DOI: 10.1073/pnas.2605383123 ISSN: 0027-8424

Successful oocyte transport through the oviduct does not depend on the longitudinal alignment of oviduct epithelial folds

Fumiko Matsukawa Usami, Masaki Arata, Kagayaki Kato, Dongbo Shi, Sanae Oka, Yingzi Yang, Toshihiko Fujimori

The luminal epithelium of the oviduct exhibits ciliary beating oriented along the ovary–uterus (O–U) axis, driving oocyte transport toward the uterus. Longitudinal epithelial folds have also been proposed to facilitate this transport, but their functional contribution has not been tested because the mechanisms that orient these folds remain unclear. In this study, we found that in Vangl1 gt/gt oviducts, which lack the core planar cell polarity (PCP) protein VANGL1, ciliary beating orientation is largely preserved, whereas longitudinal folds are disrupted. Despite fold malformation, Vangl1 gt/gt females were able to produce offspring, suggesting that oocyte transport to the uterus can occur even when longitudinal fold alignment is disrupted. Polarized distributions of core PCP proteins at cell boundaries have been proposed to establish O–U–oriented ciliary beating and cell elongation, and theoretical work predicts that O–U–aligned cell elongation drives longitudinal fold formation. Consistent with this, our three-dimensional cell-shape analysis revealed a loss of cell elongation in Vangl1 gt/gt oviducts. Moreover, although other core PCP proteins remained polarized, their polarity axes were misaligned with ciliary orientation in Vangl1 gt/gt oviducts, suggesting that ciliary orientation can be guided by mechanisms that are at least partly independent of canonical core-protein polarity. Together, our findings help define the physiological contribution of longitudinal folds and illuminate how distinct polarity systems—fold orientation, cell elongation, and ciliary beating—are established and coordinated in the oviduct.

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