Topological confinement by a membrane anchor suppresses phase separation into protein aggregates: Implications for prion diseases

K Kalpshree Gogte (Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum) F Fatemeh Mamashli (Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum) M Maria Georgina Herrera (Department Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum) S Simon Kriegler (Physical Chemistry I - Biophysical Chemistry, Faculty of Chemistry and Chemical Biology, TU Dortmund University) V Verian Bader (Department Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum) J Janine Kamps (Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum) P Prerna Grover (Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum) R Roland Winter (Physical Chemistry I - Biophysical Chemistry, Faculty of Chemistry and Chemical Biology, TU Dortmund University) K Konstanze F. Winklhofer (Department Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum) J Jörg Tatzelt (Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum)

Abstract

Protein misfolding and aggregation are a hallmark of various neurodegenerative disorders. However, the underlying mechanisms driving protein misfolding in the cellular context are incompletely understood. Here, we show that the two-dimensional confinement imposed by a membrane anchor stabilizes the native protein conformation and suppresses liquid–liquid phase separation (LLPS) and protein aggregation. Inherited prion diseases in humans and neurodegeneration in transgenic mice are linked to the expression of anchorless prion protein (PrP), suggesting that the C-terminal glycosylphosphatidylinositol (GPI) anchor of native PrP impedes spontaneous formation of neurotoxic and infectious PrP species. Combining unique in vitro and in vivo approaches, we demonstrate that anchoring to membranes prevents LLPS and spontaneous aggregation of PrP. Upon release from the membrane, PrP undergoes a conformational transition to detergent-insoluble aggregates. Our study demonstrates an essential role of the GPI anchor in preventing spontaneous misfolding of PrP C and provides a mechanistic basis for inherited prion diseases associated with anchorless PrP.

Article Details

Volume / Issue Vol. 122, Issue 1
Published January 07, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (10)

K

Kalpshree Gogte

Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum

F

Fatemeh Mamashli

Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum

M

Maria Georgina Herrera

Department Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum

S

Simon Kriegler

Physical Chemistry I - Biophysical Chemistry, Faculty of Chemistry and Chemical Biology, TU Dortmund University

V

Verian Bader

Department Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum

J

Janine Kamps

Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum

P

Prerna Grover

Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum

R

Roland Winter

Physical Chemistry I - Biophysical Chemistry, Faculty of Chemistry and Chemical Biology, TU Dortmund University

K

Konstanze F. Winklhofer

Department Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum

J

Jörg Tatzelt

Department Biochemistry of Neurodegenerative Diseases, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum