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Antibody-directed extracellular proximity biotinylation reveals that Contactin-1 regulates axo-axonic innervation of axon initial segments

Author

Listed:
  • Yuki Ogawa

    (Baylor College of Medicine)

  • Brian C. Lim

    (Baylor College of Medicine)

  • Shanu George

    (Cold Spring Harbor Laboratory)

  • Juan A. Oses-Prieto

    (University of California San Francisco)

  • Joshua M. Rasband

    (Baylor College of Medicine)

  • Yael Eshed-Eisenbach

    (Weizmann Institute of Science)

  • Hamdan Hamdan

    (Baylor College of Medicine
    Khalifa University)

  • Supna Nair

    (University of California San Francisco)

  • Francesco Boato

    (Cold Spring Harbor Laboratory)

  • Elior Peles

    (Weizmann Institute of Science)

  • Alma L. Burlingame

    (University of California San Francisco)

  • Linda Aelst

    (Cold Spring Harbor Laboratory)

  • Matthew N. Rasband

    (Baylor College of Medicine)

Abstract

Axon initial segment (AIS) cell surface proteins mediate key biological processes in neurons including action potential initiation and axo-axonic synapse formation. However, few AIS cell surface proteins have been identified. Here, we use antibody-directed proximity biotinylation to define the cell surface proteins in close proximity to the AIS cell adhesion molecule Neurofascin. To determine the distributions of the identified proteins, we use CRISPR-mediated genome editing for insertion of epitope tags in the endogenous proteins. We identify Contactin-1 (Cntn1) as an AIS cell surface protein. Cntn1 is enriched at the AIS through interactions with Neurofascin and NrCAM. We further show that Cntn1 contributes to assembly of the AIS extracellular matrix, and regulates AIS axo-axonic innervation by inhibitory basket cells in the cerebellum and inhibitory chandelier cells in the cortex.

Suggested Citation

  • Yuki Ogawa & Brian C. Lim & Shanu George & Juan A. Oses-Prieto & Joshua M. Rasband & Yael Eshed-Eisenbach & Hamdan Hamdan & Supna Nair & Francesco Boato & Elior Peles & Alma L. Burlingame & Linda Aels, 2023. "Antibody-directed extracellular proximity biotinylation reveals that Contactin-1 regulates axo-axonic innervation of axon initial segments," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42273-8
    DOI: 10.1038/s41467-023-42273-8
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    References listed on IDEAS

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    1. Keiichiro Suzuki & Yuji Tsunekawa & Reyna Hernandez-Benitez & Jun Wu & Jie Zhu & Euiseok J. Kim & Fumiyuki Hatanaka & Mako Yamamoto & Toshikazu Araoka & Zhe Li & Masakazu Kurita & Tomoaki Hishida & Mo, 2016. "In vivo genome editing via CRISPR/Cas9 mediated homology-independent targeted integration," Nature, Nature, vol. 540(7631), pages 144-149, December.
    2. 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.
    3. Hamdan Hamdan & Brian C. Lim & Tomohiro Torii & Abhijeet Joshi & Matthias Konning & Cameron Smith & Donna J. Palmer & Philip Ng & Christophe Leterrier & Juan A. Oses-Prieto & Alma L. Burlingame & Matt, 2020. "Mapping axon initial segment structure and function by multiplexed proximity biotinylation," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
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