Current Neuropharmacology

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back Subscribe
Research Article

Neuroprotective Proteins in Hypoxia-stressed Astrocyte-Derived Extracellular Vesicles

Author(s): Berenice N. Bernal-Vicente, Isaac Ponce, Manuel Santos-Gutierrez, Emmanuel Ríos-Castro and Luis B. Tovar-y-Romo*

Volume 23, Issue 14, 2025

Published on: 19 June, 2025

Page: [1962 - 1978] Pages: 17

DOI: 10.2174/011570159X359837250611052037

Price: $65

Become a Editorial Board Member
Become a Reviewer
Become a Editor
Become a Section Editor

Abstract

Background: Advances in mass spectrometry-based proteomic analysis have generated extensive protein data from cells involved in neurodegenerative diseases. The field of neuroproteomics is expanding to include the study of extracellular vesicles (EVs) to identify potential biomarkers for disease prevention and endogenous factors involved in neuroprotection.

Methods: In this study, rat cortical astrocytes in normoxia were cultured under normoxic conditions and subsequently exposed to hypoxia. Astrocyte-derived EVs released into the supernatant were collected separately from both conditions. Label-free mass spectrometry-based proteomics was then performed to assess the effects of hypoxia on the EV protein cargo. A meta-analysis comparing the results with previously published EV proteomic datasets was also conducted.

Results: This study revealed a differential expression of 83 upregulated proteins under hypoxic conditions and 61 downregulated proteins under normoxic conditions, highlighting the protective protein signatures elicited by astrocytes. The dataset has been deposited in the ProteomeXchange Consortium with the identified PXD050160.

Conclusion: The present study makes a novel contribution by employing proteomic techniques to characterize the protein cargo of EVs isolated from primary rat astrocytes. This approach enables a more refined analysis of astrocyte-specific intercellular signaling under hypoxic conditions and provides valuable insights into the roles of astrocytes in maintaining brain homeostasis and contributing to pathological processes.

Keywords: Astrocyte, hypoxia, extracellular vesicles, proteomics, EV cargo, neuroprotection, stroke.

