The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities

Cristina Molero, Katalin Petrényi, Asier González, Mercè Carmona, Samuel Gelis, J. Albert Abrie, Erick Strauss, José Ramos, V. Dombrádi, Elena Hidalgo, Joaquín Ariño

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Summary: Saccharomyces cerevisiaeHal3 and Vhs3 are moonlighting proteins, forming an atypical heterotrimeric decarboxylase (PPCDC) required for CoA biosynthesis, and regulating cation homeostasis by inhibition of the Ppz1 phosphatase. The Schizosaccharomyces pombeORF SPAC15E1.04 (renamed as Sphal3) encodes a protein whose amino-terminal half is similar to Sc Hal3 whereas its carboxyl-terminal half is related to thymidylate synthase (TS). We show that SpHal3 and/or its N-terminal domain retain the ability to bind to and modestly inhibit in vitro S.cerevisiaePpz1 as well as its S.pombe homolog Pzh1, and also exhibit PPCDC activity in vitro and provide PPCDC function in vivo, indicating that SpHal3 is a monogenic PPCDC in fission yeast. Whereas the Sp Hal3 N-terminal domain partially mimics Sc Hal3 functions, the entire protein and its carboxyl-terminal domain rescue the S.cerevisiaecdc21 mutant, thus proving TS function. Additionally, we show that the 70kDa Sp Hal3 protein is not proteolytically processed under diverse forms of stress and that, as predicted, Sphal3 is an essential gene. Therefore, Sphal3 represents a fusion event that joined three different functional activities in the same gene. The possible advantage derived from this surprising combination of essential proteins is discussed.

Original languageEnglish
Pages (from-to)367-382
Number of pages16
JournalMolecular Microbiology
Volume90
Issue number2
DOIs
Publication statusPublished - Oct 2013

Fingerprint

Schizosaccharomyces
Gene Fusion
Thymidylate Synthase
Proteins
Saccharomyces
Carboxy-Lyases
Essential Genes
Coenzyme A
Phosphoric Monoester Hydrolases
Cations
Homeostasis
Genes
In Vitro Techniques

ASJC Scopus subject areas

  • Molecular Biology
  • Microbiology

Cite this

Molero, C., Petrényi, K., González, A., Carmona, M., Gelis, S., Abrie, J. A., ... Ariño, J. (2013). The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities. Molecular Microbiology, 90(2), 367-382. https://doi.org/10.1111/mmi.12370

The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities. / Molero, Cristina; Petrényi, Katalin; González, Asier; Carmona, Mercè; Gelis, Samuel; Abrie, J. Albert; Strauss, Erick; Ramos, José; Dombrádi, V.; Hidalgo, Elena; Ariño, Joaquín.

In: Molecular Microbiology, Vol. 90, No. 2, 10.2013, p. 367-382.

Research output: Contribution to journalArticle

Molero, C, Petrényi, K, González, A, Carmona, M, Gelis, S, Abrie, JA, Strauss, E, Ramos, J, Dombrádi, V, Hidalgo, E & Ariño, J 2013, 'The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities', Molecular Microbiology, vol. 90, no. 2, pp. 367-382. https://doi.org/10.1111/mmi.12370
Molero C, Petrényi K, González A, Carmona M, Gelis S, Abrie JA et al. The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities. Molecular Microbiology. 2013 Oct;90(2):367-382. https://doi.org/10.1111/mmi.12370
Molero, Cristina ; Petrényi, Katalin ; González, Asier ; Carmona, Mercè ; Gelis, Samuel ; Abrie, J. Albert ; Strauss, Erick ; Ramos, José ; Dombrádi, V. ; Hidalgo, Elena ; Ariño, Joaquín. / The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities. In: Molecular Microbiology. 2013 ; Vol. 90, No. 2. pp. 367-382.
@article{7cf819aee82440e2918d2dd24a68414c,
title = "The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities",
abstract = "Summary: Saccharomyces cerevisiaeHal3 and Vhs3 are moonlighting proteins, forming an atypical heterotrimeric decarboxylase (PPCDC) required for CoA biosynthesis, and regulating cation homeostasis by inhibition of the Ppz1 phosphatase. The Schizosaccharomyces pombeORF SPAC15E1.04 (renamed as Sphal3) encodes a protein whose amino-terminal half is similar to Sc Hal3 whereas its carboxyl-terminal half is related to thymidylate synthase (TS). We show that SpHal3 and/or its N-terminal domain retain the ability to bind to and modestly inhibit in vitro S.cerevisiaePpz1 as well as its S.pombe homolog Pzh1, and also exhibit PPCDC activity in vitro and provide PPCDC function in vivo, indicating that SpHal3 is a monogenic PPCDC in fission yeast. Whereas the Sp Hal3 N-terminal domain partially mimics Sc Hal3 functions, the entire protein and its carboxyl-terminal domain rescue the S.cerevisiaecdc21 mutant, thus proving TS function. Additionally, we show that the 70kDa Sp Hal3 protein is not proteolytically processed under diverse forms of stress and that, as predicted, Sphal3 is an essential gene. Therefore, Sphal3 represents a fusion event that joined three different functional activities in the same gene. The possible advantage derived from this surprising combination of essential proteins is discussed.",
author = "Cristina Molero and Katalin Petr{\'e}nyi and Asier Gonz{\'a}lez and Merc{\`e} Carmona and Samuel Gelis and Abrie, {J. Albert} and Erick Strauss and Jos{\'e} Ramos and V. Dombr{\'a}di and Elena Hidalgo and Joaqu{\'i}n Ari{\~n}o",
year = "2013",
month = "10",
doi = "10.1111/mmi.12370",
language = "English",
volume = "90",
pages = "367--382",
journal = "Molecular Microbiology",
issn = "0950-382X",
publisher = "Wiley-Blackwell",
number = "2",

