α-synuclein transfer through tunneling nanotubes occurs in SH-SY5Y cells and primary brain pericytes from Parkinson’s disease patients
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Parkinson’s disease (PD) is characterized by the presence of inclusions known as Lewy bodies, which mainly consist of α-synuclein (α-syn) aggregates. There is growing evidence that α-syn self-propagates in non-neuronal cells, thereby contributing to the progression and spread of PD pathology in the brain. Tunneling nanotubes (TNTs) are long, thin, F-actin-based membranous channels that connect cells and have been proposed to act as conduits for α-syn transfer between cells. SH-SY5Y cells and primary human brain pericytes, derived from postmortem PD brains, frequently form TNTs that allow α-syn transfer and long-distance electrical coupling between cells. Pericytes in situ contain α-syn precipitates like those seen in neurons. Exchange through TNTs was rapid, but dependent on the size of the protein. Proteins were able to spread throughout a network of cells connected by TNTs. Transfer through TNTs was not restricted to α-syn; fluorescent control proteins and labeled membrane were also exchanged through TNTs. Most importantly the formation of TNTs and transfer continued during mitosis. Together, our results provide a detailed description of TNTs in SH-SY5Y cells and human brain PD pericytes, demonstrating their role in α-syn transfer and further emphasize the importance that non-neuronal cells, such as pericytes play in disease progression.
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αSyn has the ability to spread via direct neuron-to-neuron transfer.
“iii) αSyn has the ability to spread to adjacent cells via secretion in exosomes [209], uptake via endocytosis [210] and cell-surface receptors like HSPGs, or even direct neuron-to-neuron [211, 212] or astrocyte-to-neuron [213] transfer via tunneling nanotubes (Fig. 2).”
From α-synuclein in the pathophysiology of Alzheimer’s disease (2019) · cites this paper as [212]
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1 retracted
RETRACTED ARTICLE: Pericyte loss influences Alzheimer-like neurodegeneration in mice
Sagare, A. P., Bell, R. D., Zhao, Z., Ma, Q., Winkler, E. A., Ramanathan, A., & Zlokovic, B. V. (2013) · Nature Communications · doi:10.1038/ncomms3932 · Cited by 589 · see citing works
RetractedThe 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
Nanotubular Highways for Intercellular Organelle Transport
Rustom, A., Saffrich, R., Markovic, I., Walther, P., & Gerdes, H.-H. (2004) · Science · doi:10.1126/science.1093133 · Cited by 2,038 · see citing works
Li, J.-Y., Englund, E., Holton, J. L., Soulet, D., Hagell, P., Lees, A. J., Lashley, T., Quinn, N. P., Rehncrona, S., Björklund, A., et al. (2008) · Nature Medicine · doi:10.1038/nm1746 · Cited by 1,845 · see citing works
Lewy body–like pathology in long-term embryonic nigral transplants in Parkinson's disease
Kordower, J. H., Chu, Y., Hauser, R. A., Freeman, T. B., & Olanow, C. W. (2008) · Nature Medicine · doi:10.1038/nm1747 · Cited by 1,722 · see citing works
Brain tumour cells interconnect to a functional and resistant network
Osswald, M., Jung, E., Sahm, F., Solecki, G. M., Venkataramani, V., Blaes, J., Heuer, S., Horstmann, H., Wiestler, B., Syed, M., et al. (2015) · Nature · doi:10.1038/nature16071 · Cited by 1,140 · see citing works
Exosomal cell-to-cell transmission of alpha synuclein oligomers
Danzer, K. M., Kranich, L. R., Ruf, W. P., Cagsal‐Getkin, O., Winslow, A. R., Zhu, L., Vanderburg, C. R., & McLean, P. J. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-42 · Cited by 853 · see citing works
Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission
Alvarez‐Erviti, L., Seow, Y., Schapira, A. H. V., Gardiner, C., Sargent, I. L., Wood, M. J. A., & Cooper, J. A. D. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.01.029 · Cited by 741 · see citing works
Prions hijack tunnelling nanotubes for intercellular spread
