An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tongues

ABSTRACT Microbial gene expression measurements derived from infected organs are invaluable to understand pathogenesis. However, current methods are limited to “bulk” analyses that neglect microbial cell heterogeneity and the lesion's spatial architecture. Here, we report the use of hybridizati...

Full description

Saved in:
Bibliographic Details
Main Authors: Elena Lindemann-Perez, Diana L. Rodríguez, J. Christian Pérez
Format: Article
Language:English
Published: American Society for Microbiology 2024-09-01
Series:mSphere
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msphere.00282-24
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850262272531759104
author Elena Lindemann-Perez
Diana L. Rodríguez
J. Christian Pérez
author_facet Elena Lindemann-Perez
Diana L. Rodríguez
J. Christian Pérez
author_sort Elena Lindemann-Perez
collection DOAJ
description ABSTRACT Microbial gene expression measurements derived from infected organs are invaluable to understand pathogenesis. However, current methods are limited to “bulk” analyses that neglect microbial cell heterogeneity and the lesion's spatial architecture. Here, we report the use of hybridization chain reaction RNA fluorescence in situ hybridization (HCR RNA-FISH) to visualize and quantify Candida albicans transcripts at single-cell resolution in tongues of infected mice. The method is compatible with fixed-frozen and formalin-fixed paraffin-embedded tissues. We document cell-to-cell variation and intriguing spatiotemporal expression patterns for C. albicans mRNAs that encode products implicated in oral candidiasis. The approach provides a spatial dimension to gene expression analyses of host-Candida interactions.IMPORTANCECandida albicans is a fungal pathobiont inhabiting multiple mucosal surfaces of the human body. Immunosuppression, antibiotic-induced microbial dysbiosis, or implanted medical devices can impair mucosal integrity enabling C. albicans to overgrow and disseminate, causing either mucosal diseases such as oropharyngeal candidiasis or life-threatening systemic infections. Profiling fungal genes that are expressed in the infected mucosa or in any other infected organ is paramount to understand pathogenesis. Ideally, these transcript profiling measurements should reveal the expression of any gene at the single-cell level. The resolution typically achieved with current approaches, however, limits most gene expression measurements to cell population averages. The approach described in this report provides a means to dissect fungal gene expression in infected tissues at single-cell resolution.
format Article
id doaj-art-d27dfc21702c453897e19d47b29960ca
institution OA Journals
issn 2379-5042
language English
publishDate 2024-09-01
publisher American Society for Microbiology
record_format Article
series mSphere
spelling doaj-art-d27dfc21702c453897e19d47b29960ca2025-08-20T01:55:12ZengAmerican Society for MicrobiologymSphere2379-50422024-09-019910.1128/msphere.00282-24An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tonguesElena Lindemann-Perez0Diana L. Rodríguez1J. Christian Pérez2Department of Microbiology and Molecular Genetics, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, Texas, USADepartment of Microbiology and Molecular Genetics, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, Texas, USADepartment of Microbiology and Molecular Genetics, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, Texas, USAABSTRACT Microbial gene expression measurements derived from infected organs are invaluable to understand pathogenesis. However, current methods are limited to “bulk” analyses that neglect microbial cell heterogeneity and the lesion's spatial architecture. Here, we report the use of hybridization chain reaction RNA fluorescence in situ hybridization (HCR RNA-FISH) to visualize and quantify Candida albicans transcripts at single-cell resolution in tongues of infected mice. The method is compatible with fixed-frozen and formalin-fixed paraffin-embedded tissues. We document cell-to-cell variation and intriguing spatiotemporal expression patterns for C. albicans mRNAs that encode products implicated in oral candidiasis. The approach provides a spatial dimension to gene expression analyses of host-Candida interactions.IMPORTANCECandida albicans is a fungal pathobiont inhabiting multiple mucosal surfaces of the human body. Immunosuppression, antibiotic-induced microbial dysbiosis, or implanted medical devices can impair mucosal integrity enabling C. albicans to overgrow and disseminate, causing either mucosal diseases such as oropharyngeal candidiasis or life-threatening systemic infections. Profiling fungal genes that are expressed in the infected mucosa or in any other infected organ is paramount to understand pathogenesis. Ideally, these transcript profiling measurements should reveal the expression of any gene at the single-cell level. The resolution typically achieved with current approaches, however, limits most gene expression measurements to cell population averages. The approach described in this report provides a means to dissect fungal gene expression in infected tissues at single-cell resolution.https://journals.asm.org/doi/10.1128/msphere.00282-24Candida albicanshybridization chain reactionRNA-FISHCandida-host interactionsoropharyngeal candidiasisCandida-infected tissue
spellingShingle Elena Lindemann-Perez
Diana L. Rodríguez
J. Christian Pérez
An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tongues
mSphere
Candida albicans
hybridization chain reaction
RNA-FISH
Candida-host interactions
oropharyngeal candidiasis
Candida-infected tissue
title An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tongues
title_full An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tongues
title_fullStr An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tongues
title_full_unstemmed An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tongues
title_short An approach to analyze spatiotemporal patterns of gene expression at single-cell resolution in Candida albicans-infected mouse tongues
title_sort approach to analyze spatiotemporal patterns of gene expression at single cell resolution in candida albicans infected mouse tongues
topic Candida albicans
hybridization chain reaction
RNA-FISH
Candida-host interactions
oropharyngeal candidiasis
Candida-infected tissue
url https://journals.asm.org/doi/10.1128/msphere.00282-24
work_keys_str_mv AT elenalindemannperez anapproachtoanalyzespatiotemporalpatternsofgeneexpressionatsinglecellresolutionincandidaalbicansinfectedmousetongues
AT dianalrodriguez anapproachtoanalyzespatiotemporalpatternsofgeneexpressionatsinglecellresolutionincandidaalbicansinfectedmousetongues
AT jchristianperez anapproachtoanalyzespatiotemporalpatternsofgeneexpressionatsinglecellresolutionincandidaalbicansinfectedmousetongues
AT elenalindemannperez approachtoanalyzespatiotemporalpatternsofgeneexpressionatsinglecellresolutionincandidaalbicansinfectedmousetongues
AT dianalrodriguez approachtoanalyzespatiotemporalpatternsofgeneexpressionatsinglecellresolutionincandidaalbicansinfectedmousetongues
AT jchristianperez approachtoanalyzespatiotemporalpatternsofgeneexpressionatsinglecellresolutionincandidaalbicansinfectedmousetongues