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Chromosome Research

, Volume 26, Issue 1–2, pp 61–84 | Cite as

Contribution of transposable elements and distal enhancers to evolution of human-specific features of interphase chromatin architecture in embryonic stem cells

  • Gennadi V. Glinsky
Original Article

Abstract

Transposable elements have made major evolutionary impacts on creation of primate-specific and human-specific genomic regulatory loci and species-specific genomic regulatory networks (GRNs). Molecular and genetic definitions of human-specific changes to GRNs contributing to development of unique to human phenotypes remain a highly significant challenge. Genome-wide proximity placement analysis of diverse families of human-specific genomic regulatory loci (HSGRL) identified topologically associating domains (TADs) that are significantly enriched for HSGRL and designated rapidly evolving in human TADs. Here, the analysis of HSGRL, hESC-enriched enhancers, super-enhancers (SEs), and specific sub-TAD structures termed super-enhancer domains (SEDs) has been performed. In the hESC genome, 331 of 504 (66%) of SED-harboring TADs contain HSGRL and 68% of SEDs co-localize with HSGRL, suggesting that emergence of HSGRL may have rewired SED-associated GRNs within specific TADs by inserting novel and/or erasing existing non-coding regulatory sequences. Consequently, markedly distinct features of the principal regulatory structures of interphase chromatin evolved in the hESC genome compared to mouse: the SED quantity is 3-fold higher and the median SED size is significantly larger. Concomitantly, the overall TAD quantity is increased by 42% while the median TAD size is significantly decreased (p = 9.11E-37) in the hESC genome. Present analyses illustrate a putative global role for transposable elements and HSGRL in shaping the human-specific features of the interphase chromatin organization and functions, which are facilitated by accelerated creation of novel transcription factor binding sites and new enhancers driven by targeted placement of HSGRL at defined genomic coordinates. A trend toward the convergence of TAD and SED architectures of interphase chromatin in the hESC genome may reflect changes of 3D-folding patterns of linear chromatin fibers designed to enhance both regulatory complexity and functional precision of GRNs by creating predominantly a single gene (or a set of functionally linked genes) per regulatory domain structures. Collectively, present analyses reveal critical evolutionary contributions of transposable elements and distal enhancers to creation of thousands primate- and human-specific elements of a chromatin folding code, which defines the 3D context of interphase chromatin both restricting and facilitating biological functions of GRNs.

Keywords

Topologically associating domains Super-enhancers Super-enhancer domains Human-specific genomic regulatory sequences Chromatin loops Human ESC Pluripotent state regulators NANOG POU5F1 (OCT4) CTCF Methyl-cytosine deamination Recombination Alu elements LTR7 RNAs L1 retrotransposition LINE LTR LTR7/HERVH LTR5_HS/HERVK Evolution of Modern Humans 

Abbreviations

5hmC

5-Hydromethylcytosine

CTCF

CCCTC-binding factor

DHS

DNase hypersensitivity sites

FHSRR

fixed human-specific regulatory regions

GRNs

genomic regulatory networks

HAR

human-accelerated regions

hCONDEL

human-specific conserved deletions

hESC

human embryonic stem cells

HSGRL

human-specific genomic regulatory loci

HSNBS

human-specific NANOG-binding sites

HSTFBS

human-specific transcription factor-binding sites

LAD

lamina-associated domain

LINE

long interspersed nuclear element

lncRNA

long non-coding RNA

LTR

long terminal repeat

MADE

methylation-associated DNA editing

mC

methylcytosine

mESC

mouse embryonic stem cells

NANOG

Nanog homeobox

Nt

nucleotide

POU5F1

POU class 5 homeobox 1

TAD

topologically associating domains

TE

transposable elements

TF

transcription factor

SE

super-enhancers

SED

super-enhancer domains

Notes

Acknowledgements

This work was made possible by the open public access policies of major grant funding agencies and international genomic databases and the willingness of many investigators worldwide to share their primary research data. I would like to thank my colleagues for their valuable critical contributions during the informal review and formal peer review process of this work.

Author contributions

This is a single author contribution. All elements of this work, including the conception of ideas, formulation, and development of concepts, execution of experiments, analysis of data, and writing of the paper, were performed by the author.

Supplementary material

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© Springer Science+Business Media B.V., part of Springer Nature 2018
corrected publication February/2018

Authors and Affiliations

  1. 1.Institute of Engineering in MedicineUniversity of California, San DiegoLa JollaUSA

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