Single-cell protein-mRNA correlation analysis enabled by multiplexed dual-analyte co-detection

We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This is achieved by combining the oligo extension reaction (OER), which converts protein levels to DNA levels, with reverse transcription for mRNA detection...

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Published inScientific reports Vol. 7; no. 1; pp. 2776 - 8
Main Authors Gong, Haibiao, Wang, Xiaohui, Liu, Benjamin, Boutet, Stephane, Holcomb, Ilona, Dakshinamoorthy, Gajalakshmi, Ooi, Aik, Sanada, Chad, Sun, Gang, Ramakrishnan, Ramesh
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 05.06.2017
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Abstract We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This is achieved by combining the oligo extension reaction (OER), which converts protein levels to DNA levels, with reverse transcription for mRNA detection. Unsupervised gene expression profiling analysis, including principal component analysis and hierarchical clustering, revealed different aspects of the protein-mRNA relationship. Violin plot analysis showed that some genes exhibited similar distribution patterns for proteins and mRNAs. We also demonstrate that cells can be separated into subpopulations based on their protein-mRNA expression profiles, and that different subpopulations have distinct correlation coefficient values. Our results demonstrated that integrated investigations of mRNA and protein levels in single cells allows comprehensive analysis not attainable at bulk levels.
AbstractList We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This is achieved by combining the oligo extension reaction (OER), which converts protein levels to DNA levels, with reverse transcription for mRNA detection. Unsupervised gene expression profiling analysis, including principal component analysis and hierarchical clustering, revealed different aspects of the protein-mRNA relationship. Violin plot analysis showed that some genes exhibited similar distribution patterns for proteins and mRNAs. We also demonstrate that cells can be separated into subpopulations based on their protein-mRNA expression profiles, and that different subpopulations have distinct correlation coefficient values. Our results demonstrated that integrated investigations of mRNA and protein levels in single cells allows comprehensive analysis not attainable at bulk levels.
Abstract We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This is achieved by combining the oligo extension reaction (OER), which converts protein levels to DNA levels, with reverse transcription for mRNA detection. Unsupervised gene expression profiling analysis, including principal component analysis and hierarchical clustering, revealed different aspects of the protein-mRNA relationship. Violin plot analysis showed that some genes exhibited similar distribution patterns for proteins and mRNAs. We also demonstrate that cells can be separated into subpopulations based on their protein-mRNA expression profiles, and that different subpopulations have distinct correlation coefficient values. Our results demonstrated that integrated investigations of mRNA and protein levels in single cells allows comprehensive analysis not attainable at bulk levels.
Abstract We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This is achieved by combining the oligo extension reaction (OER), which converts protein levels to DNA levels, with reverse transcription for mRNA detection. Unsupervised gene expression profiling analysis, including principal component analysis and hierarchical clustering, revealed different aspects of the protein-mRNA relationship. Violin plot analysis showed that some genes exhibited similar distribution patterns for proteins and mRNAs. We also demonstrate that cells can be separated into subpopulations based on their protein-mRNA expression profiles, and that different subpopulations have distinct correlation coefficient values. Our results demonstrated that integrated investigations of mRNA and protein levels in single cells allows comprehensive analysis not attainable at bulk levels.
