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Title: Structural Analysis Reveals Features of Ribosome Assembly Factor Nsa1/WDR74 Important for Localization and Interaction with Rix7/NVL2

Journal Article · · Structure

Ribosome assembly is a complex process that requires hundreds of essential assembly factors, including Rix7 (NVL2 in mammals) and Nsa1 (WDR74 in mammals). Rix7 is a type II double ring, AAA-ATPase, which is closely related to the well-known Cdc48/p97. Previous studies in Saccharomyces cerevisiae suggest that Rix7 mediates the release of Nsa1 from nucleolar pre-60S particles; however, the underlying mechanisms of this release are unknown. Through multiple structural analyses we show that S. cerevisiae Nsa1 is composed of an N-terminal seven-bladed WD40 domain followed by a lysine-rich C terminus that extends away from the WD40 domain and is required for nucleolar localization. Additional co-immunoprecipitation assays with the mammalian homologs identified a well-conserved interface within WDR74 that is important for its association with NVL2. We further show that WDR74 associates with the D1 AAA domain of NVL2, which represents a novel mode of binding of a substrate with a type II AAA-ATPase.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institute of Environmental Health Sciences (NIEHS); National Institutes of Health (NIHI)
Grant/Contract Number:
W-31-109-Eng-38; AC02-05CH11231; ZIA ES103247; S10OD018483
OSTI ID:
1435653
Alternate ID(s):
OSTI ID: 1368256; OSTI ID: 1397654
Journal Information:
Structure, Journal Name: Structure Vol. 25 Journal Issue: 5; ISSN 0969-2126
Publisher:
ElsevierCopyright Statement
Country of Publication:
United Kingdom
Language:
English
Citation Metrics:
Cited by: 16 works
Citation information provided by
Web of Science

References (58)

The Landscape of Prognostic Outlier Genes in High-Risk Prostate Cancer journal December 2015
NVL2 Is a Nucleolar AAA-ATPase that Interacts with Ribosomal Protein L5 through Its Nucleolar Localization Sequence journal December 2004
The AAA-ATPase NVL2 is a component of pre-ribosomal particles that interacts with the DExD/H-box RNA helicase DOB1 journal August 2006
The AAA-ATPase NVL2 is a telomerase component essential for holoenzyme assembly journal January 2012
Overview of the CCP 4 suite and current developments journal March 2011
Structure and function of the AAA+ ATPase p97/Cdc48p journal May 2016
Global Rigid Body Modeling of Macromolecular Complexes against Small-Angle Scattering Data journal August 2005
Architecture of the Rix1–Rea1 checkpoint machinery during pre-60S-ribosome remodeling journal November 2015
Dali server: conservation mapping in 3D journal May 2010
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates journal December 1995
Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus journal September 2013
NVL2, a nucleolar AAA-ATPase, is associated with the nuclear exosome and is involved in pre-rRNA processing journal August 2015
Concerted removal of the Erb1–Ytm1 complex in ribosome biogenesis relies on an elaborate interface journal December 2015
Ribosomopathies: Mechanisms of Disease journal January 2014
Driving ribosome assembly journal June 2010
Translation Initiation Factor eIF3b Contains a Nine-Bladed β-Propeller and Interacts with the 40S Ribosomal Subunit journal June 2014
Transcriptomic signature of cell lines isolated from canine mammary adenocarcinoma metastases to lungs journal March 2010
AAA-ATPase NVL2 acts on MTR4-exosome complex to dissociate the nucleolar protein WDR74 journal November 2015
The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles journal June 2008
Evolutionary Relationships and Structural Mechanisms of aaa+ Proteins journal June 2006
A time- and cost-efficient system for high-level protein production in mammalian cells journal September 2006
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard journal May 2009
mTOR signaling regulates the processing of pre-rRNA in human cells journal November 2011
The Crystal Structure of the Ubiquitin-like Domain of Ribosome Assembly Factor Ytm1 and Characterization of Its Interaction with the AAA-ATPase Midasin journal January 2016
Ribosomal Proteins and Human Diseases: Pathogenesis, Molecular Mechanisms, and Therapeutic Implications: RIBOSOMAL PROTEINS AND HUMAN DISEASES journal August 2014
Ribosome Biogenesis in the Yeast Saccharomyces cerevisiae journal November 2013
Characterization and prediction of protein nucleolar localization sequences journal July 2010
The Exosome Is Recruited to RNA Substrates through Specific Adaptor Proteins journal August 2015
A protein interaction map of the LSU processome journal April 2015
NIH Image to ImageJ: 25 years of image analysis journal June 2012
WD40 proteins propel cellular networks journal October 2010
Potent, Reversible, and Specific Chemical Inhibitors of Eukaryotic Ribosome Biogenesis journal October 2016
Wdr74 Is Required for Blastocyst Formation in the Mouse journal July 2011
The AAA-ATPase Rea1 Drives Removal of Biogenesis Factors during Multiple Stages of 60S Ribosome Assembly journal June 2010
Origin and Functional Evolution of the Cdc48/p97/VCP AAA+ Protein Unfolding and Remodeling Machine journal May 2016
Genome-wide analysis of noncoding regulatory mutations in cancer journal September 2014
The nucleolus as a fundamental regulator of the p53 response and a new target for cancer therapy journal July 2015
High-Throughput SAXS for the Characterization of Biomolecules in Solution: A Practical Approach book October 2013
Mechanochemical Removal of Ribosome Biogenesis Factors from Nascent 60S Ribosomal Subunits journal September 2009
Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation journal November 2012
Features and development of Coot journal March 2010
A nuclear AAA-type ATPase (Rix7p) is required for biogenesis and nuclear export of 60S ribosomal subunits journal July 2001
REFMAC 5 for the refinement of macromolecular crystal structures journal March 2011
New developments in the ATSAS program package for small-angle scattering data analysis journal March 2012
Eukaryotic ribosome biogenesis at a glance journal October 2013
The NVL gene confers risk for both major depressive disorder and schizophrenia in the Han Chinese population journal October 2015
Mak5 and Ebp2 Act Together on Early Pre-60S Particles and Their Reduced Functionality Bypasses the Requirement for the Essential Pre-60S Factor Nsa1 journal December 2013
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Mysterious Ribosomopathies journal August 2013
Structure and Function of the N-terminal Nucleolin Binding Domain of Nuclear Valosin-containing Protein-like 2 (NVL2) Harboring a Nucleolar Localization Signal journal June 2011
Structure and function of WD40 domain proteins journal March 2011
Control of p97 function by cofactor binding journal August 2015
ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids journal May 2010
Accurate assessment of mass, models and resolution by small-angle scattering journal April 2013
The power of AAA-ATPases on the road of pre-60S ribosome maturation — Molecular machines that strip pre-ribosomal particles journal January 2012
[20] Processing of X-ray diffraction data collected in oscillation mode book January 1997
Identification of Human MVB12 Proteins as ESCRT-I Subunits that Function in HIV Budding journal July 2007
A network of assembly factors is involved in remodeling rRNA elements during preribosome maturation journal November 2014

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