Graphical Abstract

[1]
Pantazopoulou, M.; Lamprokostopoulou, A.; Karampela, D.S.; Alexaki, A.; Delis, A.; Coens, A.; Samiotaki, M.; Kriebardis, A.G.; Melki, R.; Pagakis, S.N.; Stefanis, L.; Vekrellis, K. Differential intracellular trafficking of extracellular vesicles in microglia and astrocytes. Cell. Mol. Life Sci., 2023, 80(7), 193.
[http://dx.doi.org/10.1007/s00018-023-04841-5] [PMID: 37391572]
[2]
Khan, N.A.; Asim, M.; El-Menyar, A.; Biswas, K.H.; Rizoli, S.; Al-Thani, H. The evolving role of extracellular vesicles (exosomes) as biomarkers in traumatic brain injury: Clinical perspectives and therapeutic implications. Front. Aging Neurosci., 2022, 14, 933434.
[http://dx.doi.org/10.3389/fnagi.2022.933434]
[3]
Lizarraga-Valderrama, L.R.; Sheridan, G.K. Extracellular vesicles and intercellular communication in the central nervous system. FEBS Lett., 2021, 595(10), 1391-1410.
[http://dx.doi.org/10.1002/1873-3468.14074] [PMID: 33728650]
[4]
Vinaiphat, A.; Sze, S.K. Proteomics for comprehensive characterization of extracellular vesicles in neurodegenerative disease. Exp. Neurol., 2022, 355, 114149.
[http://dx.doi.org/10.1016/j.expneurol.2022.114149] [PMID: 35732219]
[5]
Allen, S.P.; Seehra, R.S.; Heath, P.R.; Hall, B.P.C.; Bates, J.; Garwood, C.J.; Matuszyk, M.M.; Wharton, S.B.; Simpson, J.E. Transcriptomic analysis of human astrocytes in vitro reveals hypoxia-induced mitochondrial dysfunction, modulation of metabolism, and dysregulation of the immune response. Int. J. Mol. Sci., 2020, 21(21), 8028.
[http://dx.doi.org/10.3390/ijms21218028] [PMID: 33126586]
[6]
Vangeison, G.; Rempe, D.A. The Janus-faced effects of hypoxia on astrocyte function. Neuroscientist, 2009, 15(6), 579-588.
[http://dx.doi.org/10.1177/1073858409332405] [PMID: 19359669]
[7]
Baumann, J.; Tsao, C.C.; Huang, S.F.; Gassmann, M.; Ogunshola, O.O. Astrocyte-specific hypoxia-inducible factor 1 (HIF-1) does not disrupt the endothelial barrier during hypoxia in vitro. Fluids Barriers CNS, 2021, 18(1), 13.
[http://dx.doi.org/10.1186/s12987-021-00247-2] [PMID: 33736658]
[8]
Guo, M.; Ma, X.; Feng, Y.; Han, S.; Dong, Q.; Cui, M.; Zhao, Y. In chronic hypoxia, glucose availability and hypoxic severity dictate the balance between HIF-1 and HIF-2 in astrocytes. FASEB J., 2019, 33(10), 11123-11136.
[http://dx.doi.org/10.1096/fj.201900402RR] [PMID: 31298941]
[9]
Schwanhäusser, B.; Busse, D.; Li, N.; Dittmar, G.; Schuchhardt, J.; Wolf, J.; Chen, W.; Selbach, M. Global quantification of mammalian gene expression control. Nature, 2011, 473(7347), 337-342.
[http://dx.doi.org/10.1038/nature10098] [PMID: 21593866]
[10]
Kowal, J.; Arras, G.; Colombo, M.; Jouve, M.; Morath, J.P.; Primdal-Bengtson, B.; Dingli, F.; Loew, D.; Tkach, M.; Théry, C. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Natl. Acad. Sci. USA, 2016, 113(8), E968-E977.
[http://dx.doi.org/10.1073/pnas.1521230113] [PMID: 26858453]
[11]
Heras-Romero, Y.; Morales-Guadarrama, A.; Santana-Martínez, R.; Ponce, I.; Rincón-Heredia, R.; Poot-Hernández, A.C.; Martínez-Moreno, A.; Urrieta, E.; Bernal-Vicente, B.N.; Campero-Romero, A.N.; Moreno-Castilla, P.; Greig, N.H.; Escobar, M.L.; Concha, L.; Tovar-y-Romo, L.B. Improved post-stroke spontaneous recovery by astrocytic extracellular vesicles. Mol. Ther., 2022, 30(2), 798-815.
[http://dx.doi.org/10.1016/j.ymthe.2021.09.023] [PMID: 34563674]
[12]
