formation in 5637 bladder cancer cells
D’Aloia, A., Berruti, G., Costa, B., Schiller, C., Ambrosini, R., Pastori, V., Martegani, E., & Ceriani, M. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.11.036 · Cited by 41 · see citing works
Self-citationMyers, T. A., Nickerson, C. A., Kaushal, D., Ott, C. M., zu Bentrup, K. H., Ramamurthy, R., Nelman-Gonzalez, M. A., Pierson, D. L., & Philipp, M. T. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.06.031 · Cited by 39 · see citing works
Blackshaw, S. E., ARKISON, S., Cameron, C., & Davies, J. A. (1997) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1997.0093 · Cited by 39 · see citing works
Campioni, G., Pasquale, V., Busti, S., Ducci, G., Sacco, E., & Vanoni, M. (2022) · Cells · doi:10.3390/cells11050866 · Cited by 35 · see citing works
Self-citationFunctional Properties of Human Stem Cell‐Derived Neurons in Health and Disease
Weick, J. P. (2016) · Stem Cells International · doi:10.1155/2016/4190438 · Cited by 33 · see citing works
D’Aloia, A., Arrigoni, E., Costa, B., Berruti, G., Martegani, E., Sacco, E., & Ceriani, M. (2021) · Cancers · doi:10.3390/cancers13246330 · Cited by 33 · see citing works
Self-citationJeong, J. H., Woo, Y. J., Chua, S. C., & Jo, Y. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162839 · Cited by 31 · see citing works
D’Aloia, A., Ceriani, M., Tisi, R., Stucchi, S., Sacco, E., & Costa, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137145 · Cited by 29 · see citing works
Self-citationYang, J., Lin, Y.-T., Chen, W., Yang, Y., Sun, S., & Chen, S. (2020) · Biology · doi:10.3390/biology9110348 · Cited by 28 · see citing works
Nuclear Choline Acetyltransferase Activates Transcription of a High-affinity Choline Transporter
Matsuo, A., Bellier, J., Nishimura, M., Yasuhara, O., Saito, N., & Kimurâ, H. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.147611 · Cited by 28 · see citing works
Pansri, P., Phanthong, P., Suthprasertporn, N., Kitiyanant, Y., Tubsuwan, A., Dinnyés, A., Kobolák, J., & Kitiyanant, N. (2021) · PeerJ · doi:10.7717/peerj.11388 · Cited by 28 · see citing works
Pasquale, V., Ducci, G., Campioni, G., Ventrici, A., Assalini, C., Busti, S., Vanoni, M., Vago, R., & Sacco, E. (2020) · Cells · doi:10.3390/cells9122669 · Cited by 24 · see citing works
Self-citationBaksa, B., Kovács, A., Bayasgalan, T., Szentesi, P., Kőszeghy, Á., Szűcs, P., & Pál, B. Z. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03025-4 · Cited by 23 · see citing works
Halliwell, R. F., Salmanzadeh, H., Coyne, L., & Cao, W. (2021) · Cells · doi:10.3390/cells10081953 · Cited by 22 · see citing works
Li, Z.-F., Cui, L., Jin, M.-M., Hu, D., Hou, X.-G., Liu, S.-S., Zhang, X., & Zhu, J. (2022) · Disease Models & Mechanisms · doi:10.1242/dmm.049125 · Cited by 17 · see citing works
Properties of differentiated SH-SY5Y grown on carbon-based materials
Yoon, S., Lee, G., Park, S. B., Cho, H., Lee, J.-O., & Koh, B. (2020) · RSC Advances · doi:10.1039/d0ra03383a · Cited by 16 · see citing works
Quantitative Characterization of Phenotypical Markers After Differentiation of SH-SY5Y Cells
Ducray, A., Wiedmer, L., Herren, F. L., Widmer, H. R., & Mevissen, M. (2020) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527319666200708132716 · Cited by 14 · see citing works
Changes in Biophysical Properties of Undifferentiated SH-SY5Y Cells During Long-term Cultures
Santillo, S. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.10.033 · Cited by 14 · see citing works
Extracellular matrix effects on a neuroblastoma cell line.
