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RUFY3 and RUFY4 are ARL8 effectors that promote coupling of endolysosomes to dynein-dynactin

Author

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  • Tal Keren-Kaplan

    (Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health)

  • Amra Sarić

    (Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health)

  • Saikat Ghosh

    (Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health)

  • Chad D. Williamson

    (Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health)

  • Rui Jia

    (Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health)

  • Yan Li

    (National Institute of Neurological Disorders and Stroke, National Institutes of Health)

  • Juan S. Bonifacino

    (Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health)

Abstract

The small GTPase ARL8 associates with endolysosomes, leading to the recruitment of several effectors that couple endolysosomes to kinesins for anterograde transport along microtubules, and to tethering factors for eventual fusion with other organelles. Herein we report the identification of the RUN- and FYVE-domain-containing proteins RUFY3 and RUFY4 as ARL8 effectors that promote coupling of endolysosomes to dynein-dynactin for retrograde transport along microtubules. Using various methodologies, we find that RUFY3 and RUFY4 interact with both GTP-bound ARL8 and dynein-dynactin. In addition, we show that RUFY3 and RUFY4 promote concentration of endolysosomes in the juxtanuclear area of non-neuronal cells, and drive redistribution of endolysosomes from the axon to the soma in hippocampal neurons. The function of RUFY3 in retrograde transport contributes to the juxtanuclear redistribution of endolysosomes upon cytosol alkalinization. These studies thus identify RUFY3 and RUFY4 as ARL8-dependent, dynein-dynactin adaptors or regulators, and highlight the role of ARL8 in the control of both anterograde and retrograde endolysosome transport.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28952-y
    DOI: 10.1038/s41467-022-28952-y
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    References listed on IDEAS

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    1. Gaurav Kumar & Prateek Chawla & Neha Dhiman & Sanya Chadha & Sheetal Sharma & Kanupriya Sethi & Mahak Sharma & Amit Tuli, 2022. "RUFY3 links Arl8b and JIP4-Dynein complex to regulate lysosome size and positioning," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    2. Rose Willett & José A. Martina & James P. Zewe & Rachel Wills & Gerald R. V. Hammond & Rosa Puertollano, 2017. "TFEB regulates lysosomal positioning by modulating TMEM55B expression and JIP4 recruitment to lysosomes," Nature Communications, Nature, vol. 8(1), pages 1-17, December.
    3. 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.
    4. Amra Saric & Spencer A. Freeman & Chad D. Williamson & Michal Jarnik & Carlos M. Guardia & Michael S. Fernandopulle & David C. Gershlick & Juan S. Bonifacino, 2021. "SNX19 restricts endolysosome motility through contacts with the endoplasmic reticulum," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    5. Camilla Raiborg & Eva M. Wenzel & Nina M. Pedersen & Hallvard Olsvik & Kay O. Schink & Sebastian W. Schultz & Marina Vietri & Veronica Nisi & Cecilia Bucci & Andreas Brech & Terje Johansen & Harald St, 2015. "Repeated ER–endosome contacts promote endosome translocation and neurite outgrowth," Nature, Nature, vol. 520(7546), pages 234-238, April.
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    1. Eutteum Jeong & Rose Willett & Alberto Rissone & Martina Spina & Rosa Puertollano, 2024. "TMEM55B links autophagy flux, lysosomal repair, and TFE3 activation in response to oxidative stress," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Agnieszka A. Kendrick & Jenna R. Christensen, 2022. "Bidirectional lysosome transport: a balancing act between ARL8 effectors," Nature Communications, Nature, vol. 13(1), pages 1-3, December.
    3. Rahul Kumar & Maleeha Khan & Vincent Francis & Adriana Aguila & Gopinath Kulasekaran & Emily Banks & Peter S. McPherson, 2024. "DENND6A links Arl8b to a Rab34/RILP/dynein complex, regulating lysosomal positioning and autophagy," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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