MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates
Open accessAbstract
While multiple studies have reported the accelerated evolution of brain gene expression in the human lineage, the mechanisms underlying such changes are unknown. Here, we address this issue from a developmental perspective, by analyzing mRNA and microRNA (miRNA) expression in two brain regions within macaques, chimpanzees, and humans throughout their lifespan. We find that constitutive gene expression divergence (species differences independent of age) is comparable between humans and chimpanzees. However, humans display a 3-5 times faster evolutionary rate in divergence of developmental patterns, compared to chimpanzees. Such accelerated evolution of human brain developmental patterns (i) cannot be explained by life-history changes among species, (ii) is twice as pronounced in the prefrontal cortex than the cerebellum, (iii) preferentially affects neuron-related genes, and (iv) unlike constitutive divergence does not depend on cis-regulatory changes, but might be driven by human-specific changes in expression of trans-acting regulators. We show that developmental profiles of miRNAs, as well as their target genes, show the fastest rates of human-specific evolutionary change, and using a combination of computational and experimental methods, we identify miR-92a, miR-454, and miR-320b as possible regulators of human-specific neural development. Our results suggest that different mechanisms underlie adaptive and neutral transcriptome divergence, and that changes in the expression of a few key regulators may have been a major driving force behind rapid evolution of the human brain.
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miRNA mediated regulation is implicated in evolution of gene expression across postnatal development of prefrontal cortex and cerebellum in humans, chimpanzees, and macaques.
“miRNA mediated regulation was also implicated in the evolution of gene expression across the postnatal development of the prefrontal cortex and cerebellum in humans, chimpanzees, and macaques (Somel et al., 2011).”
From The Cellular and Molecular Landscapes of the Developing Human Central Nervous System (2016) · cites this paper as Somel et al., 2011
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- Authors
- Somel, M., Liu, X., Tang, L., Yan, Z., Hu, H., Guo, S., Jiang, X., Zhang, X., Xu, G., Xie, G., Li, N., Hu, Y., Chen, W., Pääbo, S., & Khaitovich, P.
- Affiliations
- Chinese Academy of Sciences (CN)
- Max Delbrück Center (DE)
- Max Planck Institute for Evolutionary Anthropology (DE)
- Corresponding author
- Pääbo, Svante
- Khaitovich, Philipp
- ORCID
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-12-06
- Volume
- 9
- Issue
- 12
- Pages
- e1001214
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC3232219
- OpenAlex
- W2034299131
- Cited by
- 232
- References
- 56
- Citations by year
- 2026: 8 · 2025: 8 · 2024: 6 · 2023: 9 · 2022: 9 · 2021: 25 · 2020: 15 · 2019: 15 · 2018: 14 · 2017: 19 · 2016: 14 · 2015: 15 · 2014: 24 · 2013: 25 · 2012: 25
- FWCI
- 8.16
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Figshare (submittedVersion, cc-by)
- OpenMETU (Middle East Technical University) (submittedVersion, cc-by-nc-nd)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- National Natural Science Foundation of China
- Chinese Academy of Sciences (KSCX2-YW-R)
- Ministry of Science and Technology of the People's Republic of China
- Universität Zürich
- Directorate for Biological Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- microRNA, human brain evolution, brain development, transcriptome divergence, miRNA target genes, prefrontal cortex, cerebellum, miR-92a, miR-320b, trans-acting regulators, cis-regulatory evolution, macaque, chimpanzees
- MeSH terms
- Aged, Animals, Brain, Cerebellum, Pan troglodytes, Humans, Infant, Newborn, Macaca mulatta, Nerve Tissue Proteins, Neurons, Organ Specificity, RNA, Messenger, Species Specificity, Tissue Banks, Prefrontal Cortex, Gene Expression Regulation, Developmental, Evolution, Molecular, Computational Biology, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, MicroRNAs, Neurogenesis, Young Adult
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