Three-layered control of mRNA poly(A) tail synthesis in Saccharomyces cerevisiae

Matti Turtola; Cemre M. Manav; Ananthanarayanan Kumar; Agnieszka Tudek; Seweryn Mroczek; Pawel S. Krawczyk; Andrzej Dziembowski; Manfred Schmid; Lori A. Passmore; Ana Casanal; Torben Heick Jensen

doi:10.1101/GAD.348634.121

Three-layered control of mRNA poly(A) tail synthesis in Saccharomyces cerevisiae

Matti Turtola
, Cemre M. Manav
, Ananthanarayanan Kumar
, Agnieszka Tudek
, Seweryn Mroczek
, Pawel S. Krawczyk
, Andrzej Dziembowski
, Manfred Schmid
, Lori A. Passmore
, Ana Casanal
, Torben Heick Jensen^*

^*Corresponding author af dette arbejde

Institut for Molekylærbiologi og Genetik - RNA-biologi og -innovation

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

13 Citationer (Scopus)

57 Downloads (Pure)

Abstract

Biogenesis of most eukaryotic mRNAs involves the addition of an untemplated polyadenosine (pA) tail by the cleavage and polyadenylation machinery. The pA tail, and its exact length, impacts mRNA stability, nuclear export, and translation.To define how polyadenylation is controlled in S. cerevisiae, we have used an in vivo assay capable of assessing nuclear pA tail synthesis, analyzed tail length distributions by direct RNA sequencing, and reconstituted polyadenylation reactions with purified components. This revealed three control mechanisms for pA tail length. First, we found that the pA binding protein (PABP) Nab2p is the primary regulator of pA tail length. Second, when Nab2p is limiting, the nuclear pool of Pab1p, the second major PABP in yeast, controls the process. Third, when both PABPs are absent, the cleavage and polyadenylation factor (CPF) limits pA tail synthesis. Thus, Pab1p and CPF provide fail-safe mechanisms to a primary Nab2p-dependent pathway, thereby preventing uncontrolled polyadenylation and allowing mRNA export and translation.

Originalsprog	Engelsk
Tidsskrift	Genes and Development
Vol/bind	35
Nummer	17-18
Sider (fra-til)	1290-1303
Antal sider	14
ISSN	0890-9369
DOI	https://doi.org/10.1101/GAD.348634.121
Status	Udgivet - sep. 2021

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10.1101/GAD.348634.121Licens: CC BY-NC

Genes Dev.-2021-Turtola-1290-303Forlagets udgivne version, 5,66 MBLicens: CC BY-NC

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title = "Three-layered control of mRNA poly(A) tail synthesis in Saccharomyces cerevisiae",

abstract = "Biogenesis of most eukaryotic mRNAs involves the addition of an untemplated polyadenosine (pA) tail by the cleavage and polyadenylation machinery. The pA tail, and its exact length, impacts mRNA stability, nuclear export, and translation.To define how polyadenylation is controlled in S. cerevisiae, we have used an in vivo assay capable of assessing nuclear pA tail synthesis, analyzed tail length distributions by direct RNA sequencing, and reconstituted polyadenylation reactions with purified components. This revealed three control mechanisms for pA tail length. First, we found that the pA binding protein (PABP) Nab2p is the primary regulator of pA tail length. Second, when Nab2p is limiting, the nuclear pool of Pab1p, the second major PABP in yeast, controls the process. Third, when both PABPs are absent, the cleavage and polyadenylation factor (CPF) limits pA tail synthesis. Thus, Pab1p and CPF provide fail-safe mechanisms to a primary Nab2p-dependent pathway, thereby preventing uncontrolled polyadenylation and allowing mRNA export and translation.",

keywords = "Cleavage and polyadenylation factor, MRNA nuclear export, Nab2p, Pab1p, Poly(A) binding protein, Poly(A) tail length, Polyadenylation",

author = "Matti Turtola and Manav, \{Cemre M.\} and Ananthanarayanan Kumar and Agnieszka Tudek and Seweryn Mroczek and Krawczyk, \{Pawel S.\} and Andrzej Dziembowski and Manfred Schmid and Passmore, \{Lori A.\} and Ana Casanal and Jensen, \{Torben Heick\}",

year = "2021",

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doi = "10.1101/GAD.348634.121",

language = "English",

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pages = "1290--1303",

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T1 - Three-layered control of mRNA poly(A) tail synthesis in Saccharomyces cerevisiae

AU - Turtola, Matti

AU - Manav, Cemre M.

AU - Kumar, Ananthanarayanan

AU - Tudek, Agnieszka

AU - Mroczek, Seweryn

AU - Krawczyk, Pawel S.

AU - Dziembowski, Andrzej

AU - Schmid, Manfred

AU - Passmore, Lori A.

AU - Casanal, Ana

AU - Jensen, Torben Heick

PY - 2021/9

Y1 - 2021/9

N2 - Biogenesis of most eukaryotic mRNAs involves the addition of an untemplated polyadenosine (pA) tail by the cleavage and polyadenylation machinery. The pA tail, and its exact length, impacts mRNA stability, nuclear export, and translation.To define how polyadenylation is controlled in S. cerevisiae, we have used an in vivo assay capable of assessing nuclear pA tail synthesis, analyzed tail length distributions by direct RNA sequencing, and reconstituted polyadenylation reactions with purified components. This revealed three control mechanisms for pA tail length. First, we found that the pA binding protein (PABP) Nab2p is the primary regulator of pA tail length. Second, when Nab2p is limiting, the nuclear pool of Pab1p, the second major PABP in yeast, controls the process. Third, when both PABPs are absent, the cleavage and polyadenylation factor (CPF) limits pA tail synthesis. Thus, Pab1p and CPF provide fail-safe mechanisms to a primary Nab2p-dependent pathway, thereby preventing uncontrolled polyadenylation and allowing mRNA export and translation.

AB - Biogenesis of most eukaryotic mRNAs involves the addition of an untemplated polyadenosine (pA) tail by the cleavage and polyadenylation machinery. The pA tail, and its exact length, impacts mRNA stability, nuclear export, and translation.To define how polyadenylation is controlled in S. cerevisiae, we have used an in vivo assay capable of assessing nuclear pA tail synthesis, analyzed tail length distributions by direct RNA sequencing, and reconstituted polyadenylation reactions with purified components. This revealed three control mechanisms for pA tail length. First, we found that the pA binding protein (PABP) Nab2p is the primary regulator of pA tail length. Second, when Nab2p is limiting, the nuclear pool of Pab1p, the second major PABP in yeast, controls the process. Third, when both PABPs are absent, the cleavage and polyadenylation factor (CPF) limits pA tail synthesis. Thus, Pab1p and CPF provide fail-safe mechanisms to a primary Nab2p-dependent pathway, thereby preventing uncontrolled polyadenylation and allowing mRNA export and translation.

KW - Cleavage and polyadenylation factor

KW - MRNA nuclear export

KW - Nab2p

KW - Pab1p

KW - Poly(A) binding protein

KW - Poly(A) tail length

KW - Polyadenylation

UR - https://www.scopus.com/pages/publications/85115085212

U2 - 10.1101/GAD.348634.121

DO - 10.1101/GAD.348634.121

M3 - Journal article

C2 - 34385261

AN - SCOPUS:85115085212

SN - 0890-9369

VL - 35

SP - 1290

EP - 1303

JO - Genes and Development

JF - Genes and Development

IS - 17-18

ER -

Three-layered control of mRNA poly(A) tail synthesis in Saccharomyces cerevisiae

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