Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradation

Abstract Profiling of biological relationships between different molecular layers dissects regulatory mechanisms that ultimately determine cellular function. To thoroughly assess the role of protein post‐translational turnover, we devised a strategy combining pulse stable isotope‐labeled amino acids...

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Main Authors: Barbora Salovska, Hongwen Zhu, Tejas Gandhi, Max Frank, Wenxue Li, George Rosenberger, Chongde Wu, Pierre‐Luc Germain, Hu Zhou, Zdenek Hodny, Lukas Reiter, Yansheng Liu
Format: Article
Language:English
Published: Springer Nature 2020-03-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.15252/msb.20199170
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author Barbora Salovska
Hongwen Zhu
Tejas Gandhi
Max Frank
Wenxue Li
George Rosenberger
Chongde Wu
Pierre‐Luc Germain
Hu Zhou
Zdenek Hodny
Lukas Reiter
Yansheng Liu
author_facet Barbora Salovska
Hongwen Zhu
Tejas Gandhi
Max Frank
Wenxue Li
George Rosenberger
Chongde Wu
Pierre‐Luc Germain
Hu Zhou
Zdenek Hodny
Lukas Reiter
Yansheng Liu
author_sort Barbora Salovska
collection DOAJ
description Abstract Profiling of biological relationships between different molecular layers dissects regulatory mechanisms that ultimately determine cellular function. To thoroughly assess the role of protein post‐translational turnover, we devised a strategy combining pulse stable isotope‐labeled amino acids in cells (pSILAC), data‐independent acquisition mass spectrometry (DIA‐MS), and a novel data analysis framework that resolves protein degradation rate on the level of mRNA alternative splicing isoforms and isoform groups. We demonstrated our approach by the genome‐wide correlation analysis between mRNA amounts and protein degradation across different strains of HeLa cells that harbor a high grade of gene dosage variation. The dataset revealed that specific biological processes, cellular organelles, spatial compartments of organelles, and individual protein isoforms of the same genes could have distinctive degradation rate. The protein degradation diversity thus dissects the corresponding buffering or concerting protein turnover control across cancer cell lines. The data further indicate that specific mRNA splicing events such as intron retention significantly impact the protein abundance levels. Our findings support the tight association between transcriptome variability and proteostasis and provide a methodological foundation for studying functional protein degradation.
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publishDate 2020-03-01
publisher Springer Nature
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series Molecular Systems Biology
spelling doaj-art-7eb9b1cb88724f28b0e02d5b8de1d4d02025-08-20T03:06:39ZengSpringer NatureMolecular Systems Biology1744-42922020-03-0116311910.15252/msb.20199170Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradationBarbora Salovska0Hongwen Zhu1Tejas Gandhi2Max Frank3Wenxue Li4George Rosenberger5Chongde Wu6Pierre‐Luc Germain7Hu Zhou8Zdenek Hodny9Lukas Reiter10Yansheng Liu11Yale Cancer Biology Institute, Yale UniversityDepartment of Analytical Chemistry and CAS Key Laboratory of Receptor Research, Shanghai Institute of Materia Medica, Chinese Academy of SciencesBiognosysEuropean Molecular Biology LaboratoryYale Cancer Biology Institute, Yale UniversityDepartment of Systems Biology, Columbia UniversityYale Cancer Biology Institute, Yale UniversityInstitute for Neuroscience, D‐HEST, ETH ZurichDepartment of Analytical Chemistry and CAS Key Laboratory of Receptor Research, Shanghai Institute of Materia Medica, Chinese Academy of SciencesDepartment of Genome Integrity, Institute of Molecular Genetics of the Czech Academy of SciencesBiognosysYale Cancer Biology Institute, Yale UniversityAbstract Profiling of biological relationships between different molecular layers dissects regulatory mechanisms that ultimately determine cellular function. To thoroughly assess the role of protein post‐translational turnover, we devised a strategy combining pulse stable isotope‐labeled amino acids in cells (pSILAC), data‐independent acquisition mass spectrometry (DIA‐MS), and a novel data analysis framework that resolves protein degradation rate on the level of mRNA alternative splicing isoforms and isoform groups. We demonstrated our approach by the genome‐wide correlation analysis between mRNA amounts and protein degradation across different strains of HeLa cells that harbor a high grade of gene dosage variation. The dataset revealed that specific biological processes, cellular organelles, spatial compartments of organelles, and individual protein isoforms of the same genes could have distinctive degradation rate. The protein degradation diversity thus dissects the corresponding buffering or concerting protein turnover control across cancer cell lines. The data further indicate that specific mRNA splicing events such as intron retention significantly impact the protein abundance levels. Our findings support the tight association between transcriptome variability and proteostasis and provide a methodological foundation for studying functional protein degradation.https://doi.org/10.15252/msb.20199170alternative splicingDIA mass spectrometryprotein turnoverproteomicspulsed SILAC
spellingShingle Barbora Salovska
Hongwen Zhu
Tejas Gandhi
Max Frank
Wenxue Li
George Rosenberger
Chongde Wu
Pierre‐Luc Germain
Hu Zhou
Zdenek Hodny
Lukas Reiter
Yansheng Liu
Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradation
Molecular Systems Biology
alternative splicing
DIA mass spectrometry
protein turnover
proteomics
pulsed SILAC
title Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradation
title_full Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradation
title_fullStr Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradation
title_full_unstemmed Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradation
title_short Isoform‐resolved correlation analysis between mRNA abundance regulation and protein level degradation
title_sort isoform resolved correlation analysis between mrna abundance regulation and protein level degradation
topic alternative splicing
DIA mass spectrometry
protein turnover
proteomics
pulsed SILAC
url https://doi.org/10.15252/msb.20199170
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AT hongwenzhu isoformresolvedcorrelationanalysisbetweenmrnaabundanceregulationandproteinleveldegradation
AT tejasgandhi isoformresolvedcorrelationanalysisbetweenmrnaabundanceregulationandproteinleveldegradation
AT maxfrank isoformresolvedcorrelationanalysisbetweenmrnaabundanceregulationandproteinleveldegradation
AT wenxueli isoformresolvedcorrelationanalysisbetweenmrnaabundanceregulationandproteinleveldegradation
AT georgerosenberger isoformresolvedcorrelationanalysisbetweenmrnaabundanceregulationandproteinleveldegradation
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AT lukasreiter isoformresolvedcorrelationanalysisbetweenmrnaabundanceregulationandproteinleveldegradation
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