Proteoform-Specific Insights into Cellular Proteome Regulation

Knowledge regarding compositions of proteomes at the proteoform level enhances insights into cellular phenotypes. A strategy is described herein for discovery of proteoform-specific information about cellular proteomes. This strategy involved analysis of data obtained by bottom-up mass spectrometry...

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Published inMolecular & cellular proteomics Vol. 15; no. 10; pp. 3297 - 3320
Main Authors Norris, Emma L., Headlam, Madeleine J., Dave, Keyur A., Smith, David D., Bukreyev, Alexander, Singh, Toshna, Jayakody, Buddhika A., Chappell, Keith J., Collins, Peter L., Gorman, Jeffrey J.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.10.2016
The American Society for Biochemistry and Molecular Biology
Subjects
A549 Cells - metabolism
A549 Cells - virology
Chromatography, Liquid - methods
Gene Expression Regulation
Humans
Phosphorylation
Proteolysis
Proteome - metabolism
Proteomics - methods
Respiratory Syncytial Virus, Human - physiology
Tandem Mass Spectrometry - methods
Technological Innovation and Resources
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Abstract Knowledge regarding compositions of proteomes at the proteoform level enhances insights into cellular phenotypes. A strategy is described herein for discovery of proteoform-specific information about cellular proteomes. This strategy involved analysis of data obtained by bottom-up mass spectrometry of multiple protein OGE separations on a fraction by fraction basis. The strategy was exemplified using five matched sets of lysates of uninfected and human respiratory syncytial virus-infected A549 cells. Template matching demonstrated that 67.3% of 10475 protein profiles identified focused to narrow pI windows indicative of efficacious focusing. Furthermore, correlation between experimental and theoretical pI gradients indicated reproducible focusing. Based on these observations a proteoform profiling strategy was developed to identify proteoforms, detect proteoform diversity and discover potential proteoform regulation. One component of this strategy involved examination of the focusing profiles for protein groups. A novel concordance analysis facilitated differentiation between proteoforms, including proteoforms generated by alternate splicing and proteolysis. Evaluation of focusing profiles and concordance analysis were applicable to cells from a single and/or multiple biological states. Statistical analyses identified proteoform variation between biological states. Regulation relevant to cellular responses to human respiratory syncytial virus was revealed. Western blotting and Protomap analyses validated the proteoform regulation. Discovery of STAT1, WARS, MX1, and HSPB1 proteoform regulation by human respiratory syncytial virus highlighted the impact of the profiling strategy. Novel truncated proteoforms of MX1 were identified in infected cells and phosphorylation driven regulation of HSPB1 proteoforms was correlated with infection. The proteoform profiling strategy is generally applicable to investigating interactions between viruses and host cells and the analysis of other biological systems.
AbstractList Knowledge regarding compositions of proteomes at the proteoform level enhances insights into cellular phenotypes. A strategy is described herein for discovery of proteoform-specific information about cellular proteomes. This strategy involved analysis of data obtained by bottom-up mass spectrometry of multiple protein OGE separations on a fraction by fraction basis. The strategy was exemplified using five matched sets of lysates of uninfected and human respiratory syncytial virus-infected A549 cells. Template matching demonstrated that 67.3% of 10475 protein profiles identified focused to narrow pI windows indicative of efficacious focusing. Furthermore, correlation between experimental and theoretical pI gradients indicated reproducible focusing. Based on these observations a proteoform profiling strategy was developed to identify proteoforms, detect proteoform diversity and discover potential proteoform regulation. One component of this strategy involved examination of the focusing profiles for protein groups. A novel concordance analysis facilitated differentiation between proteoforms, including proteoforms generated by alternate splicing and proteolysis. Evaluation of focusing profiles and concordance analysis were applicable to cells from a single and/or multiple biological states. Statistical analyses identified proteoform variation between biological states. Regulation relevant to cellular responses to human respiratory syncytial virus was revealed. Western blotting and Protomap analyses validated the proteoform regulation. Discovery of STAT1, WARS, MX1, and HSPB1 proteoform regulation by human respiratory syncytial virus highlighted the impact of the profiling strategy. Novel truncated proteoforms of MX1 were identified in infected cells and phosphorylation driven regulation of HSPB1 proteoforms was correlated with infection. The proteoform profiling strategy is generally applicable to investigating interactions between viruses and host cells and the analysis of other biological systems.
Author Norris, Emma L.
Jayakody, Buddhika A.
Headlam, Madeleine J.
Dave, Keyur A.
Collins, Peter L.
Singh, Toshna
Chappell, Keith J.
Bukreyev, Alexander
Gorman, Jeffrey J.
Smith, David D.
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CitedBy_id crossref_primary_10_1152_physrev_00030_2019
crossref_primary_10_1128_spectrum_02528_23
crossref_primary_10_1074_mcp_O116_066001
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These authors contributed equally to this work.
Current address: Departments of Pathology and Microbiology and Immunology, Galveston National Laboratory, Keiller Building, Room 3.145, 301 University Boulevard, University of Texas Medical Branch, Galveston, Texas 77555-0609.
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Snippet Knowledge regarding compositions of proteomes at the proteoform level enhances insights into cellular phenotypes. A strategy is described herein for discovery...
SourceID pubmedcentral
proquest
crossref
pubmed
elsevier
SourceType Open Access Repository
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StartPage 3297
SubjectTerms A549 Cells - metabolism
A549 Cells - virology
Chromatography, Liquid - methods
Gene Expression Regulation
Humans
Phosphorylation
Proteolysis
Proteome - metabolism
Proteomics - methods
Respiratory Syncytial Virus, Human - physiology
Tandem Mass Spectrometry - methods
Technological Innovation and Resources
Title Proteoform-Specific Insights into Cellular Proteome Regulation
URI https://dx.doi.org/10.1074/mcp.O116.058438
https://www.ncbi.nlm.nih.gov/pubmed/27451424
https://search.proquest.com/docview/1826726205
https://pubmed.ncbi.nlm.nih.gov/PMC5054351
Volume 15
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