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Cell type-specific biotin labeling in vivo resolves regional neuronal and astrocyte proteomic differences in mouse brain

Author

Listed:
  • Sruti Rayaprolu

    (Emory University
    Emory University)

  • Sara Bitarafan

    (Georgia W. Woodruff School of Mechanical Engineering, Parker H. Petit Institute for Bioengineering and Bioscience, and Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology)

  • Juliet V. Santiago

    (Emory University
    Emory University)

  • Ranjita Betarbet

    (Emory University
    Emory University)

  • Sydney Sunna

    (Emory University
    Emory University)

  • Lihong Cheng

    (Emory University
    Emory University)

  • Hailian Xiao

    (Emory University
    Emory University)

  • Ruth S. Nelson

    (Emory University
    Emory University)

  • Prateek Kumar

    (Emory University
    Emory University)

  • Pritha Bagchi

    (Emory University
    Emory University
    Emory University)

  • Duc M. Duong

    (Emory University
    Emory University
    Emory University)

  • Annie M. Goettemoeller

    (Emory University)

  • Viktor János Oláh

    (Emory University)

  • Matt Rowan

    (Emory University)

  • Allan I. Levey

    (Emory University
    Emory University)

  • Levi B. Wood

    (Georgia W. Woodruff School of Mechanical Engineering, Parker H. Petit Institute for Bioengineering and Bioscience, and Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology)

  • Nicholas T. Seyfried

    (Emory University
    Emory University
    Emory University)

  • Srikant Rangaraju

    (Emory University
    Emory University)

Abstract

Proteomic profiling of brain cell types using isolation-based strategies pose limitations in resolving cellular phenotypes representative of their native state. We describe a mouse line for cell type-specific expression of biotin ligase TurboID, for in vivo biotinylation of proteins. Using adenoviral and transgenic approaches to label neurons, we show robust protein biotinylation in neuronal soma and axons throughout the brain, allowing quantitation of over 2000 neuron-derived proteins spanning synaptic proteins, transporters, ion channels and disease-relevant druggable targets. Next, we contrast Camk2a-neuron and Aldh1l1-astrocyte proteomes and identify brain region-specific proteomic differences within both cell types, some of which might potentially underlie the selective vulnerability to neurological diseases. Leveraging the cellular specificity of proteomic labeling, we apply an antibody-based approach to uncover differences in neuron and astrocyte-derived signaling phospho-proteins and cytokines. This approach will facilitate the characterization of cell-type specific proteomes in a diverse number of tissues under both physiological and pathological states.

Suggested Citation

  • Sruti Rayaprolu & Sara Bitarafan & Juliet V. Santiago & Ranjita Betarbet & Sydney Sunna & Lihong Cheng & Hailian Xiao & Ruth S. Nelson & Prateek Kumar & Pritha Bagchi & Duc M. Duong & Annie M. Goettem, 2022. "Cell type-specific biotin labeling in vivo resolves regional neuronal and astrocyte proteomic differences in mouse brain," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30623-x
    DOI: 10.1038/s41467-022-30623-x
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    1. Tetsuya Takano & John T. Wallace & Katherine T. Baldwin & Alicia M. Purkey & Akiyoshi Uezu & Jamie L. Courtland & Erik J. Soderblom & Tomomi Shimogori & Patricia F. Maness & Cagla Eroglu & Scott H. So, 2020. "Chemico-genetic discovery of astrocytic control of inhibition in vivo," Nature, Nature, vol. 588(7837), pages 296-302, December.
    2. Joon-Hyuk Lee & Ji-young Kim & Seulgi Noh & Hyoeun Lee & Se Young Lee & Ji Young Mun & Hyungju Park & Won-Suk Chung, 2021. "Astrocytes phagocytose adult hippocampal synapses for circuit homeostasis," Nature, Nature, vol. 590(7847), pages 612-617, February.
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    Cited by:

    1. Jonathan J. Swietlik & Stefanie Bärthel & Chiara Falcomatà & Diana Fink & Ankit Sinha & Jingyuan Cheng & Stefan Ebner & Peter Landgraf & Daniela C. Dieterich & Henrik Daub & Dieter Saur & Felix Meissn, 2023. "Cell-selective proteomics segregates pancreatic cancer subtypes by extracellular proteins in tumors and circulation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Prateek Kumar & Annie M. Goettemoeller & Claudia Espinosa-Garcia & Brendan R. Tobin & Ali Tfaily & Ruth S. Nelson & Aditya Natu & Eric B. Dammer & Juliet V. Santiago & Sneha Malepati & Lihong Cheng & , 2024. "Native-state proteomics of Parvalbumin interneurons identifies unique molecular signatures and vulnerabilities to early Alzheimer’s pathology," Nature Communications, Nature, vol. 15(1), pages 1-26, December.

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