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Lipid kinases VPS34 and PIKfyve coordinate a phosphoinositide cascade to regulate retriever-mediated recycling on endosomes

Giridharan, Sai Srinivas Panapakkam, Luo, Guangming, Rivero-Rios, Pilar, Steinfeld, Noah, Tronchere, Helene, Singla, Amika, Burstein, Ezra, Billadeau, Daniel D, Sutton, Michael A, Weisman, Lois S·2022·eLife
DOI 10.7554/elife.69709PMC PMC8816382

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Abstract

Cell surface receptors control how cells respond to their environment. Many cell surface receptors recycle from endosomes to the plasma membrane via a recently discovered pathway, which includes sorting-nexin SNX17, Retriever, WASH, and CCC complexes. Here, using mammalian cells, we discover that PIKfyve and its upstream PI3-kinase VPS34 positively regulate this pathway. VPS34 produces phosphatidylinositol 3-phosphate (PI3P), which is the substrate for PIKfyve to generate PI3,5P 2 . We show that PIKfyve controls recycling of cargoes including integrins, receptors that control cell migration. Furthermore, endogenous PIKfyve colocalizes with SNX17, Retriever, WASH, and CCC complexes on endosomes. Importantly, PIKfyve inhibition results in displacement of Retriever and CCC from endosomes. In addition, we show that recruitment of SNX17 is an early step and requires VPS34. These discoveries suggest that VPS34 and PIKfyve coordinate an ordered pathway to regulate recycling from endosomes and suggest how PIKfyve functions in cell migration.

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Authors
Giridharan, S. S. P., Luo, G., Rivero-Rios, P., Steinfeld, N., Tronchere, H., Singla, A., Burstein, E., Billadeau, D. D., Sutton, M. A., & Weisman, L. S.
Affiliations
  • Life Sciences Institute and Department of Cellular and Developmental Biology, University of Michigan
  • INSERM U1048 I2MC, France and Université Paul Sabatier
  • Department of Internal Medicine, and Department of Molecular Biology, University of Texas Southwestern Medical Center
  • Division of Oncology Research and Schulze Center for Novel Therapeutics, Mayo Clinic
  • Neuroscience Graduate Program, Molecular and Behavioral Neuroscience Institute, Molecular and Integrative Physiology, University of Michigan
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2022-01-18
Volume
11
ISSN
2050-084X
DOI
10.7554/elife.69709
PMC
PMC8816382
Cited by
61
References
6
Language
en
Licence
Funders
  • National Institute of Neurological Disorders and Stroke (Research Project Grant R01 NS064015, Research Project Grant R01-NS099340)
  • National Institute of Diabetes and Digestive and Kidney Diseases (Research Project Grant R01-DK107733)
  • American Heart Association (Postdoctoral Fellowship 14POST20480137, Postdoctoral Fellowship 19POST34450253)
  • University of Michigan Protein Folding Diseases Fast Forward Initiative (Pilot grant)

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