ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img

Proteomic Analysis of Gliosomes from Mouse Brain: Identification and Investigation of Glial Membrane Proteins

View Author Information
Department of Molecular & Cellular Neurobiology, Center for Neurogenomics and Cognitive Research, Neuroscience Campus Amsterdam, VU University Amsterdam, 1081 HV Amsterdam, The Netherlands
Department of Pharmacy, Pharmacology and Toxicology Unit and Center of Excellence for Biomedical Research, University of Genoa, 16148 Genoa, Italy
§ INSERM U862, Neurocentre Magendie, 33077 Bordeaux, France
Université de Bordeaux, 33077 Bordeaux, France
*E-mail: [email protected]; Phone: +31 20 5987120; Fax: +31 20 5989281.
Cite this: J. Proteome Res. 2014, 13, 12, 5918–5927
Publication Date (Web):October 13, 2014
https://doi.org/10.1021/pr500829z
Copyright © 2014 American Chemical Society

    Article Views

    1599

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (3)»

    Abstract

    Abstract Image

    Astrocytes are being increasingly recognized as crucial contributors to neuronal function at synapses, axons, and somas. Reliable methods that can provide insight into astrocyte proteins at the neuron–astrocyte functional interface are highly desirable. Here, we conducted a mass spectrometry analysis of Percoll gradient-isolated gliosomes, a viable preparation of glial subcellular particles often used to study mechanisms of astrocytic transmitter uptake and release and their regulation. Gliosomes were compared with synaptosomes, a preparation containing the neurotransmitter release machinery, and, accordingly, synaptosomes were enriched for proteins involved in synaptic vesicle-mediated transport. Interestingly, gliosome preparations were found to be enriched for different classes of known astrocyte proteins, such as VAMP3 (involved in astrocyte exocytosis), Ezrin (perisynaptic astrocyte cytoskeletal protein), and Basigin (astrocyte membrane glycoprotein), as well as for G-protein-mediated signaling proteins. Mass spectrometry data are available via ProteomeXchange with the identifier PXD001375. Together, these data provide the first detailed description of the gliosome proteome and show that gliosomes can be a useful preparation to study glial membrane proteins and associated processes.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    Figure 1: Validation of mass spectrometry measurements of homogenate samples. Bar graph depicts log2 enrichment + SEM of indicated proteins as compared to homogenate measured on the same set of samples (n = 3–5) by mass spectrometry and immunoblot. Corresponding immunoblots can be found in Figure 2. * FDR p ≤ 10% for mass spectrometry measurements and p ≤ 0.05 for immunoblots as determined by a one-tailed paired Student’s t test. Table 1: Mass spectrometry data indicating the identified proteins, numbers of peptides, post-translational modifications, and measured intensities per sample. Table 2: Over-represented biological process terms in gliosomes versus homogenate with gene names. Table 3: Over-represented biological process terms in synaptosomes versus homogenate with gene names. Table 4: Over-represented biological process terms in synaptosomes versus gliosomes with gene names. Table 5: Over-represented molecular function terms in gliosomes versus homogenate with gene names. Table 6: Over-represented molecular function terms in synaptosomes versus homogenate with gene names. Table 7: Over-represented molecular function terms in gliosomes versus synaptosomes with gene names. Table 8: Over-represented molecular function terms in synaptosomes versus gliosomes with gene names. Table 9: Over-represented cellular component terms in gliosomes versus homogenate with gene names. Table 10: Over-represented cellular component terms in synaptosomes versus homogenate with gene names. Table 11: Over-represented cellular component terms in gliosomes versus synaptosomes with gene names. Table 12: Over-represented cellular component terms in synaptosomes versus gliosomes with gene names. This material is available free of charge via the Internet at http://pubs.acs.org. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (54) via the PRIDE partner repository with the dataset identifier PDX001375.

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 25 publications.

