The mammalian inactive X chromosome (Xi) condenses into a bipartite structure 
with two superdomains of frequent long-range contacts, separated by a hinge 
region. Using Hi-C in edited mouse cells with allelic deletions or inversions 
within the hinge, here we show that the conserved Dxz4 locus is necessary to 
maintain this bipartite structure. Dxz4 orientation controls the distribution of 
contacts on the Xi, as shown by a massive reversal in long-range contacts after 
Dxz4 inversion. Despite an increase in CTCF binding and chromatin accessibility 
on the Xi in Dxz4-edited cells, only minor changes in TAD structure and gene 
expression were detected, in accordance with multiple epigenetic mechanisms 
ensuring X silencing. We propose that Dxz4 represents a structural platform for 
frequent long-range contacts with multiple loci in a direction dictated by the 
orientation of its bank of CTCF motifs, which may work as a ratchet to form the 
distinctive bipartite structure of the condensed Xi.