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Dual function of Rpn5 in two PCI complexes, the 26S proteasome and COP9 signalosome

Journal Article · · Molecular Biology of the Cell
 [1];  [2];  [2];  [3];  [2];  [2];  [4];  [4];  [5];  [2];  [2];  [6]
  1. Technion–Israel Inst. of Technology, Haifa (Israel). Dept. of Biology; DOE/OSTI
  2. Technion–Israel Inst. of Technology, Haifa (Israel). Dept. of Biology
  3. Univ. of Haifa (Israel). Dept. of Evolutionary and Environmental Biology
  4. Univ. of Wisconsin, Madison, WI (United States). Dept. of Genetics
  5. Miltenyi Biotec, Bergisch-Gladbach (Germany)
  6. Univ. of Haifa (Israel). Dept. of Evolutionary and Environmental Biology; Univ. of Haifa (Israel). Dept. of Biology
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Subunit composition and architectural structure of the 26S proteasome lid is strictly conserved between all eukaryotes. This eight-subunit complex bears high similarity to the eukaryotic translation initiation factor 3 and to the COP9 signalosome (CSN), which together define the proteasome CSN/COP9/initiation factor (PCI) troika. In some unicellular eukaryotes, the latter two complexes lack key subunits, encouraging questions about the conservation of their structural design. Here we demonstrate that, in Saccharomyces cerevisiae, Rpn5 plays dual roles by stabilizing proteasome and CSN structures independently. Proteasome and CSN complexes are easily dissected, with Rpn5 the only subunit in common. Together with Rpn5, we identified a total of six bona fide subunits at roughly stoichiometric ratios in isolated, affinity-purified CSN. Moreover, the copy of Rpn5 associated with the CSN is required for enzymatic hydrolysis of Rub1/Nedd8 conjugated to cullins. We propose that multitasking by a single subunit, Rpn5 in this case, allows it to function in different complexes simultaneously. These observations demonstrate that functional substitution of subunits by paralogues is feasible, implying that the canonical composition of the three PCI complexes in S. cerevisiae is more robust than hitherto appreciated.
Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
FG02-88ER13968
OSTI ID:
1625223
Journal Information:
Molecular Biology of the Cell, Journal Name: Molecular Biology of the Cell Journal Issue: 7 Vol. 22; ISSN 1059-1524
Publisher:
American Society for Cell BiologyCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (16)

De Novo Disruption of the Proteasome Regulatory Subunit PSMD12 Causes a Syndromic Neurodevelopmental Disorder journal February 2017
Proteasome lid bridges mitochondrial stress with Cdc53/Cullin1 NEDDylation status journal January 2019
The Protein Quality Control Machinery Regulates Its Misassembled Proteasome Subunits journal April 2015
The Minimal Deneddylase Core of the COP9 Signalosome Excludes the Csn6 MPN− Domain journal August 2012
n-Butylidenephthalide Protects against Dopaminergic Neuron Degeneration and α-Synuclein Accumulation in Caenorhabditis elegans Models of Parkinson's Disease journal January 2014
The Proteasome Lid Triggers COP9 Signalosome Activity during the Transition of Saccharomyces cerevisiae Cells into Quiescence journal September 2019
NMR 1H, 13C, 15N backbone and side chain resonance assignment of the N-terminal domain of yeast proteasome lid subunit Rpn5 journal September 2018
Diversity of COP9 signalosome structures and functional consequences journal June 2015
Moonlighting and pleiotropy within two regulators of the degradation machinery: the proteasome lid and the CSN journal November 2014
Recognition and Cleavage of Related to Ubiquitin 1 (Rub1) and Rub1-Ubiquitin Chains by Components of the Ubiquitin-Proteasome System journal December 2012
Improved discovery of genetic interactions using CRISPRiSeq across multiple environments journal February 2019
The COP9 signalosome is involved in the regulation of lipid metabolism and of transition metals uptake in Saccharomyces cerevisiae journal November 2013
Yeast as a tool to select inhibitors of the cullin deneddylating enzyme Csn5 journal March 2016
The NEDD8 modification pathway in plants journal March 2014
Yeast as a tool to select inhibitors of the cullin deneddylating enzyme Csn5 text January 2016
Yeast as a tool to select inhibitors of the cullin deneddylating enzyme Csn5 text January 2016

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