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Despite significant progress in structural and functional characterization ofhuman genome, understanding of mechanisms underlying the genetic basis of humanphenotypic uniqueness remains limited. We report that non-randomly distributedtransposable element-derived sequences, most notably HERV-H/LTR7 and L1HS, areassociated with creation of 99.8% unique to human transcription factor bindingsites in genome of embryonic stem cells (ESC). 4,094 unique to human regulatoryloci display selective and site-specific binding of critical regulators (NANOG,POU5F1, CTCF, Lamin B1) and are preferentially placed within the matrix oftranscriptionally active DNA segments hyper-methylated in ESC. Unique to humanNANOG-binding sites are enriched near the rapidly evolving in primatesprotein-coding genes regulating brain size, pluripotency lncRNAs, hESCenhancers, and 5-hydroxymethylcytosine-harboring regions immediately adjacentto binding sites. We propose a proximity placement model explaining how 33-47%excess of NANOG and POU5F1 proteins immobilized on a DNA scaffold may play afunctional role at distal regulatory elements.

Identification and characterization of unique to human regulatory  sequences in embryonic stem cells reveal associations with transposable  elements, distal enhancers, non-coding RNA, and DNA methylation-driven  mechanisms of genome editing