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Spatiotemporal proteomics reveals the biosynthetic lysosomal membrane protein interactome in neurons

Author

Listed:
  • Chun Hei Li

    (Utrecht University)

  • Noortje Kersten

    (Utrecht University)

  • Nazmiye Özkan

    (Utrecht University)

  • Dan T. M. Nguyen

    (Utrecht University)

  • Max Koppers

    (Utrecht University
    Vrije Universiteit Amsterdam)

  • Harm Post

    (Utrecht University)

  • Maarten Altelaar

    (Utrecht University)

  • Ginny G. Farias

    (Utrecht University)

Abstract

Lysosomes are membrane-bound organelles critical for maintaining cellular homeostasis. Delivery of biosynthetic lysosomal proteins to lysosomes is crucial to orchestrate proper lysosomal function. However, it remains unknown how the delivery of biosynthetic lysosomal proteins to lysosomes is ensured in neurons, which are highly polarized cells. Here, we developed Protein Origin, Trafficking And Targeting to Organelle Mapping (POTATOMap), by combining trafficking synchronization and proximity-labelling based proteomics, to unravel the trafficking routes and interactome of the biosynthetic lysosomal membrane protein LAMP1 at specified time points. This approach, combined with advanced microscopy, enables us to identify the neuronal domain-specific trafficking machineries of biosynthetic LAMP1. We reveal a role in replenishing axonal lysosomes, in delivery of newly synthesized axonal synaptic proteins, and interactions with RNA granules to facilitate hitchhiking in the axon. POTATOMap offers a robust approach to map out dynamic biosynthetic protein trafficking and interactome from their origin to destination.

Suggested Citation

  • Chun Hei Li & Noortje Kersten & Nazmiye Özkan & Dan T. M. Nguyen & Max Koppers & Harm Post & Maarten Altelaar & Ginny G. Farias, 2024. "Spatiotemporal proteomics reveals the biosynthetic lysosomal membrane protein interactome in neurons," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55052-w
    DOI: 10.1038/s41467-024-55052-w
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    1. Nouf N. Laqtom & Wentao Dong & Uche N. Medoh & Andrew L. Cangelosi & Vimisha Dharamdasani & Sze Ham Chan & Tenzin Kunchok & Caroline A. Lewis & Ivonne Heinze & Rachel Tang & Christian Grimm & An N. Da, 2022. "CLN3 is required for the clearance of glycerophosphodiesters from lysosomes," Nature, Nature, vol. 609(7929), pages 1005-1011, September.
    2. Sara Cuylen & Claudia Blaukopf & Antonio Z. Politi & Thomas Müller-Reichert & Beate Neumann & Ina Poser & Jan Ellenberg & Anthony A. Hyman & Daniel W. Gerlich, 2016. "Ki-67 acts as a biological surfactant to disperse mitotic chromosomes," Nature, Nature, vol. 535(7611), pages 308-312, July.
    3. Hankum Park & Frances V. Hundley & Qing Yu & Katherine A. Overmyer & Dain R. Brademan & Lia Serrano & Joao A. Paulo & Julia C. Paoli & Sharan Swarup & Joshua J. Coon & Steven P. Gygi & J. Wade Harper, 2022. "Spatial snapshots of amyloid precursor protein intramembrane processing via early endosome proteomics," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    4. Maaike S. Pols & Eline van Meel & Viola Oorschot & Corlinda ten Brink & Minoru Fukuda & M.G. Swetha & Satyajit Mayor & Judith Klumperman, 2013. "hVps41 and VAMP7 function in direct TGN to late endosome transport of lysosomal membrane proteins," Nature Communications, Nature, vol. 4(1), pages 1-12, June.
    5. Jay Xiaojun Tan & Toren Finkel, 2022. "A phosphoinositide signalling pathway mediates rapid lysosomal repair," Nature, Nature, vol. 609(7928), pages 815-821, September.
    6. 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.
    7. Anand Patwardhan & Sabine Bardin & Stéphanie Miserey-Lenkei & Lionel Larue & Bruno Goud & Graça Raposo & Cédric Delevoye, 2017. "Routing of the RAB6 secretory pathway towards the lysosome related organelle of melanocytes," Nature Communications, Nature, vol. 8(1), pages 1-14, August.
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