The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation
Cyclins are a family of proteins characterized by possessing a cyclin box domain that mediates binding to cyclin dependent kinases (CDKs) partners. In this study, the search for a partner cyclin of the PHO85-1 CDK retrieved PCL-1 an ortholog of yeast Pcls (for Pho85 cyclins) that performs functions...
Main Authors: | , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2022-12-01
|
Series: | Frontiers in Microbiology |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1078972/full |
_version_ | 1828088920458395648 |
---|---|
author | Jonatas Erick Maimoni Campanella Thiago de Souza Candido Luiz Carlos Bertucci Barbosa Antoniel Augusto Severo Gomes Carla Andréa Leite Erika Silva Higashi Paula Aboud Barbugli Marcos Roberto de Matos Fontes Maria Célia Bertolini |
author_facet | Jonatas Erick Maimoni Campanella Thiago de Souza Candido Luiz Carlos Bertucci Barbosa Antoniel Augusto Severo Gomes Carla Andréa Leite Erika Silva Higashi Paula Aboud Barbugli Marcos Roberto de Matos Fontes Maria Célia Bertolini |
author_sort | Jonatas Erick Maimoni Campanella |
collection | DOAJ |
description | Cyclins are a family of proteins characterized by possessing a cyclin box domain that mediates binding to cyclin dependent kinases (CDKs) partners. In this study, the search for a partner cyclin of the PHO85-1 CDK retrieved PCL-1 an ortholog of yeast Pcls (for Pho85 cyclins) that performs functions common to Pcls belonging to different cyclin families. We show here that PCL-1, as a typical cyclin, is involved in cell cycle control and cell progression. In addition, PCL-1 regulates glycogen metabolism; Δpcl-1 cells accumulate higher glycogen levels than wild-type cells and the glycogen synthase (GSN) enzyme is less phosphorylated and, therefore, more active in the mutant cells. Together with PHO85-1, PCL-1 phosphorylates in vitro GSN at the Ser636 amino acid residue. Modeling studies identified PHO85-1 and PCL-1 as a CDK/cyclin complex, with a conserved intermolecular region stabilized by hydrophobic and polar interactions. PCL-1 is also involved in calcium and NaCl stress response. Δpcl-1 cells are sensitive to high NaCl concentration; on the contrary, they grow better and overexpress calcium responsive genes under high calcium chloride concentration compared to the wild-type strain. The expression of the calcium-responsive CRZ-1 transcription factor is modulated by PCL-1, and this transcription factor seems to be less phosphorylated in Δpcl-1 cells since exhibits nuclear location in these cells in the absence of calcium. Our results show that PCL-1 locates at different cell regions suggesting that it may determine its activity by controlling its intracellular location and reveal an interesting functional divergence between yeast and filamentous fungus cyclins. |
first_indexed | 2024-04-11T05:32:42Z |
format | Article |
id | doaj.art-9ed1ff6e2acf40908de6ff0e1338740a |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-04-11T05:32:42Z |
publishDate | 2022-12-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Microbiology |
spelling | doaj.art-9ed1ff6e2acf40908de6ff0e1338740a2022-12-22T16:42:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-12-011310.3389/fmicb.2022.10789721078972The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulationJonatas Erick Maimoni Campanella0Thiago de Souza Candido1Luiz Carlos Bertucci Barbosa2Antoniel Augusto Severo Gomes3Carla Andréa Leite4Erika Silva Higashi5Paula Aboud Barbugli6Marcos Roberto de Matos Fontes7Maria Célia Bertolini8Departamento de Bioquímica e Química Orgânica, Instituto de Química, Universidade Estadual Paulista, Araraquara, São Paulo, BrazilDepartamento de Bioquímica e Química Orgânica, Instituto de Química, Universidade Estadual Paulista, Araraquara, São Paulo, BrazilDepartamento de Bioquímica e Química Orgânica, Instituto de Química, Universidade Estadual Paulista, Araraquara, São Paulo, BrazilDepartamento de Biofísica e Farmacologia, Instituto de Biociências, Universidade Estadual Paulista, Botucatu, São Paulo, BrazilDepartamento de Bioquímica e Química Orgânica, Instituto de Química, Universidade Estadual Paulista, Araraquara, São Paulo, BrazilDepartamento de Bioquímica e Química Orgânica, Instituto de Química, Universidade Estadual Paulista, Araraquara, São Paulo, BrazilDepartamento de Materiais Dentários e Prótese, Faculdade de Odontologia, Universidade Estadual Paulista, Araraquara, São Paulo, BrazilDepartamento de Biofísica e Farmacologia, Instituto de Biociências, Universidade Estadual Paulista, Botucatu, São Paulo, BrazilDepartamento de Bioquímica e Química Orgânica, Instituto de Química, Universidade Estadual