}

TY - JOUR

T1 - The Schizosaccharomyces pombe fusion gene hal3 encodes three distinct activities

AU - Molero, Cristina

AU - Petrényi, Katalin

AU - González, Asier

AU - Carmona, Mercè

AU - Gelis, Samuel

AU - Abrie, J. Albert

AU - Strauss, Erick

AU - Ramos, José

AU - Dombrádi, V.

AU - Hidalgo, Elena

AU - Ariño, Joaquín

PY - 2013/10

Y1 - 2013/10

N2 - Summary: Saccharomyces cerevisiaeHal3 and Vhs3 are moonlighting proteins, forming an atypical heterotrimeric decarboxylase (PPCDC) required for CoA biosynthesis, and regulating cation homeostasis by inhibition of the Ppz1 phosphatase. The Schizosaccharomyces pombeORF SPAC15E1.04 (renamed as Sphal3) encodes a protein whose amino-terminal half is similar to Sc Hal3 whereas its carboxyl-terminal half is related to thymidylate synthase (TS). We show that SpHal3 and/or its N-terminal domain retain the ability to bind to and modestly inhibit in vitro S.cerevisiaePpz1 as well as its S.pombe homolog Pzh1, and also exhibit PPCDC activity in vitro and provide PPCDC function in vivo, indicating that SpHal3 is a monogenic PPCDC in fission yeast. Whereas the Sp Hal3 N-terminal domain partially mimics Sc Hal3 functions, the entire protein and its carboxyl-terminal domain rescue the S.cerevisiaecdc21 mutant, thus proving TS function. Additionally, we show that the 70kDa Sp Hal3 protein is not proteolytically processed under diverse forms of stress and that, as predicted, Sphal3 is an essential gene. Therefore, Sphal3 represents a fusion event that joined three different functional activities in the same gene. The possible advantage derived from this surprising combination of essential proteins is discussed.

AB - Summary: Saccharomyces cerevisiaeHal3 and Vhs3 are moonlighting proteins, forming an atypical heterotrimeric decarboxylase (PPCDC) required for CoA biosynthesis, and regulating cation homeostasis by inhibition of the Ppz1 phosphatase. The Schizosaccharomyces pombeORF SPAC15E1.04 (renamed as Sphal3) encodes a protein whose amino-terminal half is similar to Sc Hal3 whereas its carboxyl-terminal half is related to thymidylate synthase (TS). We show that SpHal3 and/or its N-terminal domain retain the ability to bind to and modestly inhibit in vitro S.cerevisiaePpz1 as well as its S.pombe homolog Pzh1, and also exhibit PPCDC activity in vitro and provide PPCDC function in vivo, indicating that SpHal3 is a monogenic PPCDC in fission yeast. Whereas the Sp Hal3 N-terminal domain partially mimics Sc Hal3 functions, the entire protein and its carboxyl-terminal domain rescue the S.cerevisiaecdc21 mutant, thus proving TS function. Additionally, we show that the 70kDa Sp Hal3 protein is not proteolytically processed under diverse forms of stress and that, as predicted, Sphal3 is an essential gene. Therefore, Sphal3 represents a fusion event that joined three different functional activities in the same gene. The possible advantage derived from this surprising combination of essential proteins is discussed.

UR - http://www.scopus.com/inward/record.url?scp=84885379613&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84885379613&partnerID=8YFLogxK

U2 - 10.1111/mmi.12370

DO - 10.1111/mmi.12370

M3 - Article

C2 - 23962284

AN - SCOPUS:84885379613

VL - 90

SP - 367

EP - 382

JO - Molecular Microbiology

JF - Molecular Microbiology

SN - 0950-382X

IS - 2

ER -