An Ancestral miR-1304 Allele Present in Neanderthals Regulates Genes Involved in Enamel Formation and Could Explain Dental Differences with Modern Humans
Open accessAbstract
Genetic changes in regulatory elements are likely to result in phenotypic effects that might explain population-specific as well as species-specific traits. MicroRNAs (miRNAs) are posttranscriptional repressors involved in the control of almost every biological process. These small noncoding RNAs are present in various phylogenetic groups, and a large number of them remain highly conserved at the sequence level. MicroRNA-mediated regulation depends on perfect matching between the seven nucleotides of its seed region and the target sequence usually located at the 3' untranslated region of the regulated gene. Hence, even single changes in seed regions are predicted to be deleterious as they may affect miRNA target specificity. In accordance to this, purifying selection has strongly acted on these regions. Comparison between the genomes of present-day humans from various populations, Neanderthal, and other nonhuman primates showed an miRNA, miR-1304, that carries a polymorphism on its seed region. The ancestral allele is found in Neanderthal, nonhuman primates, at low frequency (~5%) in modern Asian populations and rarely in Africans. Using miRNA target site prediction algorithms, we found that the derived allele increases the number of putative target genes for the derived miRNA more than ten-fold, indicating an important functional evolution for miR-1304. Analysis of the predicted targets for derived miR-1304 indicates an association with behavior and nervous system development and function. Two of the predicted target genes for the ancestral miR-1304 allele are important genes for teeth formation, enamelin, and amelotin. MicroRNA overexpression experiments using a luciferase-based assay showed that the ancestral version of miR-1304 reduces the enamelin- and amelotin-associated reporter gene expression by 50%, whereas the derived miR-1304 does not have any effect. Deletion of the corresponding target sites for miR-1304 in these dental genes avoided their repression, which further supports their regulation by the ancestral miR-1304. Morphological studies described several differences in the dentition of Neanderthals and present-day humans like slower dentition timing and thicker enamel for present-day humans. The observed miR-1304-mediated regulation of enamelin and amelotin could at least partially underlie these differences between the two Homo species as well as other still-unraveled phenotypic differences among modern human populations.
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MiRNA function can be affected by variants introgressed from Neanderthals.
“MiRNA seed regions are under significant background selection [47] and their function can be affected by variants introgressed from Neanderthals [48].”
From Denisovan and Neanderthal archaic introgression differentially impacted the genetics of complex traits in modern populations (2022) · cites this paper as [48]
The Abstract reports that a miR-1304 seed-region variant changes predicted target specificity, supporting an effect on miRNA function. The Discussion says Neanderthal admixture could have reintroduced the ancestral allele into Asian populations, but does not establish that it was introgressed; the allele also occurs in Africans. (LLM, conf=0.86)
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“Studies conducted primarily on Neanderthal introgressed DNA have suggested a non-negligible contribution to gene expression variation in modern humans [7, 8, 17], with repeated examples of Neanderthal archaic variants falling within regulatory elements or the seed region of mature micro-RNAs predicted to affect transc…”
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BackgroundInfluential
- Authors
- Lopez-Valenzuela, M., Ramirez, O., Rosas, A., Garcia-Vargas, S., de la Rasilla, M., Lalueza-Fox, C., & Espinosa-Parrilla, Y.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- ORCID
- Rosas, A.
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-01-27
- Volume
- 29
- Issue
- 7
- Pages
- 1797-1806
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- OpenAlex
- W2024631012
- Cited by
- 31
- References
- 66
- Citations by year
- 2024: 2 · 2022: 3 · 2021: 4 · 2020: 1 · 2019: 4 · 2018: 1 · 2017: 3 · 2016: 5 · 2014: 4 · 2013: 3 · 2012: 1
- FWCI
- 1.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Biology and Evolution (publishedVersion)
- PubMed (publishedVersion)
- Consultation of the Doctoral Thesis Database (TESEO) (Ministerio de Educación, Cultura y Deporte) (submittedVersion, cc-by-nc-nd)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- European Commission (236836)
- Generalitat de Catalunya
- European Regional Development Fund
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › dental development and anomalies
- Social Sciences › Anthropology › Pleistocene-Era Hominins and Archaeology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- Neanderthals, amelogenesis, enamelin, amelotin, dental morphology, purifying selection, post-transcriptional regulation, non-human primates, human evolution, enamel thickness, brain development, luciferase reporter
- MeSH terms
- Alleles, Animals, Pan troglodytes, Dental Enamel, Dental Enamel Proteins, Gorilla gorilla, Humans, Macaca mulatta, Regulatory Sequences, Nucleic Acid, 3' Untranslated Regions, MicroRNAs, Neanderthals
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