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A counting process senses the X chromosome/autosome ratio and ensures that X chromosome inactivation (XCI) initiates in the early female (XX) embryo and in differentiating female ES cells but not in their male (XY) counterparts. Counting depends on the X inactivation center (Xic ), which contains theXist gene encoding a nuclear RNA, which coats the inactive X chromosome and induces gene silencing. A 37-kb sequence lying 3′ to theXist gene is known to prevent initiation of XCI in male differentiating ES cells. This region contains the major and minor promoters of theTsix gene, which runs antisense toXist , and theDXPas34 tandem repeat lying close to theTsix major promoter. We have addressed the role of these elements in counting by using male ES cells. Targeted deletion ofDXPas34 impaired recruitment of RNA-polymerase II and TFIIB at theTsix major promoter, resulting in low levels ofTsix expression in ES cells and moderate ectopic initiation of XCI upon differentiation. A deletion extending 3′ toXist and including theTsix major promoter resulted in almost complete impairment ofTsix transcription and in efficient ectopic XCI upon differentiation of male ES cells. Internal deletions within theTsix gene did not affect significantly the level of antisense transcription withinXist and had only minor effects upon differentiation. Our results identify a function forDXPas34 in murine XCI and demonstrate the critical role ofTsix transcription in preventing XCI in differentiating male ES cells and in normal functioning of the counting pathway.

An essential role for the DXPas34 tandem repeat and Tsix transcription in the counting process of X chromosome inactivation