Luminal matrices: An inside view on organ morphogenesis

Abstract

Tubular epithelia come in various shapes and sizes to accommodate the specific needs for transport, excretion and absorption in multicellular organisms. The intestinal tract, glandular organs and conduits for liquids and gases are all lined by a continuous layer of epithelial cells, which form the boundary of the luminal space. Defects in epithelial architecture and lumen dimensions will impair transport and can lead to serious organ malfunctions. Not surprisingly, multiple cellular and molecular mechanisms participate in controlling size and form of tubular epithelial structures. One intriguing aspect of epithelial organ formation is the coordinate behavior of individual cells as they mold the mature lumen. Here, we focus on recent findings, primarily from Drosophila, demonstrating that informative cues can emanate from the developing organ lumen in the form of solid luminal material. The luminal material is produced by the surrounding epithelium and helps to coordinate changes in shape and arrangement of the very same cells, resulting in correct lumen dimensions.

Shaping of biological tubes by mechanical interaction of cell and extracellular matrix

“…It seems that aECM itself plays roles in systemic control and providing global cues for tube growth [42]. Tracheal cell secretion activities driving apical membrane expansion is regulated by a cell autonomous manner [16], suggesting that a mechanism must exist by which these cells sense the mechanical or geometrical state of the lumen and equalize membrane tension in each branch type such that a uniform tube diameter is maintained for the entire length of the tube.…”

A new paradigm for animal symmetry

“…Importantly, examples can be found in which if one way of lumen formation is blocked, then another mechanism begins to operate, showing the robust drive of epithelia to form lumina [96] (see also [72,73]). The detailed presentation of tubulogenetic mechanisms-additionally including the machinery of cell-cell and cell-extracellular matrix (ECM) interactions, the polarization of cells, cyst formation, luminogenesis, elongation, branching, as well as the role of tip cells or epithelial-mesenchymal and mesenchymal-epithelial transitions-falls beyond the scope of this paper; instead, I refer the reader to some excellent papers and the references therein [71][72][73][74]76,78,79,82,[88][89][90][91][92][93][94]97].…”

Tube fusion: Making connections in branched tubular networks

“…Blood pressure was reported to be essential for pushing the apical membranes of anastomosing tip cells towards the fusion point [9]. In Drosophila, the apical extracellular matrix of expanding tracheal tubes contains secreted proteins and a scaffold of chitin fibres, which are crucial for shaping the luminal membrane (reviewed in [80]). Luminal hydrostatic pressure and mechanical forces imposed by the chitin scaffold on the FC apical surface could also contribute to pushing the FC membrane inwards.…”