Global cellular proteo-lipidomic profiling of diverse lysosomal storage disease mutants using nMOST

Output Details

Preprint August 16, 2024

Published January 22, 2025

Lysosomal storage diseases (LSDs) comprise ~50 monogenic disorders marked by the buildup of cellular material in lysosomes, yet systematic global molecular phenotyping of proteins and lipids is lacking. We present a nanoflow-based multiomic single-shot technology (nMOST) workflow that quantifies HeLa cell proteomes and lipidomes from over two dozen LSD mutants. Global cross-correlation analysis between lipids and proteins identified autophagy defects, notably the accumulation of ferritinophagy substrates and receptors, especially in *NPC1*−/− and *NPC2*−/−mutants, where lysosomes accumulate cholesterol. Autophagic and endocytic cargo delivery failures correlated with elevated lysophosphatidylcholine species and multilamellar structures visualized by cryo–electron tomography. Loss of mitochondrial cristae, MICOS complex components, and OXPHOS components rich in iron-sulfur cluster proteins in *NPC2*−/− cells was largely alleviated when iron was provided through the transferrin system. This study reveals how lysosomal dysfunction affects mitochondrial homeostasis and underscores nMOST as a valuable discovery tool for identifying molecular phenotypes across LSDs.
Identifier (DOI)
10.1126/sciadv.adu5787
Tags
  • Original Research

Meet the Authors

  • Felix Kraus, PhD

    Project Manager: Team Harper

    Harvard University

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    Yuchen He

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    Sharan Swarup, PhD

    Key Personnel: Team Harper

    Harvard University

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    Katherine A. Overmyer

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    Yizhi Jiang, PhD

    Key Personnel: Team Harper

    Harvard Bioscience (United States)

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    Johann Brenner

  • Cristina Capitanio, MSc

    Key Personnel: Team Harper

    Max Planck Institute of Biochemistry

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    Anna Bieber, MSc

    Key Personnel: Team Harper

    Max Planck Institute of Biochemistry

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    Annie Jen

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    Nicole M. Nightingale

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    Benton J. Anderson

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    Chan Lee, PhD

    Key Personnel: Team Harper

    Harvard University

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    Joao A. Paulo

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    Ian R Smith

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    Jürgen M. Plitzko

  • Brenda Schulman, PhD

    Co-PI (Core Leadership): Team Harper

    Max Planck Institute of Biochemistry

  • Florian Wilfling, PhD

    Collaborating PI: Team Harper Team Hurley

    Max Planck Institute of Biophysics

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    Joshua J. Coon

  • J. Wade Harper

    Lead PI (Core Leadership): Team Harper

    Harvard University

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    Steven P. Gygi