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Molecular Neurobiology

, Volume 55, Issue 3, pp 1871–1904 | Cite as

Evolution of Brain Active Gene Promoters in Human Lineage Towards the Increased Plasticity of Gene Regulation

  • Konstantin V. Gunbin
  • Mikhail P. Ponomarenko
  • Valentin V. Suslov
  • Fedor Gusev
  • Gennady G. Fedonin
  • Evgeny I. Rogaev
Article

Abstract

Adaptability to a variety of environmental conditions is a prominent feature of Homo sapiens. We hypothesize that this feature can be explained by evolutionary changes in gene promoters active in the brain prefrontal cortex leading to a more flexible gene regulation network. The genotype-dependent range of gene expression can be broader in humans than in other higher primates. Thus, we searched for specific signatures of evolutionary changes in promoter architectures of multiple hominid genes, including the genes active in human cortical neurons that may indicate an increase of variability of gene expression rather than just changes in the level of expression, such as downregulation or upregulation of the genes. We performed a whole-genome search for genetic-based alterations that may impact gene regulation “flexibility” in a process of hominids evolution, such as (i) CpG dinucleotide content, (ii) predicted nucleosome-DNA dissociation constant, and (iii) predicted affinities for TATA-binding protein (TBP) in gene promoters. We tested all putative promoter regions across the human genome and especially gene promoters in active chromatin state in neurons of prefrontal cortex, the brain region critical for abstract thinking and social and behavioral adaptation. Our data imply that the origin of modern man has been associated with an increase of flexibility of promoter-driven gene regulation in brain. In contrast, after splitting from the ancestral lineages of H. sapiens, the evolution of ape species is characterized by reduced flexibility of gene promoter functioning, underlying reduced variability of the gene expression.

Keywords

Norm of reaction Genotype Core promoters Gene evolution Gene regulation Hominids 

Notes

Acknowledgements

This study was partly supported by grant 14.B25.31.0033 from the Government of the Russian Federation (Resolution No. 220) and by the Russian Science Foundation Grant No. 14-44-00077 (Alzheimer’s disease gene characteristics). MPP was partly supported by Grant 17-04-00501 from the Russian Foundation for Basic Research. VVS was partly supported by the project VI.61.1.2 from the Russian State Budget. EIR was supported, in part, by NIH/NIA AG029360.

Authors’ Contributions

KVG performed the analyses, designed, and coordinated the bioinformatics part of the work. MPP provided the software for TBP to DNA and for nucleosome to DNA-binding enumeration for analyzed sequences. VVS, KVG, and MPP suggested the interpretations. FG and GGF contributed to the selection of the promoters marked by H3K4me3. EIR coordinated the data management for the work and analysis and presentation of results in the paper. EIR, KVG, VVS, and MPP contributed significantly to the writing of this paper. All authors read and approved the manuscript.

Supplementary material

12035_2017_427_MOESM1_ESM.xlsx (2.2 mb)
File S1 Lists of human gene promoters and their chromosomal location (GRCh37). (XLSX 2253 kb)
12035_2017_427_MOESM2_ESM.txt (15.6 mb)
File S2 Alignments of neural-specific promoters. (TXT 15,961 kb)
12035_2017_427_MOESM3_ESM.xlsx (14.2 mb)
File S3 List of detected (largest per gene) evolutionary changes in gene promoters. (XLSX 14,569 kb)
12035_2017_427_MOESM4_ESM.xlsx (2.4 mb)
File S4 The results of functional enrichment analysis of gene sets characterized by significant evolutionary changes in their promoters (threshold is equal to >0.05 changes per position) obtained by DAVID 6.7 web server. (XLSX 2470 kb)
12035_2017_427_MOESM5_ESM.xlsx (14 kb)
File S5 List of genes associated with Alzheimer’s disease (based on MalaCards DB data and [107]). (XLSX 14 kb)
12035_2017_427_MOESM6_ESM.docx (152 kb)
ESM 1 Figs. A–E; Tables A–D. Fig. A. The fraction of promoters (%) with CpG dinucleotide emergence on each branch of the hominid tree per 1 Myr of evolution. Fig. B. The fraction of promoters (%) with CpG dinucleotide disappearance on each branch of the hominid tree per 1 Myr of evolution. Fig. C. The distributions of per promoter fraction of mutated CpG dinucleotides (single-nucleotide substitutions and indels) on each branch of the hominid tree per 1 Myr of evolution. Fig. D. Percentage of polymorphic positions (ancestral and extant) among the positions with nucleotide differences on the hominid tree branches (based on [61]). Fig. E. The results of functional enrichment analysis of genes with evolved promoters belonging to shared promoters set (acting in humans) summarized by REVIGO [64]. Table A. Statistical significance (χ 2) of inequality between fraction of genes with the disappearance and appearance of CpG dinucleotides in the descendent on each branch of the hominid tree. Table B. Comparison of the evolution rate (per 1 Myr) of the structural promoter characteristics between two groups of hominids tree branches the “ancestral” (A1_A2, A2_A3, A3_human) and “terminal” (A1_orangutan, A2_gorilla, A3_chimpanzee). Table C. Statistical significance (χ 2) of the inequality between the fractions of promoters with increased and decreased nucleosomal or TBP-binding potential in the descendant tree nodes comparing to ancestral ones. Table D. Comparison of the evolution rate (per 1 Myr) of the functional promoter characteristics between two groups of hominids tree branches the “ancestral” (A1_A2, A2_A3, A3_human) and “terminal” (A1_orangutan, A2_gorilla, A3_chimpanzee). (DOCX 151 kb)

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Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Konstantin V. Gunbin
    • 1
    • 2
    • 3
  • Mikhail P. Ponomarenko
    • 2
    • 3
  • Valentin V. Suslov
    • 2
    • 3
  • Fedor Gusev
    • 1
    • 4
    • 5
  • Gennady G. Fedonin
    • 4
    • 6
  • Evgeny I. Rogaev
    • 1
    • 4
    • 5
  1. 1.Center of Brain Neurobiology and NeurogeneticsInstitute of Cytology and Genetics SB RASNovosibirskRussia
  2. 2.Systems Biology DepartmentInstitute of Cytology and Genetics SB RASNovosibirskRussia
  3. 3.Novosibirsk State UniversityNovosibirskRussia
  4. 4.Vavilov Institute of General Genetics RASMoscowRussia
  5. 5.Brudnick Neuropsychiatric Research InstituteUniversity of Massachusetts Medical SchoolWorcesterUSA
  6. 6.Institute for Information Transmission Problems (the Kharkevich Institute) RASMoscowRussia

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