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Defects in ER–endosome contacts impact lysosome function in hereditary spastic paraplegia

Allison, Rachel, Edgar, James R., Pearson, Guy, Rizo, Tania, Newton, Timothy, Günther, Sven, Berner, Fiamma, Hague, Jennifer, Connell, James W., Winkler, Jürgen, Lippincott-Schwartz, Jennifer, Beetz, Christian, Winner, Beate, Reid, Evan·2017·Journal of Cell Biology
DOI 10.1083/jcb.201609033PMC PMC5412567
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Abstract

Contacts between endosomes and the endoplasmic reticulum (ER) promote endosomal tubule fission, but the mechanisms involved and consequences of tubule fission failure are incompletely understood. We found that interaction between the microtubule-severing enzyme spastin and the ESCRT protein IST1 at ER–endosome contacts drives endosomal tubule fission. Failure of fission caused defective sorting of mannose 6-phosphate receptor, with consequently disrupted lysosomal enzyme trafficking and abnormal lysosomal morphology, including in mouse primary neurons and human stem cell–derived neurons. Consistent with a role for ER-mediated endosomal tubule fission in lysosome function, similar lysosomal abnormalities were seen in cellular models lacking the WASH complex component strumpellin or the ER morphogen REEP1. Mutations in spastin, strumpellin, or REEP1 cause hereditary spastic paraplegia (HSP), a disease characterized by axonal degeneration. Our results implicate failure of the ER–endosome contact process in axonopathy and suggest that coupling of ER-mediated endosomal tubule fission to lysosome function links different classes of HSP proteins, previously considered functionally distinct, into a unifying pathway for axonal degeneration.

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  • Because gene products implicated in several other forms of HSP are involved in endosomal tubulation and impact lysosomal function, this pathway could represent an important converging theme in HSP pathogenesis.

    “Because the gene products implicated in several other forms of HSP, including the most common SPG4 form, are also involved in endosomal tubulation and impact lysosomal function, this pathway could represent an important converging theme in HSP pathogenesis (21).”

    From Hereditary spastic paraplegia SPG8 mutations impair CAV1-dependent, integrin-mediated cell adhesion (2020) · cites this paper as [21]

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Metadata

Authors
Allison, R., Edgar, J. R., Pearson, G., Rizo, T., Newton, T., Günther, S., Berner, F., Hague, J., Connell, J. W., Winkler, J., Lippincott-Schwartz, J., Beetz, C., Winner, B., & Reid, E.
Affiliations
  • Cambridge Institute for Medical Research, University of Cambridge, Cambridge CB2 0XY, England, UK 1
  • Interdisciplinary Center for Clinical Research (IZKF) Junior Research Group III and Federal Ministry of Education and Research (BMBF) Research Group Neuroscience, Friedrich-Alexander-University Erlangen-Nuernberg, 91054 Erlangen, Germany 4
  • Department of Clinical Chemistry and Laboratory Diagnostics, Jena University Hospital, 07743 Jena, Germany 7
  • Department of Molecular Neurology, Friedrich-Alexander-University Erlangen-Nuernberg, 91054 Erlangen, Germany 5
  • Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147 8
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2017-04-07
Volume
216
Issue
5
Pages
1337-1355
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.201609033
PMC
PMC5412567
Cited by
171
References
3
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor, 910 d)
Funders
  • Medical Research Council (MR/M00046X/1, G0800117, MR/K50127X/1)
  • Wellcome Trust (082381, 086598, 100140, 093026)
  • National Institute for Health Research
  • Federal Ministry of Education and Research (01GQ113)

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