Home LiteratureArticle Details
PMID: 15337848 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Recruitment of the Puf3 protein to its mRNA target for regulation of mRNA decay in yeast.

RNA (New York, N.Y.) ·Vol. 10 ·No. 10 ·2004-10-00 ·Pages 1625-36

Jackson JS, Houshmandi SS, Lopez Leban F, Olivas WM

Abstract

The Puf family of RNA-binding proteins regulates mRNA translation and decay via interactions with 3' untranslated regions (3' UTRs) of target mRNAs. In yeast, Puf3p binds the 3' UTR of COX17 mRNA and promotes rapid deadenylation and decay. We have investigated the sequences required for Puf3p recruitment to this 3' UTR and have identified two separate binding sites. These sites are specific for Puf3p, as they cannot bind another Puf protein, Puf5p. Both sites use a conserved UGUANAUA sequence, whereas one site contains additional sequences that enhance binding affinity. In vivo, presence of either site partially stimulates COX17 mRNA decay, but full decay regulation requires the presence of both sites. No other sequences outside the 3' UTR are required to mediate this decay regulation. The Puf repeat domain of Puf3p is sufficient not only for in vitro binding to the 3' UTR, but also in vivo stimulation of COX17 mRNA decay. These experiments indicate that the essential residues involved in mRNA decay regulation are wholly contained within this RNA-binding domain.