Hahn, M., Glass, T. L., & Koke, J. R. (2000) · PubMed · Cited by 11 · see citing works
Neuroblastoma SH-SY5Y Cell Differentiation to Mature Neuron by AM580 Treatment
Cai, A., Lin, Z., Liu, N., Li, X., Wang, J., Wu, Y., Gao, K., & Jiang, Y. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03730-w · Cited by 9 · see citing works
Douida, A., Batista, F., Botó, P., Regdon, Z., Robaszkiewicz, A., & Tar, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041629 · Cited by 6 · see citing works
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Chapter 7 Cerebral changes in alzheimer's disease
Plum, F. (1986) · Progress in brain research · doi:10.1016/s0079-6123(08)64602-6 · Cited by 3 · see citing works
Goodrum (2000) · doi:10.1002/(sici)1097-4547(20000215)59:4
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Shademan, B., Yousefi, H., Sharafkhani, R., & Nourazarian, A. (2025) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-025-01600-x · Cited by 9 · see citing works
Wang, J., Brückner, N., Weissmann, S., Günther, T., Zhu, S., Vogt, C., Sun, G., Guo, R., Bruno, R., Ritter, B., et al. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1012367 · Cited by 8 · see citing works
Ding, X.-S., Wang, B., Han, Z., Feng, C., Li, Y.-N., Wang, Y., Guru, J.-C., Cao, J., Zhang, R.-L., Wang, X., et al. (2026) · Redox Biology · doi:10.1016/j.redox.2026.104030 · Cited by 7 · see citing works
Nafie, M. S., Alshams, M. A., Diab, M. K., Ashour, H. F., & Yassen, A. S. A. (2025) · Chemical Biology & Drug Design · doi:10.1111/cbdd.70173 · Cited by 6 · see citing works
Kulatunga, D. C. M., Ranaraja, U., Kim, E. Y., Kim, R. E., Kim, D. E., Ji, K. B., & Kim, M. K. (2024) · Scientific Reports · doi:10.1038/s41598-024-63005-y · Cited by 6 · see citing works
Vigier, M., Uriot, M., Djelti-Delbarba, F., Claudepierre, T., Hajj, A. E., Yen, F. T., Oster, T., & Malaplate, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25136816 · Cited by 6 · see citing works
Ghani, M., Peleg, Z., Ujlaki, G., Tóth, M. E., Amsalu, H., Póliska, S., & Tar, K. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1342741 · Cited by 6 · see citing works
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Torresan, V., Dedroog, L., Deschaume, O., Koos, E., Lettinga, M. P., Gandin, A., Pelosin, M., Zanconato, F., Brusatin, G., & Bartic, C. (2024) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2024.122901 · Cited by 5 · see citing works
Brandalise, F., Priori, E. C., Giammello, F., Venuti, M., Ratto, D., Goppa, L., Locatelli, C., Savino, E., Roda, E., & Rossi, P. (2025) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2025.118204 · Cited by 4 · see citing works
Matrella, M. L., Valletti, A., Gigante, I., Rasmo, D. D., Signorile, A., Russo, S., Lobasso, S., Lobraico, D., Dibattista, M., Pacelli, C., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-57613-x · Cited by 4 · see citing works
Ferdous, J., Naitou, K., & Shiraishi, M. (2024) · Biological Trace Element Research · doi:10.1007/s12011-024-04342-x · Cited by 4 · see citing works
Murphy, R., Villegas-Salmerón, J., Sanz-Rodriguez, A., Engel, T., Mooney, C., Henshall, D. C., & Jimenez-Mateos, E. M. (2025) · PLOS One · doi:10.1371/journal.pone.0326401 · Cited by 3 · see citing works
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Tang, X.-Q., & Bowman, A. B. (2024) · Advances in neurotoxicology · doi:10.1016/bs.ant.2024.07.004 · Cited by 1 · see citing works
Daou, B., Prato, M., Alonso‐Martín, S., & Alegret, N. (2025) · Small Science · doi:10.1002/smsc.202500401 · Cited by 1 · see citing works
Zainuddin, M.-S., Magalingam, K. B., Pamidi, N., Azman, A. S., & Bhuvanendran, S. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-12156-4 · Cited by 2 · see citing works
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Wang, X., Qu, K., Wang, Z., Wang, Z., & Jia, B. (2025) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2025.102838
Dardalas, I., Kosmidis, E. K., Kimiskidis, V. Κ., Lagoudaki, R., Samaras, T., Moysiadis, T., Kouvelas, D., & Pourzitaki, C. (2025) · Neurology International · doi:10.3390/neurolint17100152
Fathallah, S., & Abdellatif, A. (2025) · Clinical Phytoscience · doi:10.1186/s40816-025-00407-z
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Almeida, I., Martins, F., Goodfellow, B. J., Rebelo, S., & Nunes, A. (2026) · Analytical Biochemistry · doi:10.1016/j.ab.2026.116139 · Cited by 1 · see citing works
Li, Y., Wang, T., Liu, H., Zhang, N., & Zhang, Z. (2026) · Processes · doi:10.3390/pr14091481
Alexander, S., John, P., & Zam, A. (2026) · IEEE International Symposium on Biomedical Imaging (ISBI) · doi:10.1109/isbi61048.2026.11515326
Czaniera, N. J., Schulten, W., Nowak, K., Pschik, D., Joneleit, J., Kaltschmidt, B., & Kaltschmidt, C. (2026) · Cells · doi:10.3390/cells15121057
Meerman, J. J., Sinnige, T. L., Klerx, W. N. M., Tuominen, A., Legler, J., Piersma, A. H., Heusinkveld, H. J., & Westerink, R. H. S. (2026) · Toxicology · doi:10.1016/j.tox.2026.154526
Lin, L., Yan, W., Zhang, E., Xu, W., Sui, X., Zheng, H., Xiao, T., & Ni, C. (2026) · Tissue and Cell · doi:10.1016/j.tice.2026.103891
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- Authors
- D’Aloia, A., Pastori, V., Blasa, S., Campioni, G., Peri, F., Sacco, E., Ceriani, M., Lecchi, M., & Costa, B.
- Affiliations
- University of Milano-Bicocca (IT)
- University of Pisa (IT)
- Corresponding author
- D’Aloia, Alessia
- ORCID
- Venue
- Cell Death Discovery
- Published
- 2024-01-12
- Volume
- 10
- Issue
- 1
- Pages
- 24-24
- ISSN
- 2058-7716 (ISSN-L)
- PMC
- PMC10786877
- OpenAlex
- W4390796340
- Cited by
- 36
- References
- 100
- Citations by year
- 2026: 14 · 2025: 12 · 2024: 10
- FWCI
- 6.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Cell Death Discovery (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Fondazione Umberto Veronesi (5186)
- Ministero dello Sviluppo Economico (PoC 2020)
- Ministero dell'Istruzione, dell'Università e della Ricerca (M4C2-I1.3 Project PE_00000019, 2019-ATE-0145, 2018-ATE-0117, 2017-ATE-0606)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- cholinergic neurons, SH-SY5Y cells, neuroblastoma cell differentiation, 3D neuronal culture, neuronal reprogramming, neuronal networks, neuronal maturation, vesicle trafficking, synaptic function, neuronal migration, disease modeling
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