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Title: A divergent Pumilio repeat protein family for pre-rRNA processing and mRNA localization

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [1];  [3];  [1]
  1. National Inst. of Health, Research Triangle Park, NC (United States). National Inst. of Environmental Health Sciences. Epigenetics and Stem Cell Biology Lab.
  2. Yale Univ., New Haven, CT (United States). School of Medicine. Dept. of Genetics
  3. Yale Univ., New Haven, CT (United States). School of Medicine. Dept. of Genetics. Dept. of Molecular Biophysics and Biochemistry. Dept. of Therapeutic Radiology

Pumilio/feminization of XX and XO animals (fem)-3 mRNA-binding factor (PUF) proteins bind sequence specifically to mRNA targets using a single-stranded RNA-binding domain comprising eight Pumilio (PUM) repeats. PUM repeats have now been identified in proteins that function in pre-rRNA processing, including human Puf-A and yeast Puf6. This is a role not previously ascribed to PUF proteins. In this paper we present crystal structures of human Puf-A that reveal a class of nucleic acid-binding proteins with 11 PUM repeats arranged in an “L”-like shape. In contrast to classical PUF proteins, Puf-A forms sequence-independent interactions with DNA or RNA, mediated by conserved basic residues. We demonstrate that equivalent basic residues in yeast Puf6 are important for RNA binding, pre-rRNA processing, and mRNA localization. Finally, PUM repeats can be assembled into alternative folds that bind to structured nucleic acids in addition to forming canonical eight-repeat crescent-shaped RNA-binding domains found in classical PUF proteins.

Research Organization:
Yale Univ., New Haven, CT (United States). School of Medicine; National Inst. of Health, Research Triangle Park, NC (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States)
Grant/Contract Number:
AC02-05CH11231; W-31-109-Eng-38; GM52581
OSTI ID:
1170010
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, Issue 52; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
ENGLISH
Citation Metrics:
Cited by: 44 works
Citation information provided by
Web of Science

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Cited By (16)

Functions, mechanisms and regulation of Pumilio/Puf family RNA binding proteins: a comprehensive review journal October 2019
Nop9 is a PUF-like protein that prevents premature cleavage to correctly process pre-18S rRNA journal October 2016
Multiple Puf proteins regulate the stability of ribosome biogenesis transcripts journal September 2018
Nop9 binds the central pseudoknot region of 18S rRNA journal January 2017
Stepwise assembly of the earliest precursors of large ribosomal subunits in yeast journal April 2017
Distinct RNA-binding modules in a single PUF protein cooperate to determine RNA specificity journal July 2019
Structural and functional similarities and differences in nucleolar Pumilio RNA-binding proteins between Arabidopsis and the charophyte Chara corallina journal May 2020
The evolution of the Puf superfamily of proteins across the tree of eukaryotes journal June 2020
Puf3 participates in ribosomal biogenesis in malaria parasites journal February 2018
Functional association of Loc1 and Puf6 with RNA helicase Dhh1 in translational regulation of Saccharomyces cerevisiae Ste12 journal July 2019
Puf6 and Loc1 Are the Dedicated Chaperones of Ribosomal Protein Rpl43 in Saccharomyces cerevisiae journal November 2019
The molecular basis for ANE syndrome revealed by the large ribosomal subunit processome interactome journal April 2016
Structural and functional similarities and differences in nucleolar Pumilio RNA-binding proteins between Arabidopsis and the charophyte Chara corallina posted_content May 2020
Structural and functional similarities and differences in nucleolar Pumilio RNA-binding proteins between Arabidopsis and the charophyte Chara corallina journal May 2020
Identification and characterization of roles for Puf1 and Puf2 proteins in the yeast response to high calcium journal June 2017
Structural basis for the specific recognition of 18S rRNA by APUM23 journal October 2017