Exploring the virulence gene interactome with CRISPR/dCas9 in the human malaria parasite

Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum , but few factors have been shown to play a direct role. We adapted a CRISPR‐based proteomics approach to identify novel factors associated with var genes in their natural chr...

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Published inMolecular systems biology Vol. 16; no. 8; pp. e9569 - n/a
Main Authors Bryant, Jessica M, Baumgarten, Sebastian, Dingli, Florent, Loew, Damarys, Sinha, Ameya, Claës, Aurélie, Preiser, Peter R, Dedon, Peter C, Scherf, Artur
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.08.2020
EMBO Press
John Wiley and Sons Inc
Springer Nature
Subjects
Adenosine Triphosphatases - metabolism
Animals
Antigens, Protozoan - genetics
Antigens, Protozoan - metabolism
Chromatin
Chromatin Immunoprecipitation Sequencing
Chromosomes
CRISPR
CRISPR-Cas Systems
Deoxyribonucleic acid
Divergence
DNA
EMBO09
EMBO23
Enrichment
Epigenetics
Erythrocytes
Genes
Genomes
Genomics
Humans
Immune system
Introns
Life Sciences
Malaria
Mass Spectrometry
Mass spectroscopy
Microbiology and Parasitology
MORC protein
Parasites
Parasitology
Pathogenesis
Plasmodium falciparum
Plasmodium falciparum - genetics
Plasmodium falciparum - immunology
Plasmodium falciparum - pathogenicity
Promoter Regions, Genetic
Protein Interaction Maps
Proteins
Proteomics
Proteomics - methods
Regulatory sequences
Structural proteins
Transcription activation
Transcription factors
Transcription Factors - metabolism
Var gene
var genes
Vector-borne diseases
Virulence
Virulence Factors - genetics
Virulence Factors - metabolism
CRISPR
chromatin
genes
epigenetics
Plasmodium falciparum
var genes
Virology & Host Pathogen Interaction
Microbiology
var genes Subject Categories Chromatin
Transcription & Genomics
Online AccessGet full text

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Abstract Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum , but few factors have been shown to play a direct role. We adapted a CRISPR‐based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 (“dCas9”) was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of Pf ISWI, an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of Pf ISWI identified several proteins enriched at the var gene promoter such as acetyl‐CoA synthetase, a putative MORC protein, and an ApiAP2 transcription factor. These findings validate the CRISPR/dCas9 proteomics method and define a new var gene‐associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin‐associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite. Synopsis CRISPR/dCas9‐based proteomics is used to purify specific DNA regulatory elements in their natural chromatin context and to identify novel chromatin factors associated with virulence genes in the human malaria parasite, Plasmodium falciparum . dCas9 immunoprecipitation and mass spectrometry identify proteins previously implicated in var gene biology in addition to novel factors, including a putative chromatin remodeler, ISWI. Proteomic analysis of ISWI reveals a new var gene‐associated complex comprising a putative MORC family protein and an ApiAP2 transcription factor. ISWI binds to promoter regions and plays a role in transcriptional activation of genes, including the active var gene in ring stage parasites. Graphical Abstract CRISPR/dCas9‐based proteomics is used to purify specific DNA regulatory elements in their natural chromatin context and to identify novel chromatin factors associated with virulence genes in the human malaria parasite, Plasmodium falciparum .
AbstractList Abstract Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum, but few factors have been shown to play a direct role. We adapted a CRISPR‐based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 (“dCas9”) was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of PfISWI, an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of PfISWI identified several proteins enriched at the var gene promoter such as acetyl‐CoA synthetase, a putative MORC protein, and an ApiAP2 transcription factor. These findings validate the CRISPR/dCas9 proteomics method and define a new var gene‐associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin‐associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite.
Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum, but few factors have been shown to play a direct role. We adapted a CRISPR-based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 ("dCas9") was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of PfISWI, an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of PfISWI identified several proteins enriched at the var gene promoter such as acetyl-CoA synthetase, a putative MORC protein, and an ApiAP2 transcription factor. These findings validate the CRISPR/dCas9 proteomics method and define a new var gene-associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin-associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite.Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum, but few factors have been shown to play a direct role. We adapted a CRISPR-based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 ("dCas9") was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of PfISWI, an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of PfISWI identified several proteins enriched at the var gene promoter such as acetyl-CoA synthetase, a putative MORC protein, and an ApiAP2 transcription factor. These findings validate the CRISPR/dCas9 proteomics method and define a new var gene-associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin-associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite.
Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum, but few factors have been shown to play a direct role. We adapted a CRISPR‐based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 (“dCas9”) was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of PfISWI, an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of PfISWI identified several proteins enriched at the var gene promoter such as acetyl‐CoA synthetase, a putative MORC protein, and an ApiAP2 transcription factor. These findings validate the CRISPR/dCas9 proteomics method and define a new var gene‐associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin‐associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite. Synopsis CRISPR/dCas9‐based proteomics is used to purify specific DNA regulatory elements in their natural chromatin context and to identify novel chromatin factors associated with virulence genes in the human malaria parasite, Plasmodium falciparum. dCas9 immunoprecipitation and mass spectrometry identify proteins previously implicated in var gene biology in addition to novel factors, including a putative chromatin remodeler, ISWI. Proteomic analysis of ISWI reveals a new var gene‐associated complex comprising a putative MORC family protein and an ApiAP2 transcription factor. ISWI binds to promoter regions and plays a role in transcriptional activation of genes, including the active var gene in ring stage parasites. CRISPR/dCas9‐based proteomics is used to purify specific DNA regulatory elements in their natural chromatin context and to identify novel chromatin factors associated with virulence genes in the human malaria parasite, Plasmodium falciparum.
Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum, but few factors have been shown to play a direct role. We adapted a CRISPR-based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 ("dCas9") was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of PfISWI, an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of PfISWI identified several proteins enriched at the var gene promoter such as acetyl-CoA synthetase, a putative MORC protein, and an ApiAP2 transcription factor. These findings validate the CRISPR/dCas9 proteomics method and define a new var gene-associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin-associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite.
Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum , but few factors have been shown to play a direct role. We adapted a CRISPR ‐based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 (“ dC as9”) was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of Pf ISWI , an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of Pf ISWI identified several proteins enriched at the var gene promoter such as acetyl‐CoA synthetase, a putative MORC protein, and an Api AP 2 transcription factor. These findings validate the CRISPR / dC as9 proteomics method and define a new var gene‐associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin‐associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite. CRISPR / dC as9‐based proteomics is used to purify specific DNA regulatory elements in their natural chromatin context and to identify novel chromatin factors associated with virulence genes in the human malaria parasite, Plasmodium falciparum .
Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum , but few factors have been shown to play a direct role. We adapted a CRISPR‐based proteomics approach to identify novel factors associated with var genes in their natural chromatin context. Catalytically inactive Cas9 (“dCas9”) was targeted to var gene regulatory elements, immunoprecipitated, and analyzed with mass spectrometry. Known and novel factors were enriched including structural proteins, DNA helicases, and chromatin remodelers. Functional characterization of Pf ISWI, an evolutionarily divergent putative chromatin remodeler enriched at the var gene promoter, revealed a role in transcriptional activation. Proteomics of Pf ISWI identified several proteins enriched at the var gene promoter such as acetyl‐CoA synthetase, a putative MORC protein, and an ApiAP2 transcription factor. These findings validate the CRISPR/dCas9 proteomics method and define a new var gene‐associated chromatin complex. This study establishes a tool for targeted chromatin purification of unaltered genomic loci and identifies novel chromatin‐associated factors potentially involved in transcriptional control and/or chromatin organization of virulence genes in the human malaria parasite. Synopsis CRISPR/dCas9‐based proteomics is used to purify specific DNA regulatory elements in their natural chromatin context and to identify novel chromatin factors associated with virulence genes in the human malaria parasite, Plasmodium falciparum . dCas9 immunoprecipitation and mass spectrometry identify proteins previously implicated in var gene biology in addition to novel factors, including a putative chromatin remodeler, ISWI. Proteomic analysis of ISWI reveals a new var gene‐associated complex comprising a putative MORC family protein and an ApiAP2 transcription factor. ISWI binds to promoter regions and plays a role in transcriptional activation of genes, including the active var gene in ring stage parasites. Graphical Abstract CRISPR/dCas9‐based proteomics is used to purify specific DNA regulatory elements in their natural chromatin context and to identify novel chromatin factors associated with virulence genes in the human malaria parasite, Plasmodium falciparum .