Paulista, Araraquara, São Paulo, BrazilCyclins are a family of proteins characterized by possessing a cyclin box domain that mediates binding to cyclin dependent kinases (CDKs) partners. In this study, the search for a partner cyclin of the PHO85-1 CDK retrieved PCL-1 an ortholog of yeast Pcls (for Pho85 cyclins) that performs functions common to Pcls belonging to different cyclin families. We show here that PCL-1, as a typical cyclin, is involved in cell cycle control and cell progression. In addition, PCL-1 regulates glycogen metabolism; Δpcl-1 cells accumulate higher glycogen levels than wild-type cells and the glycogen synthase (GSN) enzyme is less phosphorylated and, therefore, more active in the mutant cells. Together with PHO85-1, PCL-1 phosphorylates in vitro GSN at the Ser636 amino acid residue. Modeling studies identified PHO85-1 and PCL-1 as a CDK/cyclin complex, with a conserved intermolecular region stabilized by hydrophobic and polar interactions. PCL-1 is also involved in calcium and NaCl stress response. Δpcl-1 cells are sensitive to high NaCl concentration; on the contrary, they grow better and overexpress calcium responsive genes under high calcium chloride concentration compared to the wild-type strain. The expression of the calcium-responsive CRZ-1 transcription factor is modulated by PCL-1, and this transcription factor seems to be less phosphorylated in Δpcl-1 cells since exhibits nuclear location in these cells in the absence of calcium. Our results show that PCL-1 locates at different cell regions suggesting that it may determine its activity by controlling its intracellular location and reveal an interesting functional divergence between yeast and filamentous fungus cyclins.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1078972/fullCDK/cyclin complexprotein phosphorylationstress responseCRZ-1 transcription factorNeurospora crassa |
spellingShingle | Jonatas Erick Maimoni Campanella Thiago de Souza Candido Luiz Carlos Bertucci Barbosa Antoniel Augusto Severo Gomes Carla Andréa Leite Erika Silva Higashi Paula Aboud Barbugli Marcos Roberto de Matos Fontes Maria Célia Bertolini The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation Frontiers in Microbiology CDK/cyclin complex protein phosphorylation stress response CRZ-1 transcription factor Neurospora crassa |
title | The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation |
title_full | The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation |
title_fullStr | The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation |
title_full_unstemmed | The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation |
title_short | The Neurospora crassa PCL-1 cyclin is a PHO85-1 (PGOV) kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation |
title_sort | neurospora crassa pcl 1 cyclin is a pho85 1 pgov kinase partner that directs the complex to glycogen metabolism and is involved in calcium metabolism regulation |
topic | CDK/cyclin complex protein phosphorylation stress response CRZ-1 transcription factor Neurospora crassa |
url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.1078972/full |
work_keys_str_mv | AT jonataserickmaimonicampanella theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT thiagodesouzacandido theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT luizcarlosbertuccibarbosa theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT antonielaugustoseverogomes theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT carlaandrealeite theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT erikasilvahigashi theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT paulaaboudbarbugli theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT marcosrobertodematosfontes theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT mariaceliabertolini theneurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT jonataserickmaimonicampanella neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT thiagodesouzacandido neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT luizcarlosbertuccibarbosa neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT antonielaugustoseverogomes neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT carlaandrealeite neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT erikasilvahigashi neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT paulaaboudbarbugli neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT marcosrobertodematosfontes neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation AT mariaceliabertolini neurosporacrassapcl1cyclinisapho851pgovkinasepartnerthatdirectsthecomplextoglycogenmetabolismandisinvolvedincalciummetabolismregulation |