Human Brain Evolution: Emerging Roles for Regulatory DNA and RNA

Overview

Journal Curr Opin Neurobiol

Specialties Biology
Neurology

Date 2021 Dec 3

PMID 34861533

Citations 7

Authors

Jing Liu

Federica Mosti

Debra L Silver

Affiliations

Soon will be listed here.

Abstract

Humans diverge from other primates in numerous ways, including their neuroanatomy and cognitive capacities. Human-specific features are particularly prominent in the cerebral cortex, which has undergone an expansion in size and acquired unique cellular composition and circuitry. Human-specific gene expression is postulated to explain neocortical anatomical differences across evolution. In particular, noncoding regulatory loci are strongly linked to human traits, including progenitor proliferation and cortical size. In this review, we highlight emerging noncoding elements implicated in human cortical evolution, including roles for regulatory DNA and RNA. Further, we discuss the association of human-specific genetic changes with neurodevelopmental diseases.

Citing Articles

The Human Accelerated Region HAR202 Controls NPAS3 Expression in the Developing Forebrain Displaying Differential Enhancer Activity Between Modern and Archaic Human Sequences.

Caporale A, Cinalli A, Rubinstein M, Franchini L Mol Biol Evol. 2024; 41(10).

PMID: 39241178 PMC: 11461159. DOI: 10.1093/molbev/msae186.

Deciphering the Role of Rapidly Evolving Conserved Elements in Primate Brain Development and Exploring Their Potential Involvement in Alzheimer's Disease.

Hu B, Zhuang X, Zhou L, Zhang G, Cooper D, Wu D Mol Biol Evol. 2024; 41(1).

PMID: 38175672 PMC: 10798191. DOI: 10.1093/molbev/msae001.

Celf4 controls mRNA translation underlying synaptic development in the prenatal mammalian neocortex.

Salamon I, Park Y, Miskic T, Kopic J, Matteson P, Page N Nat Commun. 2023; 14(1):6025.

PMID: 37758766 PMC: 10533865. DOI: 10.1038/s41467-023-41730-8.

Evolution and dysfunction of human cognitive and social traits: A transcriptional regulation perspective.

Zug R, Uller T Evol Hum Sci. 2023; 4:e43.

PMID: 37588924 PMC: 10426018. DOI: 10.1017/ehs.2022.42.

Keeping the balance: Trade-offs between human brain evolution, autism, and schizophrenia.

Dunski E, Pekowska A Front Genet. 2022; 13:1009390.

PMID: 36479251 PMC: 9719942. DOI: 10.3389/fgene.2022.1009390.

References

Santos-Rodriguez G, Voineagu I, Weatheritt R . Evolutionary dynamics of circular RNAs in primates. Elife. 2021; 10. PMC: 8516421. DOI: 10.7554/eLife.69148. View

Diaz J, Siththanandan V, Lu V, Gonzalez-Nava N, Pasquina L, MacDonald J . An evolutionarily acquired microRNA shapes development of mammalian cortical projections. Proc Natl Acad Sci U S A. 2020; 117(46):29113-29122. PMC: 7682328. DOI: 10.1073/pnas.2006700117. View

Capra J, Erwin G, Mckinsey G, Rubenstein J, Pollard K . Many human accelerated regions are developmental enhancers. Philos Trans R Soc Lond B Biol Sci. 2013; 368(1632):20130025. PMC: 3826498. DOI: 10.1098/rstb.2013.0025. View

Xu K, Schadt E, Pollard K, Roussos P, Dudley J . Genomic and network patterns of schizophrenia genetic variation in human evolutionary accelerated regions. Mol Biol Evol. 2015; 32(5):1148-60. PMC: 4408416. DOI: 10.1093/molbev/msv031. View

Gokhman D, Mishol N, de Manuel M, de Juan D, Shuqrun J, Meshorer E . Reconstructing Denisovan Anatomy Using DNA Methylation Maps. Cell. 2019; 179(1):180-192.e10. DOI: 10.1016/j.cell.2019.08.035. View

