Cargando…

Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi

Protein prenylation is a crucial post-translational modification largely mediated by two heterodimeric enzyme complexes, farnesyltransferase and geranylgeranyltransferase type-I (GGTase-I), each composed of a shared α-subunit and a unique β-subunit. GGTase-I enzymes are validated drug targets that c...

Descripción completa

Detalles Bibliográficos
Autores principales: Souza, Ana Camila Oliveira, Al Abdallah, Qusai, DeJarnette, Kaci, Martin-Vicente, Adela, Nywening, Ashley V., DeJarnette, Christian, Sansevere, Emily A., Ge, Wenbo, Palmer, Glen E., Fortwendel, Jarrod R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6550545/
https://www.ncbi.nlm.nih.gov/pubmed/31131706
http://dx.doi.org/10.1080/21505594.2019.1620063
_version_ 1783424203560583168
author Souza, Ana Camila Oliveira
Al Abdallah, Qusai
DeJarnette, Kaci
Martin-Vicente, Adela
Nywening, Ashley V.
DeJarnette, Christian
Sansevere, Emily A.
Ge, Wenbo
Palmer, Glen E.
Fortwendel, Jarrod R
author_facet Souza, Ana Camila Oliveira
Al Abdallah, Qusai
DeJarnette, Kaci
Martin-Vicente, Adela
Nywening, Ashley V.
DeJarnette, Christian
Sansevere, Emily A.
Ge, Wenbo
Palmer, Glen E.
Fortwendel, Jarrod R
author_sort Souza, Ana Camila Oliveira
collection PubMed
description Protein prenylation is a crucial post-translational modification largely mediated by two heterodimeric enzyme complexes, farnesyltransferase and geranylgeranyltransferase type-I (GGTase-I), each composed of a shared α-subunit and a unique β-subunit. GGTase-I enzymes are validated drug targets that contribute to virulence in Cryptococcus neoformans and to the yeast-to-hyphal transition in Candida albicans. Therefore, we sought to investigate the importance of the α-subunit, RamB, and the β-subunit, Cdc43, of the A. fumigatus GGTase-I complex to hyphal growth and virulence. Deletion of cdc43 resulted in impaired hyphal morphogenesis and thermo-sensitivity, which was exacerbated during growth in rich media. The Δcdc43 mutant also displayed hypersensitivity to cell wall stress agents and to cell wall synthesis inhibitors, suggesting alterations of cell wall biosynthesis or stress signaling. In support of this, analyses of cell wall content revealed decreased amounts of β-glucan in the Δcdc43 strain. Despite strong in vitro phenotypes, the Δcdc43 mutant was fully virulent in two models of murine invasive aspergillosis, similar to the control strain. We further found that a strain expressing the α-subunit gene, ramB, from a tetracycline-inducible promoter was inviable under non-inducing in vitro growth conditions and was virtually avirulent in both mouse models. Lastly, virulence studies using C. albicans strains with tetracycline-repressible RAM2 or CDC43 expression revealed reduced pathogenicity associated with downregulation of either gene in a murine model of disseminated infection. Together, these findings indicate a differential requirement for protein geranylgeranylation for fungal virulence, and further inform the selection of specific prenyltransferases as promising antifungal drug targets for each pathogen.
format Online
Article
Text
id pubmed-6550545
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Taylor & Francis
record_format MEDLINE/PubMed
spelling pubmed-65505452019-06-17 Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi Souza, Ana Camila Oliveira Al Abdallah, Qusai DeJarnette, Kaci Martin-Vicente, Adela Nywening, Ashley V. DeJarnette, Christian Sansevere, Emily A. Ge, Wenbo Palmer, Glen E. Fortwendel, Jarrod R Virulence Research Paper Protein prenylation is a crucial post-translational modification largely mediated by two heterodimeric enzyme complexes, farnesyltransferase and geranylgeranyltransferase type-I (GGTase-I), each composed of a shared α-subunit and a unique β-subunit. GGTase-I enzymes are validated drug targets that contribute to virulence in Cryptococcus neoformans and to the yeast-to-hyphal transition in Candida albicans. Therefore, we sought to investigate the importance of the α-subunit, RamB, and the β-subunit, Cdc43, of the A. fumigatus GGTase-I complex to hyphal growth and virulence. Deletion of cdc43 resulted in impaired hyphal morphogenesis and thermo-sensitivity, which was exacerbated during growth in rich media. The Δcdc43 mutant also displayed hypersensitivity to cell wall stress agents and to cell wall synthesis inhibitors, suggesting alterations of cell wall biosynthesis or stress signaling. In support of this, analyses of cell wall content revealed decreased amounts of β-glucan in the Δcdc43 strain. Despite strong in vitro phenotypes, the Δcdc43 mutant was fully virulent in two models of murine invasive aspergillosis, similar to the control strain. We further found that a strain expressing the α-subunit gene, ramB, from a tetracycline-inducible promoter was inviable under non-inducing in vitro growth conditions and was virtually avirulent in both mouse models. Lastly, virulence studies using C. albicans strains with tetracycline-repressible RAM2 or CDC43 expression revealed reduced pathogenicity associated with downregulation of either gene in a murine model of disseminated infection. Together, these findings indicate a differential requirement for protein geranylgeranylation for fungal virulence, and further inform the selection of specific prenyltransferases as promising antifungal drug targets for each pathogen. Taylor & Francis 2019-05-25 /pmc/articles/PMC6550545/ /pubmed/31131706 http://dx.doi.org/10.1080/21505594.2019.1620063 Text en © 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Paper
Souza, Ana Camila Oliveira
Al Abdallah, Qusai
DeJarnette, Kaci
Martin-Vicente, Adela
Nywening, Ashley V.
DeJarnette, Christian
Sansevere, Emily A.
Ge, Wenbo
Palmer, Glen E.
Fortwendel, Jarrod R
Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi
title Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi
title_full Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi
title_fullStr Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi
title_full_unstemmed Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi
title_short Differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi
title_sort differential requirements of protein geranylgeranylation for the virulence of human pathogenic fungi
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6550545/
https://www.ncbi.nlm.nih.gov/pubmed/31131706
http://dx.doi.org/10.1080/21505594.2019.1620063
work_keys_str_mv AT souzaanacamilaoliveira differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT alabdallahqusai differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT dejarnettekaci differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT martinvicenteadela differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT nyweningashleyv differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT dejarnettechristian differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT sansevereemilya differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT gewenbo differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT palmerglene differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi
AT fortwendeljarrodr differentialrequirementsofproteingeranylgeranylationforthevirulenceofhumanpathogenicfungi