Primate Transcript and Protein Expression Levels Evolve Under Compensatory Selection Pressures
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Don't Ape Protein Variation: Changes in DNA and messenger RNA (mRNA) expression levels have been used to estimate evolutionary changes between species. However protein expression levels may better reflect selection on divergent and constrained phenotypes. Khan et al. (p. 1100 , published online 17 October; see the Perspective by Vogel ) measured the differences among and within species between mRNA expression and protein levels in humans, chimpanzees, and rhesus macaques, identifying protein transcripts that seem to be under lineage-specific constraint between humans and chimpanzees.
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Protein expression is more conserved between species than mRNA expression is.
“protein expression is more conserved across species than mRNA expression (11, 14, 15)”
From Dynamic profiling of the protein life cycle in response to pathogens (2015) · cites this paper as [15]
Protein expression evolves under greater evolutionary constraint than transcript levels.
“Comparative studies (9-13) have suggested that protein expression evolves under greater evolutionary constraint than transcript levels (14)”
From Impact of regulatory variation from RNA to protein (2015) · cites this paper as [14]
The observation that many eQTLs are not associated with protein differences is consistent with protein levels diverging less than transcript levels across species.
“Our observation that many SNPs identified as eQTLs are not associated with differences in protein levels is consistent with the notion that, across species, protein levels diverge less than transcript levels (12-17).”
From Impact of regulatory variation from RNA to protein (2015) · cites this paper as [14]
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Cites
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · see citing works
Ong, S.-E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., & Mann, M. (2002) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m200025-mcp200 · Cited by 5,574 · see citing works
Insights into the regulation of protein abundance from proteomic and transcriptomic analyses
Vogel, C., & Marcotte, E. M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3185 · Cited by 4,195 · see citing works
The evolution of gene expression levels in mammalian organs
Brawand, D., Soumillon, M., Necsulea, A., Julien, P., Csárdi, G., Harrigan, P., Weier, M., Liechti, A., Aximu-Petri, A., Kircher, M., et al. (2011) · Nature · doi:10.1038/nature10532 · Cited by 1,248 · see citing works
Intra- and Interspecific Variation in Primate Gene Expression Patterns
Enard, W., Khaitovich, P., Klose, J., Zöllner, S. K., Heißig, F., Giavalisco, P., Nieselt, K., Muchmore, E. A., Varki, A. P., Ravid, R., et al. (2002) · Science · doi:10.1126/science.1068996 · Cited by 845 · see citing works
Parallel Patterns of Evolution in the Genomes and Transcriptomes of Humans and Chimpanzees
Khaitovich, P., Hellmann, I., Enard, W., Nowick, K., Leinweber, M., Franz, H., Weiß, G., Lachmann, M., & Pääbo, S. (2005) · Science · doi:10.1126/science.1108296 · Cited by 590 · see citing works
Comparative studies of gene expression and the evolution of gene regulation
Romero, I. G., Ruvinsky, I., & Gilad, Y. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3229 · Cited by 488 · see citing works
Precision proteomics: The case for high resolution and high mass accuracy
Mann, M., & Kelleher, N. L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800788105 · Cited by 450 · see citing works
Constructing genomic maps of positive selection in humans: Where do we go from here?Preprint
Akey, J. M. (2009) · Genome Research · doi:10.1101/gr.086652.108 · Cited by 422 · see citing works
Variation and genetic control of protein abundance in humans
Wu, L., Candille, S. I., Choi, Y., Xie, D., Jiang, L., Li-Pook-Than, J., Tang, H., & Snyder, M. (2013) · Nature · doi:10.1038/nature12223 · Cited by 364 · see citing works
Expression profiling in primates reveals a rapid evolution of human transcription factors
Gilad, Y., Oshlack, A., Smyth, G. K., Speed, T. P., & White, K. P. (2006) · Nature · doi:10.1038/nature04559 · Cited by 323 · see citing works
Self-citationRapid evolution of male-biased gene expression in Drosophila
Meiklejohn, C. D., Parsch, J., Ranz, J. M., & Hartl, D. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1630690100 · Cited by 302 · see citing works
RNA sequencing reveals two major classes of gene expression levels in metazoan cells
Hebenstreit, D., Fang, M., Gu, M., Charoensawan, V., van Oudenaarden, A., & Teichmann, S. A. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.28 · Cited by 289 · see citing works
Sex-specific and lineage-specific alternative splicing in primatesPreprint
Blekhman, R., Marioni, J. C., Zumbo, P., Stephens, M., & Gilad, Y. (2009) · Genome Research · doi:10.1101/gr.099226.109 · Cited by 266 · see citing works