Tilot A, Khramtsova E, Liang D, Grasby K, Jahanshad N, Painter J . The Evolutionary History of Common Genetic Variants Influencing Human Cortical Surface Area. Cereb Cortex. 2020; 31(4):1873-1887. PMC: 7945014. DOI: 10.1093/cercor/bhaa327. View

Baresic A, Nash A, Dahoun T, Howes O, Lenhard B . Understanding the genetics of neuropsychiatric disorders: the potential role of genomic regulatory blocks. Mol Psychiatry. 2019; 25(1):6-18. PMC: 6906185. DOI: 10.1038/s41380-019-0518-x. View

Price A, Collado-Torres L, Ivanov N, Xia W, Burke E, Shin J . Divergent neuronal DNA methylation patterns across human cortical development reveal critical periods and a unique role of CpH methylation. Genome Biol. 2019; 20(1):196. PMC: 6761727. DOI: 10.1186/s13059-019-1805-1. View

Camp J, Badsha F, Florio M, Kanton S, Gerber T, Wilsch-Brauninger M . Human cerebral organoids recapitulate gene expression programs of fetal neocortex development. Proc Natl Acad Sci U S A. 2015; 112(51):15672-7. PMC: 4697386. DOI: 10.1073/pnas.1520760112. View

10.

Otani T, Marchetto M, Gage F, Simons B, Livesey F . 2D and 3D Stem Cell Models of Primate Cortical Development Identify Species-Specific Differences in Progenitor Behavior Contributing to Brain Size. Cell Stem Cell. 2016; 18(4):467-80. PMC: 4826446. DOI: 10.1016/j.stem.2016.03.003. View

11.

Agoglia R, Sun D, Birey F, Yoon S, Miura Y, Sabatini K . Primate cell fusion disentangles gene regulatory divergence in neurodevelopment. Nature. 2021; 592(7854):421-427. PMC: 8719633. DOI: 10.1038/s41586-021-03343-3. View

12.

Rajman M, Schratt G . MicroRNAs in neural development: from master regulators to fine-tuners. Development. 2017; 144(13):2310-2322. DOI: 10.1242/dev.144337. View

13.

Dong R, Ma X, Chen L, Yang L . Increased complexity of circRNA expression during species evolution. RNA Biol. 2016; 14(8):1064-1074. PMC: 5680680. DOI: 10.1080/15476286.2016.1269999. View

14.

Haygood R, Fedrigo O, Hanson B, Yokoyama K, Wray G . Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet. 2007; 39(9):1140-4. DOI: 10.1038/ng2104. View

15.

Zimmer-Bensch G . Emerging Roles of Long Non-Coding RNAs as Drivers of Brain Evolution. Cells. 2019; 8(11). PMC: 6912723. DOI: 10.3390/cells8111399. View

16.

King M, Wilson A . Evolution at two levels in humans and chimpanzees. Science. 1975; 188(4184):107-16. DOI: 10.1126/science.1090005. View

17.

Kamm G, Pisciottano F, Kliger R, Franchini L . The developmental brain gene NPAS3 contains the largest number of accelerated regulatory sequences in the human genome. Mol Biol Evol. 2013; 30(5):1088-102. PMC: 3670734. DOI: 10.1093/molbev/mst023. View

18.

Godlewski J, Lenart J, Salinska E . MicroRNA in Brain pathology: Neurodegeneration the Other Side of the Brain Cancer. Noncoding RNA. 2019; 5(1). PMC: 6468660. DOI: 10.3390/ncrna5010020. View

19.

Trujillo C, Rice E, Schaefer N, Chaim I, Wheeler E, Madrigal A . Reintroduction of the archaic variant of in cortical organoids alters neurodevelopment. Science. 2021; 371(6530). PMC: 8006534. DOI: 10.1126/science.aax2537. View

20.

Somel M, Liu X, Tang L, Yan Z, Hu H, Guo S . MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates. PLoS Biol. 2011; 9(12):e1001214. PMC: 3232219. DOI: 10.1371/journal.pbio.1001214. View