ArticleNumber 2776
Author Holcomb, Ilona
Sun, Gang
Gong, Haibiao
Dakshinamoorthy, Gajalakshmi
Ramakrishnan, Ramesh
Wang, Xiaohui
Boutet, Stephane
Liu, Benjamin
Sanada, Chad
Ooi, Aik
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Cites_doi 10.1016/j.molcel.2016.02.030
10.1021/acs.bioconjchem.5b00613
10.1042/bst0210921
10.1186/s13059-016-1045-6
10.1373/clinchem.2012.191445
10.1038/nmeth.2694
10.1038/nbt.3498
10.1126/science.1198704
10.1016/j.ymeth.2012.10.004
10.1093/nar/gni063
10.1038/nmeth.1338
10.1016/j.celrep.2015.12.021
10.1002/(SICI)1097-0320(19990301)35:3<284::AID-CYTO12>3.0.CO;2-K
10.1073/pnas.91.12.5490
10.1093/nar/gkr424
10.1177/030098589803500601
10.1038/nature10098
10.1038/nprot.2013.006
10.1016/j.cell.2015.10.039
10.1038/nbt.2038
10.1101/gr.110882.110
10.1016/j.copbio.2013.06.001
10.1371/journal.pone.0095192
10.1038/nmeth.3742
10.1038/nmeth0411-311
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References Willison, Klug (CR1) 2013; 24
Weibrecht (CR11) 2013; 8
Grun, van Oudenaarden (CR25) 2015; 163
Albayrak (CR15) 2016; 61
Gong (CR10) 2016; 27
Livak (CR18) 2013; 59
Assarsson (CR9) 2014; 9
Genshaft (CR16) 2016; 17
Zhang (CR23) 2016; 166
Jacobberger, Sramkoski, Wormsley, Bolton (CR19) 1999; 35
Lundberg, Eriksson, Tran, Assarsson, Fredriksson (CR8) 2011; 39
Schafer (CR22) 1998; 35
Kalisky, Quake (CR2) 2011; 8
Darmanis (CR14) 2016; 14
Bendall (CR6) 2011; 332
Schwanhausser (CR24) 2011; 473
Islam (CR26) 2011; 21
Pines (CR21) 1993; 21
Wu (CR5) 2014; 11
Di Giusto, Wlassoff, Gooding, Messerle, King (CR7) 2005; 33
Taniguchi, Kajiyama, Kambara (CR3) 2009; 6
Henglein, Chenivesse, Wang, Eick, Brechot (CR20) 1994; 91
McDavid, Finak, Gottardo (CR17) 2016; 34
Dalerba (CR4) 2011; 29
Stahlberg, Thomsen, Ruff, Aman (CR13) 2012; 58
Frei (CR12) 2016; 13
E Assarsson (3057_CR9) 2014; 9
C Albayrak (3057_CR15) 2016; 61
SC Bendall (3057_CR6) 2011; 332
J Pines (3057_CR21) 1993; 21
AR Wu (3057_CR5) 2014; 11
H Gong (3057_CR10) 2016; 27
H Zhang (3057_CR23) 2016; 166
KJ Livak (3057_CR18) 2013; 59
S Darmanis (3057_CR14) 2016; 14
A Stahlberg (3057_CR13) 2012; 58
M Lundberg (3057_CR8) 2011; 39
A McDavid (3057_CR17) 2016; 34
P Dalerba (3057_CR4) 2011; 29
I Weibrecht (3057_CR11) 2013; 8
D Grun (3057_CR25) 2015; 163
KR Willison (3057_CR1) 2013; 24
S Islam (3057_CR26) 2011; 21
JW Jacobberger (3057_CR19) 1999; 35
KA Schafer (3057_CR22) 1998; 35
B Henglein (3057_CR20) 1994; 91
AP Frei (3057_CR12) 2016; 13
T Kalisky (3057_CR2) 2011; 8
DA Di Giusto (3057_CR7) 2005; 33
AS Genshaft (3057_CR16) 2016; 17
B Schwanhausser (3057_CR24) 2011; 473
K Taniguchi (3057_CR3) 2009; 6
References_xml – volume: 61
  start-page: 914
  year: 2016
  end-page: 924
  ident: CR15
  article-title: Digital Quantification of Proteins and mRNA in Single Mammalian Cells
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2016.02.030
  contributor:
    fullname: Albayrak
– volume: 27
  start-page: 217
  year: 2016
  end-page: 225
  ident: CR10
  article-title: Simple Method To Prepare Oligonucleotide-Conjugated Antibodies and Its Application in Multiplex Protein Detection in Single Cells
  publication-title: Bioconjug Chem
  doi: 10.1021/acs.bioconjchem.5b00613
  contributor:
    fullname: Gong
– volume: 21
  start-page: 921
  year: 1993
  end-page: 925
  ident: CR21
  article-title: Cyclins and their associated cyclin-dependent kinases in the human cell cycle
  publication-title: Biochem Soc Trans
  doi: 10.1042/bst0210921
  contributor:
    fullname: Pines
– volume: 17
  start-page: 188
  year: 2016
  ident: CR16
  article-title: Multiplexed, targeted profiling of single-cell proteomes and transcriptomes in a single reaction
  publication-title: Genome Biol
  doi: 10.1186/s13059-016-1045-6
  contributor:
    fullname: Genshaft
– volume: 58
  start-page: 1682
  year: 2012
  end-page: 1691
  ident: CR13
