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A conserved interaction of the dynein light intermediate chain with dynein-dynactin effectors necessary for processivity

Author

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  • In-Gyun Lee

    (University of Pennsylvania)

  • Mara A. Olenick

    (University of Pennsylvania)

  • Malgorzata Boczkowska

    (University of Pennsylvania)

  • Clara Franzini-Armstrong

    (University of Pennsylvania)

  • Erika L. F. Holzbaur

    (University of Pennsylvania)

  • Roberto Dominguez

    (University of Pennsylvania)

Abstract

Cytoplasmic dynein is the major minus-end-directed microtubule-based motor in cells. Dynein processivity and cargo selectivity depend on cargo-specific effectors that, while generally unrelated, share the ability to interact with dynein and dynactin to form processive dynein–dynactin-effector complexes. How this is achieved is poorly understood. Here, we identify a conserved region of the dynein Light Intermediate Chain 1 (LIC1) that mediates interactions with unrelated dynein–dynactin effectors. Quantitative binding studies map these interactions to a conserved helix within LIC1 and to N-terminal fragments of Hook1, Hook3, BICD2, and Spindly. A structure of the LIC1 helix bound to the N-terminal Hook domain reveals a conformational change that creates a hydrophobic cleft for binding of the LIC1 helix. The LIC1 helix competitively inhibits processive dynein–dynactin-effector motility in vitro, whereas structure-inspired mutations in this helix impair lysosomal positioning in cells. The results reveal a conserved mechanism of effector interaction with dynein–dynactin necessary for processive motility.

Suggested Citation

  • In-Gyun Lee & Mara A. Olenick & Malgorzata Boczkowska & Clara Franzini-Armstrong & Erika L. F. Holzbaur & Roberto Dominguez, 2018. "A conserved interaction of the dynein light intermediate chain with dynein-dynactin effectors necessary for processivity," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-03412-8
    DOI: 10.1038/s41467-018-03412-8
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    Cited by:

    1. Lucia Cassella & Anne Ephrussi, 2022. "Subcellular spatial transcriptomics identifies three mechanistically different classes of localizing RNAs," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Shuwen He & John P. Gillies & Juliana L. Zang & Carmen M. Córdoba-Beldad & Io Yamamoto & Yasuhiro Fujiwara & Julie Grantham & Morgan E. DeSantis & Hiroki Shibuya, 2023. "Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Ricardo Celestino & Morkos A Henen & José B Gama & Cátia Carvalho & Maxwell McCabe & Daniel J Barbosa & Alexandra Born & Parker J Nichols & Ana X Carvalho & Reto Gassmann & Beat Vögeli, 2019. "A transient helix in the disordered region of dynein light intermediate chain links the motor to structurally diverse adaptors for cargo transport," PLOS Biology, Public Library of Science, vol. 17(1), pages 1-33, January.
    4. Tal Keren-Kaplan & Amra Sarić & Saikat Ghosh & Chad D. Williamson & Rui Jia & Yan Li & Juan S. Bonifacino, 2022. "RUFY3 and RUFY4 are ARL8 effectors that promote coupling of endolysosomes to dynein-dynactin," Nature Communications, Nature, vol. 13(1), pages 1-22, December.

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