IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28952-y.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28952-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28952-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. Luciana Renna & Giovanni Stefano & Maria Paola Puggioni & Sang-Jin Kim & Anastasiya Lavell & John E. Froehlich & Graham Burkart & Stefano Mancuso & Christoph Benning & Federica Brandizzi, 2024. "ER-associated VAP27-1 and VAP27-3 proteins functionally link the lipid-binding ORP2A at the ER-chloroplast contact sites," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Rémy Char & Zhuangzhuang Liu & Cédric Jacqueline & Marion Davieau & Maria-Graciela Delgado & Clara Soufflet & Mathieu Fallet & Lionel Chasson & Raphael Chapuy & Voahirana Camosseto & Eva Strock & Reja, 2023. "RUFY3 regulates endolysosomes perinuclear positioning, antigen presentation and migration in activated phagocytes," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. James L. Daly & Chris M. Danson & Philip A. Lewis & Lu Zhao & Sara Riccardo & Lucio Filippo & Davide Cacchiarelli & Daehoon Lee & Stephen J. Cross & Kate J. Heesom & Wen-Cheng Xiong & Andrea Ballabio , 2023. "Multi-omic approach characterises the neuroprotective role of retromer in regulating lysosomal health," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    11. Kshitiz Walia & Abhishek Sharma & Sankalita Paul & Priya Chouhan & Gaurav Kumar & Rajesh Ringe & Mahak Sharma & Amit Tuli, 2024. "SARS-CoV-2 virulence factor ORF3a blocks lysosome function by modulating TBC1D5-dependent Rab7 GTPase cycle," Nature Communications, Nature, vol. 15(1), pages 1-24, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28952-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.