Gousset, K., Schiff, E., Langevin, C., Marijanovic, Z., Caputo, A., Browman, D., Chenouard, N., de Chaumont, F., Martino, A., Enninga, J., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1841 · Cited by 616 · see citing works
α-Synuclein: Membrane Interactions and Toxicity in Parkinson's Disease
Auluck, P. K., Caraveo, G., & Lindquist, S. L. (2010) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.042308.113313 · Cited by 516 · see citing works
Önfelt, B., Nedvetzki, S., Benninger, R. K. P., Purbhoo, M. A., Sowinski, S., Hume, A. N., Seabra, M. C., Neil, M. A. A., French, P. M. W., & Davis, D. M. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.12.8476 · Cited by 492 · see citing works
Size Limit of Molecules Permeating the Junctional Membrane Channels
Simpson, I. A., Rose, B., & Loewenstein, W. R. (1977) · Science · doi:10.1126/science.831276 · Cited by 421 · see citing works
Lou, E., Fujisawa, S., Morozov, A., Barlas, A., Romin, Y., Dogan, Y., Gholami, S., Moreira, A. L., Manova-Todorova, K., & Moore, M. A. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033093 · Cited by 420 · see citing works
Tunneling nanotubes spread fibrillar α-synuclein by intercellular trafficking of lysosomes
Abounit, S., Bousset, L., Loria, F., Zhu, S., de Chaumont, F., Pieri, L., Olivo‐Marin, J., Melki, R., & Zurzolo, C. (2016) · The EMBO Journal · doi:10.15252/embj.201593411 · Cited by 414 · see citing works
Global changes in DNA methylation and hydroxymethylation in Alzheimer's disease human brain
Coppieters, N., Dieriks, B. V., Lill, C. L., Faull, R. L. M., Curtis, M. A., & Dragunow, M. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.11.031 · Cited by 350 · see citing works
Self-citationCutting Edge: Membrane Nanotubes In Vivo: A Feature of MHC Class II+ Cells in the Mouse Cornea
Chinnery, H. R., Pearlman, E. M., & McMenamin, P. G. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.9.5779 · Cited by 278 · see citing works
Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo
Angot, E., Steiner, J. A., Lema Tomé, C. M., Ekström, P., Mattsson, B., Björklund, A., & Brundin, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039465 · Cited by 270 · see citing works
Austefjord, M. W., Gerdes, H., & Wang, X. (2014) · Communicative & Integrative Biology · doi:10.4161/cib.27934 · Cited by 236 · see citing works
Neuropathological basis of nonmotor manifestations of Parkinson's disease
Adler, C. H., & Beach, T. G. (2016) · Movement Disorders · doi:10.1002/mds.26605 · Cited by 230 · see citing works
Alpha synuclein is transported into and out of the brain by the blood-brain barrier
Sui, Y.-T., Bullock, K. M., Erickson, M. A., Zhang, J., & Banks, W. A. (2014) · Peptides · doi:10.1016/j.peptides.2014.09.018 · Cited by 212 · see citing works
Immunohistochemical staining of post-mortem adult human brain sections
Waldvogel, H. J., Curtis, M. A., Baer, K., Rees, M. I., & Faull, R. L. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.354 · Cited by 211 · see citing works
Self-citationTransfer of polyglutamine aggregates in neuronal cells occurs in tunneling nanotubes
Costanzo, M., Abounit, S., Marzo, L., Danckaert, A., Chamoun, Z., Roux, P., & Zurzolo, C. (2013) · Journal of Cell Science · doi:10.1242/jcs.126086 · Cited by 210 · see citing works
A longitudinal study on α-synuclein in blood plasma as a biomarker for Parkinson's disease
Foulds, P. G., Diggle, P. J., Mitchell, J. D., Parker, A., Hasegawa, M., Masuda‐Suzukake, M., Mann, D. M. A., & Allsop, D. (2013) · Scientific Reports · doi:10.1038/srep02540 · Cited by 186 · see citing works
Ding, X., Ma, M., Teng, J., Teng, R. K. F., Zhou, S. Y., Yin, J., Fonkem, E., Huang, J. H., Wu, E., & Wang, X. (2015) · Oncotarget · doi:10.18632/oncotarget.4680 · Cited by 177 · see citing works
A role for human brain pericytes in neuroinflammation
Jansson, D., Rustenhoven, J., Feng, S. X., Hurley, D., Oldfield, R. L., Bergin, P., Mee, E. W., Faull, R. L. M., & Dragunow, M. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-104 · Cited by 168 · see citing works