Campero-Romero, A.N.; Real, F.H.; Santana-Martínez, R.A.; Molina-Villa, T.; Aranda, C.; Ríos-Castro, E.; Tovar-y-Romo, L.B. Extracellular vesicles from neural progenitor cells promote functional recovery after stroke in mice with pharmacological inhibition of neurogenesis. Cell Death Discov., 2023, 9(1), 272.
[http://dx.doi.org/10.1038/s41420-023-01561-4] [PMID: 37507361]
[13]
Phan, N.V.; Rathbun, E.M.; Ouyang, Y.; Carmichael, S.T.; Segura, T. Biology-driven material design for ischaemic stroke repair. Nat. Rev. Bioeng., 2023, 2(1), 44-63.
[http://dx.doi.org/10.1038/s44222-023-00117-6]
[14]
Percie du Sert, N.; Hurst, V.; Ahluwalia, A.; Alam, S.; Avey, M.T.; Baker, M.; Browne, W.J.; Clark, A.; Cuthill, I.C.; Dirnagl, U.; Emerson, M.; Garner, P.; Holgate, S.T.; Howells, D.W.; Karp, N.A.; Lazic, S.E.; Lidster, K.; MacCallum, C.J.; Macleod, M.; Pearl, E.J.; Petersen, O.H.; Rawle, F.; Reynolds, P.; Rooney, K.; Sena, E.S.; Silberberg, S.D.; Steckler, T.; Würbel, H. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol., 2020, 18(7), e3000410.
[http://dx.doi.org/10.1371/journal.pbio.3000410] [PMID: 32663219]
[15]
Ríos-Castro, E.; Souza, G.H.M.F.; Delgadillo-Álvarez, D.M.; Ramírez-Reyes, L.; Torres-Huerta, A.L.; Velasco-Suárez, A.; Cruz-Cruz, C.; Hernández-Hernández, J.M.; Tapia-Ramírez, J. Quantitative proteomic analysis of MARC-145 cells infected with a mexican porcine reproductive and respiratory syndrome virus strain using a label-free based DIA approach. J. Am. Soc. Mass Spectrom., 2020, 31(6), 1302-1312.
[http://dx.doi.org/10.1021/jasms.0c00134] [PMID: 32379441]
[16]
Delgadillo, D.M.; Céspedes-Cruz, A.I.; Ríos-Castro, E.; Maldonado, R.M.G.; López-Nogueda, M.; Márquez-Gutiérrez, M.; Villalobos-Manzo, R.; Ramírez-Reyes, L.; Domínguez-Fuentes, M.; Tapia-Ramírez, J. Differential expression of proteins in an atypical presentation of autoimmune lymphoproliferative syndrome. Int. J. Mol. Sci., 2022, 23(10), 5366.
[http://dx.doi.org/10.3390/ijms23105366] [PMID: 35628184]
[17]
Li, G.Z.; Vissers, J.P.C.; Silva, J.C.; Golick, D.; Gorenstein, M.V.; Geromanos, S.J. Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures. Proteomics, 2009, 9(6), 1696-1719.
[http://dx.doi.org/10.1002/pmic.200800564] [PMID: 19294629]
[18]
Käll, L.; Storey, J.D.; MacCoss, M.J.; Noble, W.S. Assigning significance to peptides identified by tandem mass spectrometry using decoy databases. J. Proteome Res., 2008, 7(1), 29-34.
[http://dx.doi.org/10.1021/pr700600n] [PMID: 18067246]
[19]
Perez-Riverol, Y.; Bai, J.; Bandla, C.; García-Seisdedos, D.; Hewapathirana, S.; Kamatchinathan, S.; Kundu, D.J.; Prakash, A.; Frericks-Zipper, A.; Eisenacher, M.; Walzer, M.; Wang, S.; Brazma, A.; Vizcaíno, J.A. The PRIDE database resources in 2022: A hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res., 2022, 50(D1), D543-D552.
[http://dx.doi.org/10.1093/nar/gkab1038] [PMID: 34723319]
[20]
Guo, H.; Fan, Z.; Wang, S.; Ma, L.; Wang, J.; Yu, D.; Zhang, Z.; Wu, L.; Peng, Z.; Liu, W.; Hou, W.; Cai, Y. Astrocytic A1/A2 paradigm participates in glycogen mobilization mediated neuroprotection on reperfusion injury after ischemic stroke. J. Neuroinflammation, 2021, 18(1), 230.
[http://dx.doi.org/10.1186/s12974-021-02284-y] [PMID: 34645472]
[21]
Kyung, J.W.; Cho, I.H.; Lee, S.; Song, W.K.; Ryan, T.A.; Hoppa, M.B.; Kim, S.H. Adaptor Protein 2 (AP-2) complex is essential for functional axogenesis in hippocampal neurons. Sci. Rep., 2017, 7(1), 41620.
[http://dx.doi.org/10.1038/srep41620] [PMID: 28139716]
[22]
Jeppesen, D.K.; Fenix, A.M.; Franklin, J.L.; Higginbotham, J.N.; Zhang, Q.; Zimmerman, L.J.; Liebler, D.C.; Ping, J.; Liu, Q.; Evans, R.; Fissell, W.H.; Patton, J.G.; Rome, L.H.; Burnette, D.T.; Coffey, R.J. Reassessment of exosome composition. Cell, 2019, 177(2), 428-445.e18.
