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Cited by 17Ubiquitin and proteasome pathwaysHeat shock proteins researchGenetic Neurodegenerative Diseases

Phosphorylation of the 19S regulatory particle ATPase subunit, Rpt6, modifies susceptibility to proteotoxic stress and protein aggregation

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Marquez-Lona, Esther Magdalena, Torres-Machorro, Ana Lilia, Gonzales, Frankie R., Pillus, Lorraine, Patrick, Gentry N.·2017·PLOS ONE
DOI 10.1371/journal.pone.0179893PMC PMC5491056
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Abstract

The ubiquitin proteasome system (UPS) is a highly conserved and tightly regulated biochemical pathway that degrades the majority of proteins in eukaryotic cells. Importantly, the UPS is responsible for counteracting altered protein homeostasis induced by a variety of proteotoxic stresses. We previously reported that Rpt6, the ATPase subunit of the 19S regulatory particle (RP) of the 26S proteasome, is phosphorylated in mammalian neurons at serine 120 in response to neuronal activity. Furthermore, we found that Rpt6 S120 phosphorylation, which regulates the activity and distribution of proteasomes in neurons, is relevant for proteasome-dependent synaptic remodeling and function. To better understand the role of proteasome phosphorylation, we have constructed models of altered Rpt6 phosphorylation in S. cerevisiae by introducing chromosomal point mutations that prevent or mimic phosphorylation at the conserved serine (S119). We find that mutants which prevent Rpt6 phosphorylation at this site (rpt6-S119A), had increased susceptibility to proteotoxic stress, displayed abnormal morphology and had reduced proteasome activity. Since impaired proteasome function has been linked to the aggregation of toxic proteins including the Huntington's disease (HD) related huntingtin (Htt) protein with expanded polyglutamine repeats, we evaluated the extent of Htt aggregation in our phospho-dead (rpt6-S119A) and phospho-mimetic (rpt6-S119D) mutants. We showed Htt103Q aggregate size to be significantly larger in rpt6-S119A mutants compared to wild-type or rpt6-S119D strains. Furthermore, we observed that phosphorylation of endogenous Rpt6 at S119 is increased in response to various stress conditions. Together, these data suggest that Rpt6 phosphorylation at S119 may play an important function in proteasome-dependent relief of proteotoxic stress that can be critical in protein aggregation pathologies.

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  • Blocking phosphorylation of Rpt6 at S120 sensitizes yeast and mice to pathogenic effects of Huntington protein aggregation.

    “Furthermore, blocking phosphorylation of Rpt6 at S120 appears to sensitize both yeast and mice to pathogenic effects of Huntington protein aggregation”

    From Altered Phosphorylation of the Proteasome Subunit Rpt6 Has Minimal Impact on Synaptic Plasticity and Learning (2021) · cites this paper as Marquez-Lona et al., 2017

    The Results section (page not supplied) shows that blocking phosphorylation at yeast Rpt6 S119—the equivalent of mammalian S120—increased mutant Huntingtin aggregation and reduced growth when cells were challenged with canavanine. The Discussion (page not supplied) reports that mouse Rpt6 S120A blocked a treatment-induced increase in proteasome activity, but does not say it sensitized mice to Huntington-related pathology. It reports reduced aggregates and motor impairment for the different, phosphomimetic S120D mutant. (LLM, conf=0.88)

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Sorted by citations

Authors
Marquez-Lona, E. M., Torres-Machorro, A. L., Gonzales, F. R., Pillus, L., & Patrick, G. N.
Affiliations
University of California San Diego (US)
Corresponding author
Patrick, Gentry N.
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2017-06-29
Volume
12
Issue
6
Pages
e0179893
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0179893
PMC
PMC5491056
OpenAlex
W2728294576
Cited by
17
References
6
Citations by year
2023: 2 · 2022: 3 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 3 · 2017: 2
FWCI
1.12
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Institutes of Health (NS060847, GM090177, P50-GM085764)
  • University of California Institute for Mexico and the United States
  • Centro de Investigación Científica y de Educación Superior de Ensenada, Baja California
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Genetic Neurodegenerative Diseases
Keywords
Rpt6, 19S regulatory particle, proteasome, protein phosphorylation, ubiquitin-proteasome system, proteotoxic stress, protein aggregation, huntingtin, polyglutamine, Huntington's disease, proteasome activity, yeast model
MeSH terms
Adenosine Triphosphatases, Amino Acid Sequence, Animals, Humans, Phosphorylation, Protein Binding, Saccharomyces cerevisiae, Stress, Physiological, Sequence Homology, Amino Acid, Protein Folding, Saccharomyces cerevisiae Proteins, Proteasome Endopeptidase Complex, Rats

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