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The Alzheimer’s gene SORL1 is a regulator of endosomal traffic and recycling in human neurons

Mishra, Swati, Knupp, Allison, Szabo, Marcell P., Williams, Charles A., Kinoshita, Chizuru, Hailey, Dale W., Wang, Yuliang, Andersen, Olav M., Young, Jessica E.·2022·Cellular and Molecular Life Sciences
DOI 10.1007/s00018-022-04182-9PMC PMC8885486

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Abstract

Background: Loss of the Sortilin-related receptor 1 ( SORL1 ) gene seems to act as a causal event for Alzheimer’s disease (AD). Recent studies have established that loss of SORL1 , as well as mutations in autosomal dominant AD genes APP and PSEN1/2 , pathogenically converge by swelling early endosomes, AD’s cytopathological hallmark. Acting together with the retromer trafficking complex, SORL1 has been shown to regulate the recycling of the amyloid precursor protein (APP) out of the endosome, contributing to endosomal swelling and to APP misprocessing. We hypothesized that SORL1 plays a broader role in neuronal endosomal recycling and used human induced pluripotent stem cell-derived neurons (hiPSC-Ns) to test this hypothesis. We examined endosomal recycling of three transmembrane proteins linked to AD pathophysiology: APP, the BDNF receptor Tropomyosin-related kinase B (TRKB), and the glutamate receptor subunit AMPA1 (GLUA1). Methods: We used isogenic hiPSCs engineered to have SORL1 depleted or to have enhanced SORL1 expression. We differentiated neurons from these cell lines and mapped the trafficking of APP, TRKB and GLUA1 within the endosomal network using confocal microscopy. We also performed cell surface recycling and lysosomal degradation assays to assess the functionality of the endosomal network in both SORL1 -depleted and -overexpressing neurons. The functional impact of GLUA1 recycling was determined by measuring synaptic activity. Finally, we analyzed alterations in gene expression in SORL1 -depleted neurons using RNA sequencing. Results: We find that as with APP, endosomal trafficking of GLUA1 and TRKB is impaired by loss of SORL1 . We show that trafficking of all three cargoes to late endosomes and lysosomes is affected by manipulating SORL1 expression. We also show that depletion of SORL1 significantly impacts the endosomal recycling pathway for APP and GLUA1 at the level of the recycling endosome and trafficking to the cell surface. This has a functional effect on neuronal activity as shown by multi-electrode array (MEA). Conversely, increased SORL1 expression enhances endosomal recycling for APP and GLUA1. Our unbiased transcriptomic data further support SORL1 ’s role in endosomal recycling. We observe altered expression networks that regulate cell surface trafficking and neurotrophic signaling in SORL1-depleted neurons. Conclusion: Collectively, and together with other recent observations, these findings suggest that one role for SORL1 is to contribute to endosomal degradation and recycling pathways in neurons, a conclusion that has both pathogenic and therapeutic implications for Alzheimer’s disease.

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  • SORLA has been previously shown to regulate and traffic neuronal components, including sorting/trafficking the GDNF/GFRa1 complex, regulating calpain-dependent degradation of synapsin, and trafficking glutamate receptors such as GLUA1.

    “Indeed, SORLA has been previously regulate and traffic neuronal components, including sorting/trafficking the GDNF/GFRa1 complex (Glerup, Lume et al. 2013), regulating calpain-dependent degradation of synapsin (Hartl, Nebrich et al. 2016), and trafficking glutamate receptors such as GLUA1 (Mishra, Knupp et al. 2022), which could consequently affect neurodegenerative outcome.”

    From SORLA up-regulation suppresses pathological effects in aged tauopathy mouse brain (2026) · cites this paper as Mishra, Knupp et al. 2022

  • SORL1 expression has a reciprocal role to prototypical cargos such as transferrin in cell surface recycling.

    “SORL1 expression has been shown to have a reciprocal role prototypical cargos such as transferrin to in cell surface recycling [30].”

    From Stabilizing the retromer complex rescues synaptic dysfunction and endosomal trafficking deficits in an Alzheimer’s disease mouse model (2025) · cites this paper as [30]

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Metadata

Authors
Mishra, S., Knupp, A., Szabo, M. P., Williams, C. A., Kinoshita, C., Hailey, D. W., Wang, Y., Andersen, O. M., & Young, J. E.
ORCID
Young, Jessica E.
Venue
Cellular and Molecular Life Sciences
Publisher
Springer Science and Business Media LLC
Published
2022-02-28
Volume
79
Issue
3
ISSN
  • 1420-682X
  • 1420-9071
DOI
10.1007/s00018-022-04182-9
PMC
PMC8885486
Cited by
126
References
10
Language
en
Licence
Funders
  • national institute on aging (R01AG062148)
  • brightfocus foundation (A2018656S)
  • national institutes of health (T32AG052354)

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