Author Bryant, Jessica M
Scherf, Artur
Dedon, Peter C
Baumgarten, Sebastian
Dingli, Florent
Sinha, Ameya
Preiser, Peter R
Loew, Damarys
Claës, Aurélie
AuthorAffiliation 6 Antimicrobial Resistance Interdisciplinary Research Group Singapore‐MIT Alliance for Research and Technology Singapore Singapore
2 INSERM U1201 Paris France
4 Institut Curie PSL Research University Centre de Recherche Mass Spectrometry and Proteomics Facility Paris France
7 Department of Biological Engineering Massachusetts Institute of Technology Cambridge MA USA
3 CNRS ERL9195 Paris France
1 Biology of Host‐Parasite Interactions Unit Institut Pasteur Paris France
5 School of Biological Sciences Nanyang Technological University Singapore Singapore
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AASML
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EJD
GODZA
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CGR
CUY
CVF
ECM
EIF
NPM
3V.
7QL
7TM
7U9
7XB
88A
8FD
8FK
C1K
FR3
H94
K9.
M7N
MBDVC
P64
PKEHL
PQEST
PQUKI
PRINS
Q9U
RC3
7X8
1XC
AAHHS
ACCFJ
AEEZP
AEQDE
AIWBW
AJBDE
PMFND
VOOES
5PM
PUEGO
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ISSN 1744-4292
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IsDoiOpenAccess true
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Issue 8
Keywords CRISPR
chromatin
genes
epigenetics
Plasmodium falciparum
var genes
Virology & Host Pathogen Interaction
Microbiology
var genes Subject Categories Chromatin
Transcription & Genomics
Language English
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Snippet Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum , but few factors have been shown...
Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum, but few factors have been shown...
Abstract Mutually exclusive expression of the var multigene family is key to immune evasion and pathogenesis in Plasmodium falciparum, but few factors have...
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SubjectTerms Adenosine Triphosphatases - metabolism
Animals
Antigens, Protozoan - genetics
Antigens, Protozoan - metabolism
Chromatin
Chromatin Immunoprecipitation Sequencing
Chromosomes
CRISPR
CRISPR-Cas Systems
Deoxyribonucleic acid
Divergence
DNA
EMBO09
EMBO23
Enrichment
Epigenetics
Erythrocytes
Genes
Genomes
Genomics
Humans
Immune system
Introns
Life Sciences
Malaria
Mass Spectrometry
Mass spectroscopy
Microbiology and Parasitology
MORC protein
Parasites
Parasitology
Pathogenesis
Plasmodium falciparum
Plasmodium falciparum - genetics
Plasmodium falciparum - immunology
Plasmodium falciparum - pathogenicity
Promoter Regions, Genetic
Protein Interaction Maps
Proteins
Proteomics
Proteomics - methods
Regulatory sequences
Structural proteins
Transcription activation
Transcription factors
Transcription Factors - metabolism
Var gene
var genes
Vector-borne diseases
Virulence
Virulence Factors - genetics
Virulence Factors - metabolism
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Title Exploring the virulence gene interactome with CRISPR/dCas9 in the human malaria parasite
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Volume 16
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