    1. Guendalina Olivero, Alice Taddeucci, Giulia Vallarino, Hanna Trebesova, Alessandra Roggeri, Maria Cristina Gagliani, Katia Cortese, Massimo Grilli, Anna Pittaluga. Complement tunes glutamate release and supports synaptic impairments in an animal model of multiple sclerosis. British Journal of Pharmacology 2024, 175 https://doi.org/10.1111/bph.16328
    2. Tiziana Bonifacino, Jessica Mingardi, Roberta Facchinetti, Nathalie Sala, Giulia Frumento, Elona Ndoj, Marta Valenza, Caterina Paoli, Alessandro Ieraci, Carola Torazza, Matilde Balbi, Michele Guerinoni, Nadeem Muhammad, Isabella Russo, Marco Milanese, Caterina Scuderi, Alessandro Barbon, Luca Steardo, Giambattista Bonanno, Maurizio Popoli, Laura Musazzi. Changes at glutamate tripartite synapses in the prefrontal cortex of a new animal model of resilience/vulnerability to acute stress. Translational Psychiatry 2023, 13 (1) https://doi.org/10.1038/s41398-023-02366-w
    3. Gerardo G. Piroli, Allison M. Manuel, Richard S. McCain, Holland H. Smith, Oliver Ozohanics, Sara Mellid, J. Hunter Cox, William E. Cotham, Michael D. Walla, Alberto Cascón, Attila Ambrus, Norma Frizzell. Defective function of α-ketoglutarate dehydrogenase exacerbates mitochondrial ATP deficits during complex I deficiency. Redox Biology 2023, 67 , 102932. https://doi.org/10.1016/j.redox.2023.102932
    4. Francesca Provenzano, Carola Torazza, Tiziana Bonifacino, Giambattista Bonanno, Marco Milanese. The Key Role of Astrocytes in Amyotrophic Lateral Sclerosis and Their Commitment to Glutamate Excitotoxicity. International Journal of Molecular Sciences 2023, 24 (20) , 15430. https://doi.org/10.3390/ijms242015430
    5. Stephanie Puig, Xiangning Xue, Ryan Salisbury, Micah A. Shelton, Sam-Moon Kim, Mariah A. Hildebrand, Jill R. Glausier, Zachary Freyberg, George C. Tseng, Anastasia K. Yocum, David A. Lewis, Marianne L. Seney, Matthew L. MacDonald, Ryan W. Logan. Circadian rhythm disruptions associated with opioid use disorder in synaptic proteomes of human dorsolateral prefrontal cortex and nucleus accumbens. Molecular Psychiatry 2023, 12 https://doi.org/10.1038/s41380-023-02241-6
    6. Mandy S. J. Kater, Katharina F. Baumgart, Aina Badia‐Soteras, Tim S. Heistek, Karen E. Carney, A. Jacob Timmerman, Jan R. T. van Weering, August B. Smit, Marjo S. van der Knaap, Huibert D. Mansvelder, Mark H. G. Verheijen, Rogier Min. A novel role for MLC1 in regulating astrocyte–synapse interactions. Glia 2023, 71 (7) , 1770-1785. https://doi.org/10.1002/glia.24368
    7. Marc Oudart, Katia Avila-Gutierrez, Clara Moch, Elena Dossi, Giampaolo Milior, Anne-Cécile Boulay, Mathis Gaudey, Julien Moulard, Bérangère Lombard, Damarys Loew, Alexis-Pierre Bemelmans, Nathalie Rouach, Clément Chapat, Martine Cohen-Salmon. The ribosome-associated protein RACK1 represses Kir4.1 translation in astrocytes and influences neuronal activity. Cell Reports 2023, 42 (5) , 112456. https://doi.org/10.1016/j.celrep.2023.112456
    8. Priyadharshini Prabhakar, Rainer Pielot, Peter Landgraf, Josef Wissing, Anne Bayrhammer, Marco van Ham, Eckart D. Gundelfinger, Lothar Jänsch, Daniela C. Dieterich, Anke Müller. Monitoring regional astrocyte diversity by cell type‐specific proteomic labeling in vivo. Glia 2023, 71 (3) , 682-703. https://doi.org/10.1002/glia.24304