  article-title: Quantitative PCR analysis of DNA, RNAs, and proteins in the same single cell
  publication-title: Clin Chem
  doi: 10.1373/clinchem.2012.191445
  contributor:
    fullname: Aman
– volume: 11
  start-page: 41
  year: 2014
  end-page: 46
  ident: CR5
  article-title: Quantitative assessment of single-cell RNA-sequencing methods
  publication-title: Nat Methods
  doi: 10.1038/nmeth.2694
  contributor:
    fullname: Wu
– volume: 34
  start-page: 591
  year: 2016
  end-page: 593
  ident: CR17
  article-title: The contribution of cell cycle to heterogeneity in single-cell RNA-seq data
  publication-title: Nat Biotechnol
  doi: 10.1038/nbt.3498
  contributor:
    fullname: Gottardo
– volume: 166
  start-page: 755
  year: 2016
  end-page: 765
  ident: CR23
  article-title: Integrated Proteogenomic Characterization of Human High-Grade Serous Ovarian
  publication-title: Cancer. Cell
  contributor:
    fullname: Zhang
– volume: 332
  start-page: 687
  year: 2011
  end-page: 696
  ident: CR6
  article-title: Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum
  publication-title: Science
  doi: 10.1126/science.1198704
  contributor:
    fullname: Bendall
– volume: 59
  start-page: 71
  year: 2013
  end-page: 79
  ident: CR18
  article-title: Methods for qPCR gene expression profiling applied to 1440 lymphoblastoid single cells
  publication-title: Methods
  doi: 10.1016/j.ymeth.2012.10.004
  contributor:
    fullname: Livak
– volume: 33
  start-page: e64
  year: 2005
  ident: CR7
  article-title: Proximity extension of circular DNA aptamers with real-time protein detection
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gni063
  contributor:
    fullname: King
– volume: 6
  start-page: 503
  year: 2009
  end-page: 506
  ident: CR3
  article-title: Quantitative analysis of gene expression in a single cell by qPCR
  publication-title: Nat Methods
  doi: 10.1038/nmeth.1338
  contributor:
    fullname: Kambara
– volume: 14
  start-page: 380
  year: 2016
  end-page: 389
  ident: CR14
  article-title: Simultaneous Multiplexed Measurement of RNA and Proteins in Single Cells
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2015.12.021
  contributor:
    fullname: Darmanis
– volume: 35
  start-page: 284
  year: 1999
  end-page: 289
  ident: CR19
  article-title: Estimation of kinetic cell-cycle-related gene expression in G1 and G2 phases from immunofluorescence flow cytometry data
  publication-title: Cytometry
  doi: 10.1002/(SICI)1097-0320(19990301)35:3<284::AID-CYTO12>3.0.CO;2-K
  contributor:
    fullname: Bolton
– volume: 91
  start-page: 5490
  year: 1994
  end-page: 5494
  ident: CR20
  article-title: Structure and cell cycle-regulated transcription of the human cyclin A gene
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.91.12.5490
  contributor:
    fullname: Brechot
– volume: 39
  start-page: e102
  year: 2011
  ident: CR8
  article-title: Homogeneous antibody-based proximity extension assays provide sensitive and specific detection of low-abundant proteins in human blood
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkr424
  contributor:
    fullname: Fredriksson
– volume: 35
  start-page: 461
  year: 1998
  end-page: 478
  ident: CR22
  article-title: The cell cycle: a review
  publication-title: Vet Pathol
  doi: 10.1177/030098589803500601
  contributor:
    fullname: Schafer
– volume: 473
  start-page: 337
  year: 2011
  end-page: 342
  ident: CR24
  article-title: Global quantification of mammalian gene expression control
  publication-title: Nature
  doi: 10.1038/nature10098
  contributor:
    fullname: Schwanhausser
– volume: 8
  start-page: 355
  year: 2013
  end-page: 372
  ident: CR11
  article-title: detection of individual mRNA molecules and protein complexes or post-translational modifications using padlock probes combined with the proximity ligation assay
