The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation

  1. Martin Müller
  2. Oliver Schmidt
  3. Mihaela Angelova
  4. Klaus Faserl
  5. Sabine Weys
  6. Leopold Kremser
  7. Thaddäus Pfaffenwimmer
  8. Thomas Dalik
  9. Claudine Kraft
  10. Zlatko Trajanoski
  11. Herbert Lindner
  12. David Teis  Is a corresponding author
  1. Medical University of Innsbruck, Austria
  2. University of Vienna, Austria
  3. University of Natural Resources and Applied Biosciences, Austria

Abstract

The degradation and recycling of cellular components is essential for cell growth and survival. Here we show how selective and non-selective lysosomal protein degradation pathways cooperate to ensure cell survival upon nutrient limitation. A quantitative analysis of starvation-induced proteome remodeling in yeast reveals comprehensive changes already in the first three hours. In this period, many different integral plasma membrane proteins undergo endocytosis and degradation in vacuoles via the multivesicular body (MVB) pathway. Their degradation becomes essential to maintain critical amino acids levels that uphold protein synthesis early during starvation. This promotes cellular adaptation, including the de novo synthesis of vacuolar hydrolases to boost the vacuolar catabolic activity. This order of events primes vacuoles for the efficient degradation of bulk cytoplasm via autophagy. Hence, a catabolic cascade including the coordinated action of the MVB pathway and autophagy is essential to enter quiescence to survive extended periods of nutrient limitation.

Article and author information

Author details

  1. Martin Müller

    Division of Cell Biology, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  2. Oliver Schmidt

    Cell Biology, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Mihaela Angelova

    Division of Bioinformatics, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  4. Klaus Faserl

    Division of Clinical Biochemistry, ProteinMicroAnalysis Facility, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  5. Sabine Weys

    Division of Cell Biology, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  6. Leopold Kremser

    Division of Clinical Biochemistry, ProteinMicroAnalysis Facility, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  7. Thaddäus Pfaffenwimmer

    Max F. Perutz Laboratories, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  8. Thomas Dalik

    Department of Chemistry, University of Natural Resources and Applied Biosciences, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  9. Claudine Kraft

    Max F. Perutz Laboratories, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  10. Zlatko Trajanoski

    Division of Bioinformatics, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  11. Herbert Lindner

    Division of Clinical Biochemistry, ProteinMicroAnalysis Facility, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    Competing interests
    The authors declare that no competing interests exist.
  12. David Teis

    Division of Cell Biology, Biocenter, Medical University of Innsbruck, Innsbruck, Austria
    For correspondence
    david.teis@i-med.ac.at
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Noboru Mizushima, The University of Tokyo, Japan

Version history

  1. Received: March 26, 2015
  2. Accepted: April 19, 2015
  3. Accepted Manuscript published: April 22, 2015 (version 1)
  4. Version of Record published: May 8, 2015 (version 2)

Copyright

© 2015, Müller et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Martin Müller
  2. Oliver Schmidt
  3. Mihaela Angelova
  4. Klaus Faserl
  5. Sabine Weys
  6. Leopold Kremser
  7. Thaddäus Pfaffenwimmer
  8. Thomas Dalik
  9. Claudine Kraft
  10. Zlatko Trajanoski
  11. Herbert Lindner
  12. David Teis
(2015)
The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation
eLife 4:e07736.
https://doi.org/10.7554/eLife.07736

Share this article

https://doi.org/10.7554/eLife.07736

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