Self-citationDynamics of α‐synuclein aggregation and inhibition of pore‐like oligomer development by β‐synuclein
Tsigelny, I. F., Bar‐On, P., Sharikov, Y., Crews, L. A., Hashimoto, M., Miller, M. A., Keller, S. H., Platoshyn, O., Yuan, J. X. ‐., & Masliah, E. (2007) · FEBS Journal · doi:10.1111/j.1742-4658.2007.05733.x · Cited by 163 · see citing works
Amino acid sequence motifs and mechanistic features of the membrane translocation of α‐synuclein
Ahn, K. J., Paik, S. R., Chung, K. C., & Kim, J. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03731.x · Cited by 123 · see citing works
Konno, M., Hasegawa, T., Baba, T., Miura, E., Sugeno, N., Kikuchi, A., Fiesel, F. C., Sasaki, T., Aoki, M., Itoyama, Y., et al. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-38 · Cited by 119 · see citing works
Exosomes and nanotubes: Control of immune cell communication
McCoy-Simandle, K., Hanna, S. J., & Cox, D. (2015) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2015.12.006 · Cited by 113 · see citing works
Angot, É., & Brundin, P. (2009) · Parkinsonism & Related Disorders · doi:10.1016/s1353-8020(09)70802-8 · Cited by 101 · see citing works
α-Synuclein overexpression promotes aggregation of mutant huntingtin
Furlong, R. A., Narain, Y., Rankin, J., Wyttenbach, A., & Rubinsztein, D. C. (2000) · Biochemical Journal · doi:10.1042/bj3460577 · Cited by 86 · see citing works
Feng, L., Federoff, H. J., Vicini, S., & Maguire‐Zeiss, K. A. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07266.x · Cited by 70 · see citing works
Friedman, P. L., & Ellisman, M. H. (1981) · Journal of Neurocytology · doi:10.1007/bf01181748 · Cited by 57 · see citing works
An anti-inflammatory role for C/EBPδ in human brain pericytes
Rustenhoven, J., Scotter, E. L., Jansson, D., Kho, D. T., Oldfield, R. L., Bergin, P., Mee, E. W., Faull, R. L. M., Curtis, M. A., Graham, S. E., et al. (2015) · Scientific Reports · doi:10.1038/srep12132 · Cited by 52 · see citing works
Self-citationEugenin, E., Gaskill, P., & Berman, J. (2009) · Communicative & Integrative Biology · doi:10.4161/cib.2.3.8165 · Cited by 33 · see citing works
Sorting out the cell biology of Alzheimer’s disease: focus on BACE1 and APP
Annaert, W. G. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-s1-l6 · Cited by 10 · see citing works
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Peng, C., Trojanowski, J. Q., & Lee, V. M.-Y. (2020) · Nature Reviews Neurology · doi:10.1038/s41582-020-0333-7 · Cited by 625 · see citing works
α-synuclein in the pathophysiology of Alzheimer’s disease
Twohig, D., & Nielsen, H. M. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0320-x · Cited by 374 · see citing works
Scheiblich, H., Dansokho, C., Mercan, D., Schmidt, S. V., Bousset, L., Wischhof, L., Eikens, F., Odainic, A., Spitzer, J., Griep, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.09.007 · Cited by 360 · see citing works
Functional Mitochondria in Health and Disease
Herst, P. M., Rowe, M. R., Carson, G. M., & Berridge, M. V. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00296 · Cited by 324 · see citing works
Correlative cryo-electron microscopy reveals the structure of TNTs in neuronal cells
Sartori-Rupp, A., Cervantes, D. C., Pepe, A., Gousset, K., Delage, E., Corroyer-Dulmont, S., Schmitt, C., Locker, J. K., & Zurzolo, C. (2019) · Nature Communications · doi:10.1038/s41467-018-08178-7 · Cited by 272 · see citing works
Scheiblich, H., Eikens, F., Wischhof, L., Opitz, S., Jüngling, K., Cserép, C., Schmidt, S. V., Lambertz, J., Bellande, T., Pósfai, B., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.06.029 · Cited by 207 · see citing works
Chakraborty, R., Nonaka, T., Hasegawa, M., & Zurzolo, C. (2023) · Cell Death & Disease · doi:10.1038/s41419-023-05835-8 · Cited by 190 · see citing works
Tunneling nanotubes: Reshaping connectivity
Zurzolo, C. (2021) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2021.03.003 · Cited by 187 · see citing works
