NOPCHAP1 is a PAQosome cofactor that helps loading NOP58 on RUVBL1/2 during box C/D snoRNP biogenesis

Yoann Abel; Ana C F Paiva; Jonathan Bizarro; Marie-Eve Chagot; Paulo E Santo; Marie-Cécile Robert; Marc Quinternet; Franck Vandermoere; Pedro M F Sousa; Philippe Fort; Bruno Charpentier; Xavier Manival; Tiago M Bandeiras; Edouard Bertrand; Céline Verheggen

doi:10.1093/nar/gkaa1226

NOPCHAP1 is a PAQosome cofactor that helps loading NOP58 on RUVBL1/2 during box C/D snoRNP biogenesis

Nucleic Acids Res. 2021 Jan 25;49(2):1094-1113. doi: 10.1093/nar/gkaa1226.

Authors

Yoann Abel^{1

2

3}, Ana C F Paiva^{4

5}, Jonathan Bizarro^{1

2}, Marie-Eve Chagot⁶, Paulo E Santo^{4

5}, Marie-Cécile Robert^{1

2

3}, Marc Quinternet⁷, Franck Vandermoere⁸, Pedro M F Sousa^{4

5}, Philippe Fort⁹, Bruno Charpentier⁶, Xavier Manival⁶, Tiago M Bandeiras^{4

5}, Edouard Bertrand^{1

2

3}, Céline Verheggen^{1

2

3}

Affiliations

¹ IGMM, CNRS, Univ Montpellier, Montpellier, France.
² Equipe labellisée Ligue Nationale Contre le Cancer, Montpellier, France.
³ IGH, CNRS, Univ Montpellier, Montpellier, France.
⁴ iBET, Instituto de Biologia Experimental e Tecnológica, Apartado 12, Oeiras, 2781-901, Portugal.
⁵ Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Av. da República, Oeiras, 2780-157, Portugal.
⁶ Université de Lorraine, CNRS, IMoPA, F-54000 Nancy, France.
⁷ Université de Lorraine, CNRS, INSERM, IBSLor, Biophysics and Structural Biology Core Facility, F-54000, Nancy, France.
⁸ IGF, CNRS, INSERM, Univ Montpellier, Montpellier, France.
⁹ CRBM, CNRS, Univ Montpellier, Montpellier, France.

Abstract

The PAQosome is a large complex composed of the HSP90/R2TP chaperone and a prefoldin-like module. It promotes the biogenesis of cellular machineries but it is unclear how it discriminates closely related client proteins. Among the main PAQosome clients are C/D snoRNPs and in particular their core protein NOP58. Using NOP58 mutants and proteomic experiments, we identify different assembly intermediates and show that C12ORF45, which we rename NOPCHAP1, acts as a bridge between NOP58 and PAQosome. NOPCHAP1 makes direct physical interactions with the CC-NOP domain of NOP58 and domain II of RUVBL1/2 AAA+ ATPases. Interestingly, NOPCHAP1 interaction with RUVBL1/2 is disrupted upon ATP binding. Moreover, while it robustly binds both yeast and human NOP58, it makes little interactions with NOP56 and PRPF31, two other closely related CC-NOP proteins. Expression of NOP58, but not NOP56 or PRPF31, is decreased in NOPCHAP1 KO cells. We propose that NOPCHAP1 is a client-loading PAQosome cofactor that selects NOP58 to promote box C/D snoRNP assembly.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

ATPases Associated with Diverse Cellular Activities / metabolism*
Adenosine Triphosphate / metabolism
Carrier Proteins / metabolism*
DNA Helicases / metabolism*
Eye Proteins / metabolism
Gene Knockout Techniques
Genes, Reporter
HSP90 Heat-Shock Proteins / metabolism
HeLa Cells
Humans
Molecular Chaperones / metabolism*
Multiprotein Complexes
Nuclear Proteins / metabolism*
Protein Domains
Protein Interaction Mapping
Proteomics / methods
Recombinant Fusion Proteins / metabolism
Ribonucleoproteins, Small Nucleolar / biosynthesis*
Ribonucleoproteins, Small Nucleolar / metabolism
Saccharomyces cerevisiae Proteins / metabolism

Substances

Carrier Proteins
Eye Proteins
HSP90 Heat-Shock Proteins
Molecular Chaperones
Multiprotein Complexes
NOP56 protein, human
NOP58 protein, S cerevisiae
NOP58 protein, human
Nuclear Proteins
PRPF31 protein, human
Recombinant Fusion Proteins
Ribonucleoproteins, Small Nucleolar
Saccharomyces cerevisiae Proteins
Adenosine Triphosphate
ATPases Associated with Diverse Cellular Activities
DNA Helicases
RUVBL1 protein, human
RUVBL2 protein, human