  publication-title: Nat Protoc
  doi: 10.1038/nprot.2013.006
  contributor:
    fullname: Weibrecht
– volume: 163
  start-page: 799
  year: 2015
  end-page: 810
  ident: CR25
  article-title: Design and Analysis of Single-Cell Sequencing Experiments
  publication-title: Cell
  doi: 10.1016/j.cell.2015.10.039
  contributor:
    fullname: van Oudenaarden
– volume: 29
  start-page: 1120
  year: 2011
  end-page: 1127
  ident: CR4
  article-title: Single-cell dissection of transcriptional heterogeneity in human colon tumors
  publication-title: Nat Biotechnol
  doi: 10.1038/nbt.2038
  contributor:
    fullname: Dalerba
– volume: 21
  start-page: 1160
  year: 2011
  end-page: 1167
  ident: CR26
  article-title: Characterization of the single-cell transcriptional landscape by highly multiplex RNA-seq
  publication-title: Genome Res
  doi: 10.1101/gr.110882.110
  contributor:
    fullname: Islam
– volume: 24
  start-page: 745
  year: 2013
  end-page: 751
  ident: CR1
  article-title: Quantitative single cell and single molecule proteomics for clinical studies
  publication-title: Curr Opin Biotechnol
  doi: 10.1016/j.copbio.2013.06.001
  contributor:
    fullname: Klug
– volume: 9
  start-page: e95192
  year: 2014
  ident: CR9
  article-title: Homogenous 96-plex PEA immunoassay exhibiting high sensitivity, specificity, and excellent scalability
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0095192
  contributor:
    fullname: Assarsson
– volume: 13
  start-page: 269
  year: 2016
  end-page: 275
  ident: CR12
  article-title: Highly multiplexed simultaneous detection of RNAs and proteins in single cells
  publication-title: Nat Methods
  doi: 10.1038/nmeth.3742
  contributor:
    fullname: Frei
– volume: 8
  start-page: 311
  year: 2011
  end-page: 314
  ident: CR2
  article-title: Single-cell genomics
  publication-title: Nat Methods
  doi: 10.1038/nmeth0411-311
  contributor:
    fullname: Quake
– volume: 9
  start-page: e95192
  year: 2014
  ident: 3057_CR9
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0095192
  contributor:
    fullname: E Assarsson
– volume: 91
  start-page: 5490
  year: 1994
  ident: 3057_CR20
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.91.12.5490
  contributor:
    fullname: B Henglein
– volume: 24
  start-page: 745
  year: 2013
  ident: 3057_CR1
  publication-title: Curr Opin Biotechnol
  doi: 10.1016/j.copbio.2013.06.001
  contributor:
    fullname: KR Willison
– volume: 29
  start-page: 1120
  year: 2011
  ident: 3057_CR4
  publication-title: Nat Biotechnol
  doi: 10.1038/nbt.2038
  contributor:
    fullname: P Dalerba
– volume: 11
  start-page: 41
  year: 2014
  ident: 3057_CR5
  publication-title: Nat Methods
  doi: 10.1038/nmeth.2694
  contributor:
    fullname: AR Wu
– volume: 8
  start-page: 311
  year: 2011
  ident: 3057_CR2
  publication-title: Nat Methods
  doi: 10.1038/nmeth0411-311
  contributor:
    fullname: T Kalisky
– volume: 14
  start-page: 380
  year: 2016
  ident: 3057_CR14
  publication-title: Cell Rep
  doi: 10.1016/j.celrep.2015.12.021
  contributor:
    fullname: S Darmanis
– volume: 166
  start-page: 755
  year: 2016
  ident: 3057_CR23
  publication-title: Cancer. Cell
  contributor:
    fullname: H Zhang
– volume: 39
  start-page: e102
  year: 2011
  ident: 3057_CR8
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkr424
  contributor:
    fullname: M Lundberg
– volume: 6
  start-page: 503
  year: 2009
  ident: 3057_CR3
  publication-title: Nat Methods
  doi: 10.1038/nmeth.1338
  contributor:
    fullname: K Taniguchi
– volume: 33
  start-page: e64
  year: 2005
  ident: 3057_CR7
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gni063
  contributor:
    fullname: DA Di Giusto
– volume: 34
  start-page: 591
  year: 2016
  ident: 3057_CR17
  publication-title: Nat Biotechnol
  doi: 10.1038/nbt.3498