    9. Giselle Cheung, Danijela Bataveljic, Josien Visser, Naresh Kumar, Julien Moulard, Glenn Dallérac, Daria Mozheiko, Astrid Rollenhagen, Pascal Ezan, Cédric Mongin, Oana Chever, Alexis-Pierre Bemelmans, Joachim Lübke, Isabelle Leray, Nathalie Rouach. Physiological synaptic activity and recognition memory require astroglial glutamine. Nature Communications 2022, 13 (1) https://doi.org/10.1038/s41467-022-28331-7
    10. Darshan Sapkota, Mandy S.J. Kater, Kristina Sakers, Kayla R. Nygaard, Yating Liu, Sarah K. Koester, Stuart B. Fass, Allison M. Lake, Rohan Khazanchi, Rana R. Khankan, Mitchell C. Krawczyk, August B. Smit, Susan E. Maloney, Mark H.G. Verheijen, Ye Zhang, Joseph D. Dougherty. Activity-dependent translation dynamically alters the proteome of the perisynaptic astrocyte process. Cell Reports 2022, 41 (3) , 111474. https://doi.org/10.1016/j.celrep.2022.111474
    11. Ludovica Iovino, Veronica Giusti, Francesca Pischedda, Elena Giusto, Nicoletta Plotegher, Antonella Marte, Ilaria Battisti, Angela Di Iacovo, Algerta Marku, Giovanni Piccoli, Rina Bandopadhyay, Carla Perego, Tiziana Bonifacino, Giambattista Bonanno, Cristina Roseti, Elena Bossi, Giorgio Arrigoni, Luigi Bubacco, Elisa Greggio, Sabine Hilfiker, Laura Civiero. Trafficking of the glutamate transporter is impaired in LRRK2-related Parkinson’s disease. Acta Neuropathologica 2022, 144 (1) , 81-106. https://doi.org/10.1007/s00401-022-02437-0
    12. Noémie Mazaré, Marc Oudart, Julien Moulard, Giselle Cheung, Romain Tortuyaux, Philippe Mailly, David Mazaud, Alexis-Pierre Bemelmans, Anne-Cécile Boulay, Corinne Blugeon, Laurent Jourdren, Stéphane Le Crom, Nathalie Rouach, Martine Cohen-Salmon. Local Translation in Perisynaptic Astrocytic Processes Is Specific and Changes after Fear Conditioning. Cell Reports 2020, 32 (8) , 108076. https://doi.org/10.1016/j.celrep.2020.108076
    13. Grégory Ghézali, Flora Vasile, Nathan Curry, Marcus Fantham, Giselle Cheung, Pascal Ezan, Martine Cohen-Salmon, Clemens Kaminski, Nathalie Rouach. Neuronal Activity Drives Astroglial Connexin 30 in Perisynaptic Processes and Shapes Its Functions. Cerebral Cortex 2020, 30 (2) , 753-766. https://doi.org/10.1093/cercor/bhz123
    14. Marc Oudart, Romain Tortuyaux, Philippe Mailly, Noémie Mazaré, Anne-Cécile Boulay, Martine Cohen-Salmon. AstroDot: a new method for studying the spatial distribution of mRNA in astrocytes. Journal of Cell Science 2020, 61 https://doi.org/10.1242/jcs.239756
    15. Xuefei Liu, Hong Zheng. Leptin-Mediated Sympathoexcitation in Obese Rats: Role for Neuron–Astrocyte Crosstalk in the Arcuate Nucleus. Frontiers in Neuroscience 2019, 13 https://doi.org/10.3389/fnins.2019.01217
    16. Silvia Ravera, Carola Torazza, Tiziana Bonifacino, Francesca Provenzano, Claudia Rebosio, Marco Milanese, Cesare Usai, Isabella Panfoli, Giambattista Bonanno. Altered glucose catabolism in the presynaptic and perisynaptic compartments of SOD1 G93A mouse spinal cord and motor cortex indicates that mitochondria are the site of bioenergetic imbalance in ALS. Journal of Neurochemistry 2019, 151 (3) , 336-350. https://doi.org/10.1111/jnc.14819