Sorrentino, Z. A., Giasson, B. I., & Chakrabarty, P. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-01977-2 · Cited by 181 · see citing works
Peering into tunneling nanotubes—The path forward
Cervantes, D. C., & Zurzolo, C. (2021) · EMBO Journal · doi:10.15252/embj.2020105789 · Cited by 146 · see citing works
Magalhães, P., & Lashuel, H. A. (2022) · npj Parkinson s Disease · doi:10.1038/s41531-022-00357-0 · Cited by 157 · see citing works
Mechanisms of protein toxicity in neurodegenerative diseases
Chung, C. G., Lee, H., & Lee, S. B. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2854-4 · Cited by 142 · see citing works
Lin, K.-J., Lin, K.-L., Chen, S., Liou, C., Chuang, Y., Lin, H., & Lin, T. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20215312 · Cited by 141 · see citing works
Dilsizoglu Senol, A., Samarani, M., Syan, S., Guardia, C. M., Nonaka, T., Liv, N., Latour-Lambert, P., Hasegawa, M., Klumperman, J., Bonifacino, J. S., et al. (2021) · PLOS Biology · doi:10.1371/journal.pbio.3001287 · Cited by 134 · see citing works
Peelaerts, W., Bousset, L., Baekelandt, V., & Melki, R. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2839-5 · Cited by 121 · see citing works
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Vargas, J., Loría, F., Wu, Y.-J., Córdova, G., Nonaka, T., Bellow, S., Syan, S., Hasegawa, M., van Woerden, G. M., Trollet, C., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2018101230 · Cited by 126 · see citing works
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Nawaz, M., & Fatima, F. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00050 · Cited by 123 · see citing works
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Cascella, R., Bigi, A., Cremades, N., & Cecchi, C. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04166-9 · Cited by 125 · see citing works
Spreading of α-Synuclein and Tau: A Systematic Comparison of the Mechanisms Involved
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Dohgu, S., Takata, F., Matsumoto, J., Kimura, I., Yamauchi, A., & Kataoka, Y. (2019) · Microvascular Research · doi:10.1016/j.mvr.2019.03.005 · Cited by 112 · see citing works
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Vargas, J., Grudina, C., & Zurzolo, C. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.01.012 · Cited by 106 · see citing works
Cell communication by tunneling nanotubes: Implications in disease and therapeutic applications
Mittal, R., Karhu, E., Wang, J., Delgado, S., Zukerman, R. J., Mittal, J., & Jhaveri, V. M. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27072 · Cited by 107 · see citing works
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Yamashita, Y. M., Inaba, M., & Buszczak, M. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062932 · Cited by 105 · see citing works
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Menon, S. A., Armstrong, S. E. M., Hamzeh, A. M., Visanji, N. P., Sardi, S. P., & Tandon, A. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.852003 · Cited by 107 · see citing works
Sensitivity and specificity of phospho‐Ser129 α‐synuclein monoclonal antibodies
Delic, V., Chandra, S., Abdelmotilib, H., Maltbie, T., Wang, S., Kem, D., Scott, H. J., Underwood, R. N., Liu, Z., Volpicelli‐Daley, L. A., et al. (2018) · Journal of Comparative Neurology · doi:10.1002/cne.24468 · Cited by 95 · see citing works
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Rodriguez, L., Marano, M. M., & Tandon, A. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00344 · Cited by 93 · see citing works
Pathogenesis of α-Synuclein in Parkinson’s Disease: From a Neuron-Glia Crosstalk Perspective
Yi, S., Wang, L., Wang, H., Ho, M. S.-C., & Zhang, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232314753 · Cited by 90 · see citing works
Wu, Y., Bogale, T. A., Koıstınaho, J., Pizzi, M., Rõlova, T., & Bellucci, A. (2024) · Acta Neuropathologica · doi:10.1007/s00401-024-02696-z · Cited by 81 · see citing works
