The combined action of CTCF and its testis-specific paralog BORIS is essential for spermatogenesis

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Abstract

CTCF is a key organizer of the 3D genome. Its specialized paralog, BORIS, heterodimerizes with CTCF but is expressed only in male germ cells and in cancer states. Unexpectedly, BORIS-null mice have only minimal germ cell defects. To understand the CTCF-BORIS relationship, mouse models with varied CTCF and BORIS levels were generated. Whereas Ctcf+/+Boris+/+, Ctcf+/−Boris+/+, and Ctcf+/+Boris−/− males are fertile, Ctcf+/−Boris−/− (Compound Mutant; CM) males are sterile. Testes with combined depletion of both CTCF and BORIS show reduced size, defective meiotic recombination, increased apoptosis, and malformed spermatozoa. Although CM germ cells exhibit only 25% of CTCF WT expression, chromatin binding of CTCF is preferentially lost from CTCF-BORIS heterodimeric sites. Furthermore, CM testes lose the expression of a large number of spermatogenesis genes and gain the expression of developmentally inappropriate genes that are “toxic” to fertility. Thus, a combined action of CTCF and BORIS is required to both repress pre-meiotic genes and activate post-meiotic genes for a complete spermatogenesis program.

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Rivero-Hinojosa, S., Pugacheva, E. M., Kang, S., Méndez-Catalá, C. F., Kovalchuk, A. L., Strunnikov, A. V., … Lobanenkov, V. V. (2021). The combined action of CTCF and its testis-specific paralog BORIS is essential for spermatogenesis. Nature Communications, 12(1). https://doi.org/10.1038/s41467-021-24140-6

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