[http://dx.doi.org/10.1016/j.cell.2019.02.029] [PMID: 30951670]
[23]
Deng, F.; Miller, J. A review on protein markers of exosome from different bio-resources and the antibodies used for characterization. J. Histotechnol., 2019, 42(4), 226-239.
[http://dx.doi.org/10.1080/01478885.2019.1646984] [PMID: 31432761]
[24]
Morel, L.; Regan, M.; Higashimori, H.; Ng, S.K.; Esau, C.; Vidensky, S.; Rothstein, J.; Yang, Y. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J. Biol. Chem., 2013, 288(10), 7105-7116.
[http://dx.doi.org/10.1074/jbc.M112.410944] [PMID: 23364798]
[25]
Siman, R.; Roberts, V.L.; McNeil, E.; Dang, A.; Bavaria, J.E.; Ramchandren, S.; McGarvey, M. Biomarker evidence for mild central nervous system injury after surgically-induced circulation arrest. Brain Res., 2008, 1213, 1-11.
[http://dx.doi.org/10.1016/j.brainres.2008.03.034] [PMID: 18456245]
[26]
Shimada, T.; Fournier, A.E.; Yamagata, K. Neuroprotective function of 14-3-3 proteins in neurodegeneration. BioMed Res. Int., 2013, 2013, 1-11.
[http://dx.doi.org/10.1155/2013/564534] [PMID: 24364034]
[27]
Semenza, G.L. Hypoxia-inducible factors in physiology and medicine. Cell, 2012, 148(3), 399-408.
[http://dx.doi.org/10.1016/j.cell.2012.01.021] [PMID: 22304911]
[28]
Hartl, F.U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: From nascent chain to folded protein. Science, 2002, 295(5561), 1852-1858.
[http://dx.doi.org/10.1126/science.1068408] [PMID: 11884745]
[29]
Hochrainer, K.; Yang, W. Stroke proteomics: From discovery to diagnostic and therapeutic applications. Circ. Res., 2022, 130(8), 1145-1166.
[http://dx.doi.org/10.1161/CIRCRESAHA.122.320110] [PMID: 35420912]
[30]
Li, L.; Li, R.; Zacharek, A.; Wang, F.; Landschoot-Ward, J.; Chopp, M.; Chen, J.; Cui, X. ABCA1/ApoE/HDL signaling pathway facilitates myelination and oligodendrogenesis after stroke. Int. J. Mol. Sci., 2020, 21(12), 4369.
[http://dx.doi.org/10.3390/ijms21124369] [PMID: 32575457]
[31]
Jong, D.O.G.; Verhaar, M.C.; Chen, Y.; Vader, P.; Gremmels, H.; Posthuma, G.; Schiffelers, R.M.; Gucek, M.; Balkom, V.B.W.M. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J. Extracell. Vesicles, 2012, 1, 1-9.
[http://dx.doi.org/10.3402/jev.v1i0.18396]
[32]
Lee, J.Y.; Kim, E.; Choi, S.M.; Kim, D.W.; Kim, K.P.; Lee, I.; Kim, H.S. Microvesicles from brain-extract—treated mesenchymal stem cells improve neurological functions in a rat model of ischemic stroke. Sci. Rep., 2016, 6(1), 33038.
[http://dx.doi.org/10.1038/srep33038] [PMID: 27609711]
[33]
Couch, Y.; Akbar, N.; Davis, S.; Fischer, R.; Dickens, A.M.; Neuhaus, A.A.; Burgess, A.I.; Rothwell, P.M.; Buchan, A.M. Inflammatory stroke extracellular vesicles induce macrophage activation. Stroke, 2017, 48(8), 2292-2296.
[http://dx.doi.org/10.1161/STROKEAHA.117.017236] [PMID: 28536169]
[34]
Dickens, A.M.; Tovar-y-Romo, L.B.; Yoo, S.W.; Trout, A.L.; Bae, M.; Kanmogne, M.; Megra, B.; Williams, D.W.; Witwer, K.W.; Gacias, M.; Tabatadze, N.; Cole, R.N.; Casaccia, P.; Berman, J.W.; Anthony, D.C.; Haughey, N.J. Astrocyte-shed extracellular vesicles regulate the peripheral leukocyte response to inflammatory brain lesions. Sci. Signal., 2017, 10(473), eaai7696.
[http://dx.doi.org/10.1126/scisignal.aai7696] [PMID: 28377412]
[35]
Cosme, J.; Guo, H.; Hadipour-Lakmehsari, S.; Emili, A.; Gramolini, A.O. Hypoxia-induced changes in the fibroblast secretome, exosome, and whole-cell proteome using cultured, cardiac-derived cells isolated from neonatal mice. J. Proteome Res., 2017, 16(8), 2836-2847.