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Wiseman, J. A., Murray, H. C., Faull, R. L. M., Dragunow, M., Turner, C. P., Dieriks, B. V., & Curtis, M. A. (2024) · npj Parkinson s Disease · doi:10.1038/s41531-023-00614-w · Cited by 72 · see citing works
Self-citationStevenson, T. J., Murray, H. C., Turner, C. P., Faull, R. L. M., Dieriks, B. V., & Curtis, M. A. (2020) · Scientific Reports · doi:10.1038/s41598-020-63412-x · Cited by 70 · see citing works
Self-citationAltered microglia and neurovasculature in the Alzheimer's disease cerebellum
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Self-citationXu, K., Qiu, J., Li, Q., Bell, K. A., Du, Y., Jung, D. W., Lee, J. Y., Hao, J., & Jiang, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-09528-z · Cited by 69 · see citing works
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Bogale, T. A., Faustini, G., Longhena, F., Mitola, S. M. F., Pizzi, M., & Bellucci, A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.611761 · Cited by 59 · see citing works
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Huang, J. A., Ding, J., Wang, X., Gu, C., He, Y., Li, Y., Fan, H., Xie, Q., Qi, X., Wang, Z., et al. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.09.002 · Cited by 56 · see citing works
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Tavassoly, O., Yue, J., & Vocadlo, D. J. (2020) · FEBS Journal · doi:10.1111/febs.15349 · Cited by 52 · see citing works
Dilna, A., Deepak, K. V., Damodaran, N., Kielkopf, C. S., Kagedal, K., Ollinger, K., & Nath, S. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166246 · Cited by 51 · see citing works
Kuo, G., Kumbhar, R., Blair, W., Dawson, V. L., Dawson, T. M., & Mao, X. (2025) · Molecular Neurodegeneration · doi:10.1186/s13024-025-00797-1 · Cited by 52 · see citing works
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Han, X., & Wang, X. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052306 · Cited by 45 · see citing works
Alpha-synuclein and the prion hypothesis in Parkinson's disease
Melki, R. (2018) · Revue Neurologique · doi:10.1016/j.neurol.2018.08.002 · Cited by 45 · see citing works
Lin, C., Nicol, C. J. B., Cheng, Y., Yen, C., Wang, Y., & Chiang, M. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146492 · Cited by 45 · see citing works
Tunneling Nanotubes Facilitate Intercellular Protein Transfer and Cell Networks Function
Turos-Korgul, L., Kolba, M. D., Chrościcki, P., Zieminska, A., & Piwocka, K. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.915117 · Cited by 44 · see citing works
Tunneling Nanotubes: A New Target for Nanomedicine?
Ottonelli, I., Caraffi, R., Tosi, G., Vandelli, M. A., Duskey, J. T., & Ruozi, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23042237 · Cited by 43 · see citing works
Rab35 and its effectors promote formation of tunneling nanotubes in neuronal cells
Bhat, S., Ljubojević, N., Zhu, S., Fukuda, M., Echard, A., & Zurzolo, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-74013-z · Cited by 36 · see citing works
Enteroendocrine cells: the gatekeepers of microbiome-gut-brain communication
Grundeken, E., & Aidy, S. E. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00810-x · Cited by 41 · see citing works
Sepúlveda, D., Cisternas-Olmedo, M., Arcos, J., Nassif, M., & Vidal, R. L. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.805087 · Cited by 40 · see citing works
Palese, F., Rakotobé, M., & Zurzolo, C. (2025) · Physiological Reviews · doi:10.1152/physrev.00023.2024 · Cited by 40 · see citing works
Selective Neuronal Death in Neurodegenerative Diseases: The Ongoing Mystery.
Subramaniam, S. (2019) · Europe PMC (PubMed Central) · Cited by 40 · see citing works
Raghavan, A., Rao, P., Neužil, J., Pountney, D. L., & Nath, S. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-04040-0 · Cited by 38 · see citing works
Alpha-Synuclein Aggregates Associated with Mitochondria in Tunnelling Nanotubes
Valdinocci, D., Kovářová, J., Neužil, J., & Pountney, D. L. (2020) · Neurotoxicity Research · doi:10.1007/s12640-020-00285-y · Cited by 38 · see citing works
Amro, Z., Yool, A. J., & Collins‐Praino, L. E. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100242 · Cited by 37 · see citing works
Khor, S. L. Q., Ng, K. Y., Koh, R. Y., & Chye, S. M. (2023) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527322666230330093829 · Cited by 35 · see citing works
Huntington, T. E., & Srinivasan, R. (2021) · Aging and disease · doi:10.14336/ad.2021.0517 · Cited by 34 · see citing works
Lin, D., Liang, Y., Jing, X., Chen, Y., Lei, M., Zeng, Z., Zhou, T., Wu, X., Peng, S., Zheng, D., et al. (2017) · Brain Research · doi:10.1016/j.brainres.2017.11.007 · Cited by 33 · see citing works
Li, D., Huang, L., Zhang, C.-P., Li, Q., & Wang, J. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.890509 · Cited by 34 · see citing works
Pericytes take up and degrade α-synuclein but succumb to apoptosis under cellular stress
Stevenson, T. J., Johnson, R. H., Savistchenko, J., Rustenhoven, J., Woolf, Z., Smyth, L. C. D., Murray, H. C., Faull, R. L. M., Correia, J. A., Schweder, P. M., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-20261-0 · Cited by 33 · see citing works
Self-citationThe Nigral Coup in Parkinson’s Disease by α-Synuclein and Its Associated Rebels
Sian‐Hülsmann, J., & Riederer, P. F. (2021) · Cells · doi:10.3390/cells10030598 · Cited by 30 · see citing works
The Role of Glial Mitochondria in α-Synuclein Toxicity
Jeon, Y., Kwon, Y., Jo, M., Lee, S., Kim, S., & Kim, H. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.548283 · Cited by 31 · see citing works
Membrane Trafficking Illuminates a Path to Parkinson’s Disease
Hasegawa, T., Sugeno, N., Kikuchi, A., Baba, T., & Aoki, M. (2017) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.242.63 · Cited by 28 · see citing works
Role of cellular prion protein in interneuronal amyloid transmission
del Rı́o, J. A., Ferrer, I., & Gavı́n, R. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.03.001 · Cited by 28 · see citing works
Mahadik, P., & Patwardhan, S. (2023) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2023.109624 · Cited by 27 · see citing works
Tavassoly, O., del Cid‐Pellitero, E., Larroquette, F., Cai, E., Thomas, R. A., Soubannier, V., Luo, W., Durcan, T. M., & Fon, E. A. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01017-6 · Cited by 26 · see citing works
Prion-like properties of disease-relevant proteins in amyotrophic lateral sclerosis
Bräuer, S., Zimyanin, V. L., & Hermann, A. (2018) · Journal of Neural Transmission · doi:10.1007/s00702-018-1851-y · Cited by 27 · see citing works
Carta, A. R., Boi, L., Pisanu, A., Palmas, M. F., Carboni, E., & Simone, A. D. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108685 · Cited by 25 · see citing works
Tunneling Nanotube: An Enticing Cell–Cell Communication in the Nervous System
Dagar, S., & Subramaniam, S. (2023) · Biology · doi:10.3390/biology12101288 · Cited by 24 · see citing works
Raghavan, A., Kashyap, R., Sreedevi, P. R., Jos, S., Chatterjee, S., Alex, A., D’Souza, M. N., Giridharan, M., Muddashetty, R. S., Manjithaya, R. R., et al. (2024) · iScience · doi:10.1016/j.isci.2024.110565 · Cited by 23 · see citing works
Intercellular transmission of alpha-synuclein
Wu, S., & Schekman, R. W. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1470171 · Cited by 24 · see citing works
Duan, Q., Zhang, Q., Nie, K., Huang, R., Yang, J., He, P., Tie, Z., Huang, H., Ma, G., Zhang, Y., et al. (2023) · iScience · doi:10.1016/j.isci.2023.107458 · Cited by 23 · see citing works
Mural Cells: Potential Therapeutic Targets to Bridge Cardiovascular Disease and Neurodegeneration
Lin, A., Peiris, N. J., Dhaliwal, H., Hakim, M., Li, W., Ganesh, S., Ramaswamy, Y., Patel, S., & Misra, A. (2021) · Cells · doi:10.3390/cells10030593 · Cited by 23 · see citing works
Tunneling nanotubes: A novel pharmacological target for neurodegenerative diseases?
