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Mms21: A Putative SUMO E3 Ligase in Candida albicans That Negatively Regulates Invasiveness and Filamentation, and Is Required for the Genotoxic and Cellular Stress Response

Amjad Islam, Faiza Tebbji, Jaideep Mallick, Hannah Regan, Vanessa Dumeaux, Raha Parvizi Omran and Malcolm Whiteway
Genetics February 1, 2019 vol. 211 no. 2 579-595; https://doi.org/10.1534/genetics.118.301769
Amjad Islam
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Faiza Tebbji
Infectious Centre de Recherche en Infectiologie (CRI), Centre Hospitalier Universitaire de Quebec (CHUQ) Research Center, University Laval, Quebec City, Quebec G1V 4G2, Canada
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Jaideep Mallick
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Hannah Regan
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Vanessa Dumeaux
Prevention Evaluation Rehabilitation Formation (PERFORM) Centre, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Raha Parvizi Omran
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Malcolm Whiteway
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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  • For correspondence: malcolm.whiteway@concordia.ca
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Abstract

In the life cycle of the fungal pathogen Candida albicans, the formation of filamentous cells is a differentiation process that is critically involved in host tissue invasion, and in adaptation to host cell and environmental stresses. Here, we have used the Gene Replacement And Conditional Expression library to identify genes controlling invasiveness and filamentation; conditional repression of the library revealed 69 mutants that triggered these processes. Intriguingly, the genes encoding the small ubiquitin-like modifier (SUMO) E3 ligase Mms21, and all other tested members of the sumoylation pathway, were both nonessential and capable of triggering filamentation upon repression, suggesting an important role for sumoylation in controlling filamentation in C. albicans. We have investigated Mms21 in detail. Both Mms21 nulls (mms21Δ/Δ) and SP [Siz/Pias (protein inhibitor of activated signal transducer and activator of transcription)] domain (SUMO E3 ligase domain)-deleted mutants displayed invasiveness, filamentation, and abnormal nuclear segregation; filament formation occurred even in the absence of the hyphal transcription factor Efg1. Transcriptional analysis of mms21Δ/Δ showed an increase in expression from two- to eightfold above that of the wild-type for hyphal-specific genes, including ECE1, PGA13, PGA26, HWP1, ALS1, ALS3, SOD4, SOD5, UME6, and HGC1. The Mms21-deleted mutants were unable to recover from DNA-damaging agents like methyl methane sulfonate, hydroxyurea, hydrogen peroxide, and UV radiation, suggesting that the protein is important for genotoxic stress responses. In addition, the mms21Δ/Δ mutant displayed sensitivity to cell wall and thermal stresses, and to different antifungal drugs. All these findings suggest that Mms21 plays important roles in cellular differentiation, DNA damage and cellular stress responses, and in response to antifungal drugs.

  • Candida albicans
  • filamentation
  • Mms21
  • stress response
  • sumoylation
  • Received October 18, 2018.
  • Accepted November 28, 2018.
  • Copyright © 2019 by the Genetics Society of America
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Volume 211 Issue 2, February 2019

Genetics: 211 (2)

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Cellular genetics
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Mms21: A Putative SUMO E3 Ligase in Candida albicans That Negatively Regulates Invasiveness and Filamentation, and Is Required for the Genotoxic and Cellular Stress Response

Amjad Islam, Faiza Tebbji, Jaideep Mallick, Hannah Regan, Vanessa Dumeaux, Raha Parvizi Omran and Malcolm Whiteway
Genetics February 1, 2019 vol. 211 no. 2 579-595; https://doi.org/10.1534/genetics.118.301769
Amjad Islam
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Faiza Tebbji
Infectious Centre de Recherche en Infectiologie (CRI), Centre Hospitalier Universitaire de Quebec (CHUQ) Research Center, University Laval, Quebec City, Quebec G1V 4G2, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
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Jaideep Mallick
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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  • Search for this author on this site
Hannah Regan
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Vanessa Dumeaux
Prevention Evaluation Rehabilitation Formation (PERFORM) Centre, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Raha Parvizi Omran
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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Malcolm Whiteway
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
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  • For correspondence: malcolm.whiteway@concordia.ca
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Citation

Mms21: A Putative SUMO E3 Ligase in Candida albicans That Negatively Regulates Invasiveness and Filamentation, and Is Required for the Genotoxic and Cellular Stress Response

Amjad Islam, Faiza Tebbji, Jaideep Mallick, Hannah Regan, Vanessa Dumeaux, Raha Parvizi Omran and Malcolm Whiteway
Genetics February 1, 2019 vol. 211 no. 2 579-595; https://doi.org/10.1534/genetics.118.301769
Amjad Islam
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Faiza Tebbji
Infectious Centre de Recherche en Infectiologie (CRI), Centre Hospitalier Universitaire de Quebec (CHUQ) Research Center, University Laval, Quebec City, Quebec G1V 4G2, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jaideep Mallick
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hannah Regan
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Vanessa Dumeaux
Prevention Evaluation Rehabilitation Formation (PERFORM) Centre, Concordia University, Montreal, Quebec H4B 1R6, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Raha Parvizi Omran
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Malcolm Whiteway
Department of Biology, Concordia University, Montreal, Quebec H4B 1R6, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: malcolm.whiteway@concordia.ca

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