  contributor:
    fullname: A McDavid
– volume: 473
  start-page: 337
  year: 2011
  ident: 3057_CR24
  publication-title: Nature
  doi: 10.1038/nature10098
  contributor:
    fullname: B Schwanhausser
– volume: 332
  start-page: 687
  year: 2011
  ident: 3057_CR6
  publication-title: Science
  doi: 10.1126/science.1198704
  contributor:
    fullname: SC Bendall
– volume: 35
  start-page: 284
  year: 1999
  ident: 3057_CR19
  publication-title: Cytometry
  doi: 10.1002/(SICI)1097-0320(19990301)35:3<284::AID-CYTO12>3.0.CO;2-K
  contributor:
    fullname: JW Jacobberger
– volume: 8
  start-page: 355
  year: 2013
  ident: 3057_CR11
  publication-title: Nat Protoc
  doi: 10.1038/nprot.2013.006
  contributor:
    fullname: I Weibrecht
– volume: 35
  start-page: 461
  year: 1998
  ident: 3057_CR22
  publication-title: Vet Pathol
  doi: 10.1177/030098589803500601
  contributor:
    fullname: KA Schafer
– volume: 13
  start-page: 269
  year: 2016
  ident: 3057_CR12
  publication-title: Nat Methods
  doi: 10.1038/nmeth.3742
  contributor:
    fullname: AP Frei
– volume: 21
  start-page: 921
  year: 1993
  ident: 3057_CR21
  publication-title: Biochem Soc Trans
  doi: 10.1042/bst0210921
  contributor:
    fullname: J Pines
– volume: 61
  start-page: 914
  year: 2016
  ident: 3057_CR15
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2016.02.030
  contributor:
    fullname: C Albayrak
– volume: 21
  start-page: 1160
  year: 2011
  ident: 3057_CR26
  publication-title: Genome Res
  doi: 10.1101/gr.110882.110
  contributor:
    fullname: S Islam
– volume: 58
  start-page: 1682
  year: 2012
  ident: 3057_CR13
  publication-title: Clin Chem
  doi: 10.1373/clinchem.2012.191445
  contributor:
    fullname: A Stahlberg
– volume: 59
  start-page: 71
  year: 2013
  ident: 3057_CR18
  publication-title: Methods
  doi: 10.1016/j.ymeth.2012.10.004
  contributor:
    fullname: KJ Livak
– volume: 163
  start-page: 799
  year: 2015
  ident: 3057_CR25
  publication-title: Cell
  doi: 10.1016/j.cell.2015.10.039
  contributor:
    fullname: D Grun
– volume: 27
  start-page: 217
  year: 2016
  ident: 3057_CR10
  publication-title: Bioconjug Chem
  doi: 10.1021/acs.bioconjchem.5b00613
  contributor:
    fullname: H Gong
– volume: 17
  start-page: 188
  year: 2016
  ident: 3057_CR16
  publication-title: Genome Biol
  doi: 10.1186/s13059-016-1045-6
  contributor:
    fullname: AS Genshaft
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Snippet We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This is...
Abstract We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This...
Abstract We have investigated the correlation between proteins and mRNAs in single cells employing an integrated workflow for dual-analyte co-detection. This...
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SubjectTerms 38
38/39
38/62
38/77
45
631/1647/2017
631/1647/2067
82
82/80
96/1
Biomarkers
Cell Line
Correlation analysis
Deoxyribonucleic acid
DNA
Gene expression
Gene Expression Profiling - methods
Humanities and Social Sciences
Humans
multidisciplinary
Proteins
Proteins - metabolism
Proteomics - methods
Real-Time Polymerase Chain Reaction
Reverse transcription
RNA, Messenger - genetics
RNA, Messenger - metabolism
Science
Science (multidisciplinary)
Single-Cell Analysis - methods
Single-cell protein
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Title Single-cell protein-mRNA correlation analysis enabled by multiplexed dual-analyte co-detection
URI https://link.springer.com/article/10.1038/s41598-017-03057-5
https://www.ncbi.nlm.nih.gov/pubmed/28584233
https://www.proquest.com/docview/1955526738
https://search.proquest.com/docview/1906465114
https://pubmed.ncbi.nlm.nih.gov/PMC5459813
https://doaj.org/article/d53b4a806b534842a54ad55e4e3c21e5
Volume 7
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