Wang, X.-T., Sun, H., Chen, N.-H., & Yuan, Y.-H. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105541 · Cited by 22 · see citing works
α-Synuclein at the Presynaptic Axon Terminal as a Double-Edged Sword
Tan, L. Y., Tang, K. H., Lim, L. Y. Y., Ong, J. X., Park, H., & Jung, S. (2022) · Biomolecules · doi:10.3390/biom12040507 · Cited by 22 · see citing works
Epothilone D inhibits microglia-mediated spread of alpha-synuclein aggregates
Valdinocci, D., Grant, G. D., Dickson, T. C., & Pountney, D. L. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.04.006 · Cited by 20 · see citing works
Kempf, S., Popp, R., Naeem, Z., Frömel, T., Wittig, I., Klatt, S., & Fleming, I. (2024) · Cells · doi:10.3390/cells13171429 · Cited by 20 · see citing works
Human pericytes degrade diverse α-synuclein aggregates
Dieriks, B. V., Highet, B., Alik, A., Bellande, T., Stevenson, T. J., Low, V. F., Park, T., Correia, J. A., Schweder, P. M., Faull, R. L. M., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0277658 · Cited by 20 · see citing works
Self-citationThe role of the endolysosomal pathway in α-synuclein pathogenesis in Parkinson’s disease
Smith, J. K., Mellick, G. D., & Sykes, A. M. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1081426 · Cited by 20 · see citing works
Mechanisms of tunneling nanotube-based propagation of neurodegenerative disease proteins
Lagalwar, S. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.957067 · Cited by 19 · see citing works
Tang, B. L. (2017) · Reviews in the Neurosciences · doi:10.1515/revneuro-2017-0018 · Cited by 19 · see citing works
Fayyad, M., Majbour, N. K., Vaikath, N. N., Erskine, D., Heba, E.-T., Sudhakaran, I. P., Abdesselem, H., & El‐Agnaf, O. M. A. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.134899 · Cited by 18 · see citing works
Jiang, D., Xu, W., Peng, F., Sun, Y., Pan, C., Yu, J., Zheng, Q., & Chen, W. (2023) · Experimental Eye Research · doi:10.1016/j.exer.2023.109497 · Cited by 17 · see citing works
Zheng, H., Shi, C., Luo, H., Fan, L., Yang, Z., Hu, X., Zhang, Z., Zhang, S., Hu, Z., Fan, Y., et al. (2020) · The Neuroscientist · doi:10.1177/1073858420943180 · Cited by 16 · see citing works
Prion-like propagation of α-synuclein in the gut-brain axis
Chen, Y., Shao, Q.-H., Yuan, Y., & Chen, N. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.06.002 · Cited by 15 · see citing works
Chakraborty, R., Belian, S., & Zurzolo, C. (2023) · Extracellular Vesicles and Circulating Nucleic Acids · doi:10.20517/evcna.2023.05 · Cited by 14 · see citing works
Bhardwaj, N., Puri, S., Kumari, A., Chauhan, A., & Kumar, A. (2024) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2024.105748 · Cited by 13 · see citing works
Walecha, V., & Luthra, P. M. (2025) · Neurochemical Research · doi:10.1007/s11064-025-04559-9 · Cited by 12 · see citing works
“Janus-Faced” α-Synuclein: Role in Parkinson’s Disease
Ray, B., Mahalakshmi, A. M., Tuladhar, S., Bhat, A., Srinivasan, A., Pellegrino, C., Kannan, A., Bolla, S. R., Chidambaram, S. B., & Sakharkar, M. K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.673395 · Cited by 13 · see citing works
Wang, T., Li, M., Pei, Z., Chen, Q., Qiu-sheng, C., & Li, Z. (2025) · Tissue and Cell · doi:10.1016/j.tice.2025.102751 · Cited by 10 · see citing works
- Authors
- Dieriks, B. V., Park, T. I.-H., Fourie, C., Faull, R. L. M., Dragunow, M., & Curtis, M. A.
- Affiliations
- University of Auckland (NZ)
- Corresponding author
- Curtis, Maurice A.
- Venue
- Scientific Reports
- Published
- 2017-02-23
- Volume
- 7
- Issue
- 1
- Pages
- 42984-42984
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC5322400
- OpenAlex
- W2590505799
- Cited by
- 158
- References
- 36
- Citations by year
- 2026: 14 · 2025: 11 · 2024: 15 · 2023: 13 · 2022: 29 · 2021: 23 · 2020: 14 · 2019: 16 · 2018: 13 · 2017: 10
- FWCI
- 10.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ResearchSpace (University of Auckland) (submittedVersion, cc-by)
- Funders
- Hugh Green Foundation
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- alpha-synuclein, tunneling nanotubes, Parkinson's disease, pericytes, SH-SY5Y cells, protein transfer, Lewy bodies, mitosis, intercellular communication
- MeSH terms
- Brain, Cell Membrane, Cells, Cultured, Humans, Microscopy, Electron, Scanning, Mitosis, Neurons, Parkinson Disease, Lewy Bodies, Microscopy, Confocal, Coculture Techniques, Pericytes, Protein Transport, Nanotubes, alpha-Synuclein, Time-Lapse Imaging
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