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Type I interferon remodels lysosome function and modifies intestinal epithelial defense.

Hailong Zhang1,2,3, Abdelrahim Zoued1,2,3, Xu Liu1,2,3

  • 1Howard Hughes Medical Insitute, Boston, MA 02115.

Proceedings of the National Academy of Sciences of the United States of America
|November 11, 2020
PubMed
Summary

Type I interferon (IFN-I) signaling remodels lysosomes, enhancing their function and impacting host defense. This discovery reveals a new role for IFN-I in controlling cellular responses during bacterial infections like Salmonella.

Keywords:
Salmonella pathogenesisintestinal epitheliumlysosomemucosal defensetype I interferon

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Area of Science:

  • Cell Biology
  • Immunology
  • Microbiology

Background:

  • Organelle remodeling is crucial for cellular homeostasis.
  • Host factors controlling organelle function during microbial infections are not well understood.
  • Lysosomes play key roles in cellular defense and homeostasis.

Purpose of the Study:

  • To identify host factors that regulate organelle function during microbial infection.
  • To investigate the role of type I interferon (IFN-I) signaling in lysosome function.
  • To understand how IFN-I mediated lysosome remodeling affects host defense against Salmonella.

Main Methods:

  • Genome-scale CRISPR/Cas9 screening in intestinal epithelial cells.
  • Proteomic and genetic analyses of lysosome function.
  • In vivo studies of Salmonella pathogenesis in the intestinal epithelium.

Main Results:

  • Type I interferon (IFN-I) signaling significantly remodels lysosomes, altering their localization, acidification, protease activity, and proteomic profile.
  • IFN-I-stimulated genes, including IFITM3, SLC15A3, and CNP, were identified as contributors to lysosome acidification.
  • IFN-I-dependent lysosome acidification enhanced Salmonella virulence gene expression, promoted vacuole rupture, and induced host cell death, while also promoting Salmonella pathogenesis in vivo.

Conclusions:

  • Type I interferon (IFN-I) signaling directly remodels lysosome function, impacting cellular homeostasis and host defense mechanisms.
  • IFN-I-mediated control of lysosome acidification represents a novel mechanism of innate immunity against bacterial pathogens.
  • The findings suggest that IFN-I's influence on lysosome function has broad implications for host defense against various viral and microbial pathogens.