[http://dx.doi.org/10.1021/acs.jproteome.7b00144 ] [PMID: 28641008]
[36]
Chandran, I.V.; Welinder, C.; Gonçalves de Oliveira, K.; Cerezo-Magaña, M.; Månsson, A.S.; Johansson, M.C.; Marko-Varga, G.; Belting, M. Global extracellular vesicle proteomic signature defines U87-MG glioma cell hypoxic status with potential implications for non-invasive diagnostics. J. Neurooncol., 2019, 144(3), 477-488.
[http://dx.doi.org/10.1007/s11060-019-03262-4] [PMID: 31414377]
[37]
Wang, X.; Wang, J.; Shi, X.; Pan, C.; Liu, H.; Dong, Y.; Dong, R.; Mang, J.; Xu, Z. Proteomic analyses identify a potential mechanism by which extracellular vesicles aggravate ischemic stroke. Life Sci., 2019, 231, 116527.
[http://dx.doi.org/10.1016/j.lfs.2019.06.002] [PMID: 31176783]
[38]
You, Y.; Borgmann, K.; Edara, V.V.; Stacy, S.; Ghorpade, A.; Ikezu, T. Activated human astrocyte-derived extracellular vesicles modulate neuronal uptake, differentiation and firing. J. Extracell. Vesicles, 2020, 9(1), 1706801.
[http://dx.doi.org/10.1080/20013078.2019.1706801] [PMID: 32002171]
[39]
Deitmer, J.W.; Theparambil, S.M.; Ruminot, I.; Noor, S.I.; Becker, H.M. Energy dynamics in the brain: Contributions of astrocytes to metabolism and ph homeostasis. Front. Neurosci., 2019, 13, 1301.
[http://dx.doi.org/10.3389/fnins.2019.01301] [PMID: 31866811]
[40]
Li, J.; Pan, L.; Pembroke, W.G.; Rexach, J.E.; Godoy, M.I.; Condro, M.C.; Alvarado, A.G.; Harteni, M.; Chen, Y.W.; Stiles, L.; Chen, A.Y.; Wanner, I.B.; Yang, X.; Goldman, S.A.; Geschwind, D.H.; Kornblum, H.I.; Zhang, Y. Conservation and divergence of vulnerability and responses to stressors between human and mouse astrocytes. Nat. Commun., 2021, 12(1), 3958.
[http://dx.doi.org/10.1038/s41467-021-24232-3] [PMID: 34172753]
[41]
Smolič, T.; Tavčar, P.; Horvat, A.; Černe, U.; Vasle, H.A.; Tratnjek, L.; Kreft, M.E.; Scholz, N.; Matis, M.; Petan, T.; Zorec, R.; Vardjan, N. Astrocytes in stress accumulate lipid droplets. Glia, 2021, 69(6), 1540-1562.
[http://dx.doi.org/10.1002/glia.23978] [PMID: 33609060]
[42]
Yamagata, K. Lactate supply from astrocytes to neurons and its role in ischemic stroke-induced neurodegeneration. Neuroscience, 2022, 481, 219-231.
[http://dx.doi.org/10.1016/j.neuroscience.2021.11.035] [PMID: 34843897]
[43]
Genc, S.; Kurnaz, I.A.; Ozilgen, M. Astrocyte - neuron lactate shuttle may boost more ATP supply to the neuron under hypoxic conditions - in silico study supported by in vitro expression data. BMC Syst. Biol., 2011, 5(1), 162.
[http://dx.doi.org/10.1186/1752-0509-5-162] [PMID: 21995951]
[44]
Pantazopoulou, V.; Jeannot, P.; Rosberg, R.; Berg, T.J.; Pietras, A. Hypoxia-induced reactivity of tumor-associated astrocytes affects glioma cell properties. Cells, 2021, 10(3), 613.
[http://dx.doi.org/10.3390/cells10030613] [PMID: 33802060]
[45]
Mojsilovic-Petrovic, J.; Callaghan, D.; Cui, H.; Dean, C.; Stanimirovic, D.B.; Zhang, W. Hypoxia-inducible factor-1 (HIF-1) is involved in the regulation of hypoxia-stimulated expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) and MCP-5 (Ccl12) in astrocytes. J. Neuroinflammation, 2007, 4(1), 12.
[http://dx.doi.org/10.1186/1742-2094-4-12] [PMID: 17474992]
[46]
Perriot, S.; Mathias, A.; Perriard, G.; Canales, M.; Jonkmans, N.; Merienne, N.; Meunier, C.; Kassar, E.L.; Perrier, A.L.; Laplaud, D.A.; Schluep, M.; Déglon, N.; Pasquier, D.R. Human induced pluripotent stem cell-derived astrocytes are differentially activated by multiple sclerosis-associated cytokines. Stem Cell Reports, 2018, 11(5), 1199-1210.