MeSH Terms
3' Untranslated Regions Base Sequence Binding Sites/genetics Cation Transport Proteins/genetics,metabolism Copper Transport Proteins Molecular Chaperones Molecular Sequence Data RNA, Fungal/genetics,metabolism RNA, Messenger/genetics,metabolism RNA-Binding Proteins/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism
Chemicals
3' Untranslated Regions COX17 protein, S cerevisiae Cation Transport Proteins Copper Transport Proteins Molecular Chaperones RNA, Fungal RNA, Messenger RNA-Binding Proteins Saccharomyces cerevisiae Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Jackson John S
Department of Biology, University of Missouri-St. Louis, One University Boulevard, St. Louis, MO 63121-4499, USA.
Houshmandi S Sean
Lopez Leban Florencia
Olivas Wendy M
References (47)
47 references, click to expand
  1. Purification, characterization, and localization of yeast Cox17p, a mitochondrial copper shuttle.
    J Biol Chem. 1997 Dec 26;272(52):33191-6 PMID: 9407107
  2. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line.
    Nature. 1997 Dec 4;390(6659):477-84 PMID: 9393998
  3. The Pumilio RNA-binding domain is also a translational regulator.
    Mol Cell. 1998 May;1(6):863-72 PMID: 9660969
  4. The PUMILIO-RNA interaction: a single RNA-binding domain monomer recognizes a bipartite target sequence.
    Biochemistry. 1999 Jan 12;38(2):596-604 PMID: 9888799
  5. Control of translation initiation in animals.
    Annu Rev Cell Dev Biol. 1998;14:399-458 PMID: 9891789
  6. Starvation promotes Dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway.
    Development. 1999 Jun;126(14):3263-74 PMID: 10375515
  7. The Drosophila pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis and embryogenesis.
    Genetics. 1999 Sep;153(1):235-50 PMID: 10471709
  8. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans.
    Curr Biol. 1999 Sep 23;9(18):1009-18 PMID: 10508609
  9. The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins.
    RNA. 1997 Dec;3(12):1421-33 PMID: 9404893
  10. Recruitment of Nanos to hunchback mRNA by Pumilio.
    Genes Dev. 1999 Oct 15;13(20):2704-12 PMID: 10541556
  11. RNA-protein interactions in the control of stability and localization of messenger RNA (review).
    Int J Mol Med. 2000 Feb;5(2):111-23 PMID: 10639588
  12. Mechanisms and control of mRNA decapping in Saccharomyces cerevisiae.
    Annu Rev Biochem. 2000;69:571-95 PMID: 10966469
  13. The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast.
    EMBO J. 2000 Dec 1;19(23):6602-11 PMID: 11101532
  14. Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos.
    Nat Cell Biol. 1999 Nov;1(7):431-7 PMID: 10559987
  15. Post-transcriptional regulation through the HO 3'-UTR by Mpt5, a yeast homolog of Pumilio and FBF.
    EMBO J. 2001 Feb 1;20(3):552-61 PMID: 11157761
  16. Regulation of mRNA stability in mammalian cells.
    Gene. 2001 Mar 7;265(1-2):11-23 PMID: 11255003
  17. Drosophila Brain Tumor is a translational repressor.
    Genes Dev. 2001 Mar 15;15(6):762-73 PMID: 11274060
  18. A comprehensive two-hybrid analysis to explore the yeast protein interactome.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4569-74 PMID: 11283351
  19. Structure of Pumilio reveals similarity between RNA and peptide binding motifs.
    Cell. 2001 Apr 20;105(2):281-9 PMID: 11336677
  20. Crystal structure of a Pumilio homology domain.
    Mol Cell. 2001 Apr;7(4):855-65 PMID: 11336708
  21. Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein.
    J Biol Chem. 2001 Jun 15;276(24):20945-53 PMID: 11283000
  22. Poly(A)-independent regulation of maternal hunchback translation in the Drosophila embryo.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11359-64 PMID: 11562474
  23. Regulatory functions of 3'UTRs.
    Biochem Biophys Res Commun. 2001 Oct 26;288(2):291-5 PMID: 11606041
  24. PUM2, a novel murine puf protein, and its consensus RNA-binding site.
    RNA. 2001 Dec;7(12):1855-66 PMID: 11780640
  25. Functional organization of the yeast proteome by systematic analysis of protein complexes.
    Nature. 2002 Jan 10;415(6868):141-7 PMID: 11805826
  26. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry.
    Nature. 2002 Jan 10;415(6868):180-3 PMID: 11805837
  27. A PUF family portrait: 3'UTR regulation as a way of life.
    Trends Genet. 2002 Mar;18(3):150-7 PMID: 11858839
  28. An anterior function for the Drosophila posterior determinant Pumilio.
    Development. 2002 Jun;129(11):2699-710 PMID: 12015297
  29. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans.
    Nature. 2002 Jun 6;417(6889):660-3 PMID: 12050669
  30. Modular recognition of RNA by a human pumilio-homology domain.
    Cell. 2002 Aug 23;110(4):501-12 PMID: 12202039
  31. Pumilio homologue from saprolegnia parasitica specifically expressed in undifferentiated spore cysts.
    Eukaryot Cell. 2002 Feb;1(1):105-11 PMID: 12455976
  32. Translational control by the 3'-UTR: the ends specify the means.
    Trends Biochem Sci. 2003 Feb;28(2):91-8 PMID: 12575997
  33. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast.
    PLoS Biol. 2004 Mar;2(3):E79 PMID: 15024427
  34. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth.
    Mol Cell Biol. 1989 Aug;9(8):3260-8 PMID: 2477683
  35. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 May;10(5):2269-84 PMID: 2183028
  36. RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos.
    Cell. 1991 Nov 29;67(5):955-67 PMID: 1720354
  37. Yeast cells lacking 5'-->3' exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5' cap structure.
    Mol Cell Biol. 1993 Aug;13(8):4826-35 PMID: 8336719
  38. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation.
    Genes Dev. 1993 Aug;7(8):1632-43 PMID: 8393418
  39. A small segment of the MAT alpha 1 transcript promotes mRNA decay in Saccharomyces cerevisiae: a stimulatory role for rare codons.
    Mol Cell Biol. 1993 Sep;13(9):5141-8 PMID: 8355674
  40. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5'-->3' digestion of the transcript.
    Genes Dev. 1994 Apr 1;8(7):855-66 PMID: 7926773
  41. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos.
    Cell. 1995 Mar 10;80(5):747-56 PMID: 7889568
  42. Turnover mechanisms of the stable yeast PGK1 mRNA.
    Mol Cell Biol. 1995 Apr;15(4):2145-56 PMID: 7891709
  43. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells.
    Annu Rev Biochem. 1996;65:693-739 PMID: 8811193
  44. Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Oct;16(10):5830-8 PMID: 8816497
  45. A CCHC metal-binding domain in Nanos is essential for translational regulation.
    EMBO J. 1997 Feb 17;16(4):834-43 PMID: 9049312
  46. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA.
    Development. 1997 Aug;124(15):3015-23 PMID: 9247343
  47. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells.
    Development. 1998 Feb;125(4):679-90 PMID: 9435288
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1355-8382
Published
2004-10-00
Epub
2004-00-30
Pages
1625-36
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC1370648
Subset
IM
Grants
NIGMS NIH HHS · R01 GM063759 · United States
NIGMS NIH HHS · GM63759 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]