Ontogenesis of the tear drainage system requires Prickle1-driven polarized basement membrane deposition

Development. 2020 Nov 30;147(22):dev191726. doi: 10.1242/dev.191726.

Abstract

In terrestrial animals, the lacrimal drainage apparatus evolved to serve as conduits for tear flow; however, little is known about the ontogenesis of this system. Here, we define the anatomy of the fully formed tear duct in mice, characterize crucial morphogenetic events for the development of tear duct components and identify the site for primordial tear duct (PTD) initiation. We report that the PTD originates from the orbital lacrimal lamina, a junction formed by the epithelia of the maxillary and lateral nasal processes. We demonstrate that Prickle1, a key component of planar cell polarity signaling, is expressed in progenitors of the PTD and throughout tear duct morphogenesis. Disruption of Prickle1 stalls tear duct elongation; in particular, the loss of basement membrane deposition and aberrant cytoplasmic accumulation of laminin are salient. Altered cell adhesion, cytoskeletal transport systems, vesicular transport systems and cell axis orientation in Prickle1 mutants support the role of Prickle1 in planar cell polarity. Taken together, our results highlight a crucial role of Prickle1-mediated polarized basement membrane secretion and deposition in PTD elongation.

Keywords: Basement membrane; Ontogenesis; Planar cell polarity; Polarized deposition; Prickle1; Tear duct.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Basement Membrane / cytology
  • Basement Membrane / embryology*
  • Cell Adhesion / physiology
  • Cell Polarity / physiology*
  • Cytoskeleton / genetics
  • Cytoskeleton / metabolism
  • LIM Domain Proteins / genetics
  • LIM Domain Proteins / metabolism*
  • Mice
  • Nasolacrimal Duct / cytology
  • Nasolacrimal Duct / embryology*
  • Organogenesis / physiology*

Substances

  • Adaptor Proteins, Signal Transducing
  • LIM Domain Proteins
  • Prickle1 protein, mouse