Self-citationLemos, B. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi122 · Cited by 256 · see citing works
Comparative Functional Analysis of the Caenorhabditis elegans and Drosophila melanogaster Proteomes
Schrimpf, S. P., Weiss, M., Reiter, L., Ahrens, C. H., Jovanovic, M., Malmström, J., Brunner, E., Mohanty, S., Lercher, M. J., Hunziker, P. E., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000048 · Cited by 229 · see citing works
Absolute SILAC for Accurate Quantitation of Proteins in Complex Mixtures Down to the Attomole Level
Hanke, S., Besir, H., Oesterhelt, D., & Mann, M. (2008) · Journal of Proteome Research · doi:10.1021/pr7007175 · Cited by 216 · see citing works
Protein abundances are more conserved than mRNA abundances across diverse taxa
Laurent, J. M., Vogel, C., Kwon, T., Craig, S. A., Boutz, D. R., Huse, H. K., Nozue, K., Walia, H., Whiteley, M., Ronald, P. C., et al. (2010) · PROTEOMICS · doi:10.1002/pmic.201000327 · Cited by 156 · see citing works
Comparison of Protein and mRNA Expression Evolution in Humans and Chimpanzees
Fu, N., Drinnenberg, I. A., Kelso, J. F., Wu, J., Pääbo, S., Zeng, R., & Khaitovich, P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000216 · Cited by 88 · see citing works
Integrated proteomic and transcriptomic profiling of mouse lung development and Nmyc target genes
Cox, B., Kislinger, T., Wigle, D. A., et al. (2007) · Molecular Systems Biology · doi:10.1038/msb4100151 · Cited by 69 · see citing works
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Research works printed but not linked: 1
- [15]Storey JD Taylor JE Siegmund D Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach Journal of the Royal Statistical Society: Series B (Statistical Methodology) 2004 66 187
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Buccitelli, C., & Selbach, M. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0258-4 · Cited by 1,243 · see citing works
Impact of regulatory variation from RNA to protein
Battle, A., Khan, Z., Wang, S. H., Mitrano, A., Ford, M. J., Pritchard, J. K., & Gilad, Y. (2015) · Science · doi:10.1126/science.1260793 · Cited by 471 · see citing works
Self-citationDynamic profiling of the protein life cycle in response to pathogens
Jovanovic, M., Rooney, M. S., Mertins, P., Przybylski, D., Chevrier, N., Satija, R., Rodriguez, E. H., Fields, A. P., Schwartz, S., Raychowdhury, R., et al. (2015) · Science · doi:10.1126/science.1259038 · Cited by 460 · see citing works
Where Are the Disease-Associated eQTLs?
Umans, B. D., Battle, A., & Gilad, Y. (2021) · Trends in Genetics · doi:10.1016/j.tig.2020.08.009 · Cited by 296 · see citing works
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Wu, Y., Williams, E. G., Dubuis, S., Mottis, A., Jovaisaite, V., Houten, S. M., Argmann, C. A., Faridi, P., Wolski, W., Kutalik, Z., et al. (2014) · Cell · doi:10.1016/j.cell.2014.07.039 · Cited by 244 · see citing works
The evolution and population diversity of human-specific segmental duplications
Dennis, M. Y., Harshman, L., Nelson, B. J., Penn, O., Cantsilieris, S., Huddleston, J., Antonacci, F., Penewit, K., Denman, L., Raja, A., et al. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-016-0069 · Cited by 159 · see citing works
Genetic control of the human brain proteome
Robins, C., Wingo, A. P., Fan, W., Duong, D. M., Meigs, J., Gerasimov, E. S., Dammer, E. B., Cutler, D. J., Jager, P. L. D., Bennett, D. A., et al. (2019) · doi:10.1101/816652 · Cited by 104 · see citing works
- Authors
- Khan, Z., Ford, M. J., Cusanovich, D. A., Mitrano, A., Pritchard, J. K., & Gilad, Y.
- Affiliations
- University of Chicago (US)
- MS Bioworks, LLC, 3950 Varsity Drive, Ann Arbor, MI 48108, USA.
- Howard Hughes Medical Institute (US)
- Corresponding author
- Khan, Zia
- Pritchard, Jonathan K.
- Gilad, Yoav
- Venue
- Science
- Published
- 2013-11-29
- Volume
- 342
- Issue
- 6162
- Pages
- 1100-1104
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3994702
- OpenAlex
- W1968164444
- Cited by
- 240
- References
- 21
- Citations by year
- 2026: 5 · 2025: 20 · 2024: 10 · 2023: 20 · 2022: 15 · 2021: 22 · 2020: 23 · 2019: 17 · 2018: 18 · 2017: 19 · 2016: 15 · 2015: 27 · 2014: 27 · 2013: 1
- FWCI
- 15.44
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Human Genome Research Institute (F32HG006972)
- National Institute of General Medical Sciences (GM077959, R01GM077959)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- primate evolution, mRNA levels, protein abundance, gene expression regulation, transcriptome evolution, human, chimpanzees, rhesus monkeys, lymphoblastoid cell lines, evolutionary constraints
- MeSH terms
- Animals, Pan troglodytes, Gene Expression Regulation, Humans, Macaca mulatta, RNA, Messenger, Selection, Genetic, Species Specificity, Transcription, Genetic, Protein Biosynthesis, Evolution, Molecular
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