[http://dx.doi.org/10.1016/j.stemcr.2018.09.015] [PMID: 30409508]
[47]
Zamanian, J.L.; Xu, L.; Foo, L.C.; Nouri, N.; Zhou, L.; Giffard, R.G.; Barres, B.A. Genomic analysis of reactive astrogliosis. J. Neurosci., 2012, 32(18), 6391-6410.
[http://dx.doi.org/10.1523/JNEUROSCI.6221-11.2012] [PMID: 22553043]
[48]
Khakh, B.S.; Sofroniew, M.V. Diversity of astrocyte functions] and phenotypes in neural circuits. Nat. Neurosci., 2015, 18(7), 942-952.
[http://dx.doi.org/10.1038/nn.4043] [PMID: 26108722]
[49]
Neal, M.; Richardson, J.R. Epigenetic regulation of astrocyte function in neuroinflammation and neurodegeneration. Biochim. Biophys. Acta Mol. Basis Dis., 2018, 1864(2), 432-443.
[http://dx.doi.org/10.1016/j.bbadis.2017.11.004] [PMID: 29113750]
[50]
Thompson, J.W.; Dave, K.R.; Young, J.I.; Perez-Pinzon, M.A. Ischemic preconditioning alters the epigenetic profile of the brain from ischemic intolerance to ischemic tolerance. Neurotherapeutics, 2013, 10(4), 789-797.
[http://dx.doi.org/10.1007/s13311-013-0202-9] [PMID: 23868468]
[51]
Liddelow, S.A.; Guttenplan, K.A.; Clarke, L.E.; Bennett, F.C.; Bohlen, C.J.; Schirmer, L.; Bennett, M.L.; Münch, A.E.; Chung, W.S.; Peterson, T.C.; Wilton, D.K.; Frouin, A.; Napier, B.A.; Panicker, N.; Kumar, M.; Buckwalter, M.S.; Rowitch, D.H.; Dawson, V.L.; Dawson, T.M.; Stevens, B.; Barres, B.A. Neurotoxic reactive astrocytes are induced by activated microglia. Nature, 2017, 541(7638), 481-487.
[http://dx.doi.org/10.1038/nature21029] [PMID: 28099414]
[52]
Wheeler, M.A.; Jaronen, M.; Covacu, R.; Zandee, S.E.J.; Scalisi, G.; Rothhammer, V.; Tjon, E.C.; Chao, C.C.; Kenison, J.E.; Blain, M.; Rao, V.T.S.; Hewson, P.; Barroso, A.; Gutiérrez-Vázquez, C.; Prat, A.; Antel, J.P.; Hauser, R.; Quintana, F.J. Environmental control of astrocyte pathogenic activities in cns inflammation. Cell, 2019, 176(3), 581-596.e18.
[http://dx.doi.org/10.1016/j.cell.2018.12.012] [PMID: 30661753]
[53]
Kaur, C.; Sivakumar, V.; Zhang, Y.; Ling, E.A. Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia, 2006, 54(8), 826-839.
[http://dx.doi.org/10.1002/glia.20420] [PMID: 16977604]
[54]
Wang, Y.; Fu, A.K.Y.; Ip, N.Y. Instructive roles of astrocytes in hippocampal synaptic plasticity: Neuronal activity-dependent regulatory mechanisms. FEBS J., 2022, 289(8), 2202-2218.
[http://dx.doi.org/10.1111/febs.15878] [PMID: 33864430]
[55]
Wang, Y.; Fu, W.Y.; Cheung, K.; Hung, K.W.; Chen, C.; Geng, H.; Yung, W.H.; Qu, J.Y.; Fu, A.K.Y.; Ip, N.Y. Astrocyte-secreted IL-33 mediates homeostatic synaptic plasticity in the adult hippocampus. Proc. Natl. Acad. Sci. USA, 2021, 118(1), e2020810118.
[http://dx.doi.org/10.1073/pnas.2020810118] [PMID: 33443211]
[56]
Ito, M.; Aswendt, M.; Lee, A.G.; Ishizaka, S.; Cao, Z.; Wang, E.H.; Levy, S.L.; Smerin, D.L.; McNab, J.A.; Zeineh, M.; Leuze, C.; Goubran, M.; Cheng, M.Y.; Steinberg, G.K. RNA-sequencing analysis revealed a distinct motor cortex transcriptome in spontaneously recovered mice after stroke. Stroke, 2018, 49(9), 2191-2199.
[http://dx.doi.org/10.1161/STROKEAHA.118.021508] [PMID: 30354987]
[57]
Quiroz-Baez, R.; Hernández-Ortega, K.; Martínez-Martínez, E. Insights into the proteomic profiling of extracellular vesicles for the identification of early biomarkers of neurodegeneration. Front. Neurol., 2020, 11, 580030.
[http://dx.doi.org/10.3389/fneur.2020.580030] [PMID: 33362690]

Rights & Permissions Print Cite