Mosaic cis-regulatory evolution drives transcriptional partitioning of HERVH endogenous retrovirus in the human embryo.
HERVH
embryonic stem cells
endogenous retroviruses
genetics
genomics
human
primate evolution
transposable elements
Journal
eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614
Informations de publication
Date de publication:
18 02 2022
18 02 2022
Historique:
received:
14
12
2021
accepted:
17
02
2022
pubmed:
19
2
2022
medline:
30
4
2022
entrez:
18
2
2022
Statut:
epublish
Résumé
The human endogenous retrovirus type-H (HERVH) family is expressed in the preimplantation embryo. A subset of these elements are specifically transcribed in pluripotent stem cells where they appear to exert regulatory activities promoting self-renewal and pluripotency. How HERVH elements achieve such transcriptional specificity remains poorly understood. To uncover the sequence features underlying HERVH transcriptional activity, we performed a phyloregulatory analysis of the long terminal repeats (LTR7) of the HERVH family, which harbor its promoter, using a wealth of regulatory genomics data. We found that the family includes at least eight previously unrecognized subfamilies that have been active at different timepoints in primate evolution and display distinct expression patterns during human embryonic development. Notably, nearly all HERVH elements transcribed in ESCs belong to one of the youngest subfamilies we dubbed LTR7up. LTR7 sequence evolution was driven by a mixture of mutational processes, including point mutations, duplications, and multiple recombination events between subfamilies, that led to transcription factor binding motif modules characteristic of each subfamily. Using a reporter assay, we show that one such motif, a predicted SOX2/3 binding site unique to LTR7up, is essential for robust promoter activity in induced pluripotent stem cells. Together these findings illuminate the mechanisms by which HERVH diversified its expression pattern during evolution to colonize distinct cellular niches within the human embryo.
Identifiants
pubmed: 35179489
doi: 10.7554/eLife.76257
pii: 76257
pmc: PMC8912925
doi:
pii:
Banques de données
GEO
['GSE61475', 'GSE69647', 'GSE117395', 'GSE78099', 'GSE54726', 'GSE64758', 'GSE125553', 'GSE36552', 'GSE66507']
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM122550
Pays : United States
Organisme : NIGMS NIH HHS
ID : P01 GM099117
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM112972
Pays : United States
Organisme : NHGRI NIH HHS
ID : U01 HG009391
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Informations de copyright
© 2022, Carter et al.
Déclaration de conflit d'intérêts
TC, MS, GD, JC, JR, CF No competing interests declared
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