    17. Tiziana Bonifacino, Claudia Rebosio, Francesca Provenzano, Carola Torazza, Matilde Balbi, Marco Milanese, Luca Raiteri, Cesare Usai, Ernesto Fedele, Giambattista Bonanno. Enhanced Function and Overexpression of Metabotropic Glutamate Receptors 1 and 5 in the Spinal Cord of the SOD1G93A Mouse Model of Amyotrophic Lateral Sclerosis during Disease Progression. International Journal of Molecular Sciences 2019, 20 (18) , 4552. https://doi.org/10.3390/ijms20184552
    18. Silvia Ravera, Tiziana Bonifacino, Martina Bartolucci, Marco Milanese, Elena Gallia, Francesca Provenzano, Katia Cortese, Isabella Panfoli, Giambattista Bonanno. Characterization of the Mitochondrial Aerobic Metabolism in the Pre- and Perisynaptic Districts of the SOD1G93A Mouse Model of Amyotrophic Lateral Sclerosis. Molecular Neurobiology 2018, 55 (12) , 9220-9233. https://doi.org/10.1007/s12035-018-1059-z
    19. Valentina Cerrato, Sara Mercurio, Ketty Leto, Elisa Fucà, Eriola Hoxha, Sara Bottes, Miriam Pagin, Marco Milanese, Chew‐Yee Ngan, Giulia Concina, Sergio Ottolenghi, Chia‐Lin Wei, Giambattista Bonanno, Giulio Pavesi, Filippo Tempia, Annalisa Buffo, Silvia K. Nicolis. S ox2 conditional mutation in mouse causes ataxic symptoms, cerebellar vermis hypoplasia, and postnatal defects of B ergmann glia. Glia 2018, 66 (9) , 1929-1946. https://doi.org/10.1002/glia.23448
    20. Joshua B. Foster, Fangli Zhao, Xueqin Wang, Zan Xu, Kuanhung Lin, Candice C. Askwith, Kevin J. Hodgetts, Chien-liang Glenn Lin. Pyridazine-derivatives Enhance Structural and Functional Plasticity of Tripartite Synapse Via Activation of Local Translation in Astrocytic Processes. Neuroscience 2018, 388 , 224-238. https://doi.org/10.1016/j.neuroscience.2018.07.028
    21. Lindsey B. Gano, Li-Ping Liang, Kristen Ryan, Cole R. Michel, Joe Gomez, Athanassios Vassilopoulos, Nichole Reisdorph, Kristofer S. Fritz, Manisha Patel. Altered mitochondrial acetylation profiles in a kainic acid model of temporal lobe epilepsy. Free Radical Biology and Medicine 2018, 123 , 116-124. https://doi.org/10.1016/j.freeradbiomed.2018.05.063
    22. Damek Homiack, Emma O'Cinneide, Sema Hajmurad, Gary P. Dohanich, Laura A. Schrader. Effect of acute alarm odor exposure and biological sex on generalized avoidance and glutamatergic signaling in the hippocampus of Wistar rats. Stress 2018, 21 (4) , 292-303. https://doi.org/10.1080/10253890.2018.1484099
    23. Nikhil J. Pandya, Frank Koopmans, Johan A. Slotman, Iryna Paliukhovich, Adriaan B. Houtsmuller, August B. Smit, Ka Wan Li. Correlation profiling of brain sub-cellular proteomes reveals co-assembly of synaptic proteins and subcellular distribution. Scientific Reports 2017, 7 (1) https://doi.org/10.1038/s41598-017-11690-3
    24. Tiziana Bonifacino, Luca Cattaneo, Elena Gallia, Aldamaria Puliti, Marcello Melone, Francesca Provenzano, Simone Bossi, Ilaria Musante, Cesare Usai, Fiorenzo Conti, Giambattista Bonanno, Marco Milanese. In-vivo effects of knocking-down metabotropic glutamate receptor 5 in the SOD1 mouse model of amyotrophic lateral sclerosis. Neuropharmacology 2017, 123 , 433-445. https://doi.org/10.1016/j.neuropharm.2017.06.020
    25. A.R. Barros-Barbosa, M.G. Lobo, F. Ferreirinha, P. Correia-de-Sá, J.M. Cordeiro. P2X7 receptor activation downmodulates Na+-dependent high-affinity GABA and glutamate transport into rat brain cortex synaptosomes. Neuroscience 2015, 306 , 74-90. https://doi.org/10.1016/j.neuroscience.2015.08.026

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect