Electrophysiology of K+ transport by midgut epithelium of lepidopteran insect larvae. IV. A multicompartment model accounts for tetramethylammonium entry into goblet cavities

A quantitative model was developed to explain the kinetics of tetramethylammonium (TMA+) movement into and out of the goblet cavities of posterior midgut cells of Manduca sexta based on the data of the accompanying paper, which indicated that TMA+ does not enter the goblet cavity directly from the lumen. The model has two cellular compartments between the lumen and goblet cavity; these have been tentatively identified as the columnar cell and goblet cell cytoplasm. Five transmembrane pathways are included: from lumen to columnar cell, from columnar cell to goblet cell, from goblet cell cytoplasm to goblet cell cavity, and across the basal membrane of each cell type. These pathways need not be channels; they could use endocytotic or exocytotic mechanisms or, in the case of the cell-to-cell passage, septate junctions. However, in all cases, transfer is proportional to the electrochemical gradient. The model was tested against the results obtained after exposure to TMA+ in short-circuited and open-circuited tissues as well as results from an open-circuited tissue that did not develop a large transepithelial potential. Although driving forces for TMA+ across the membrane barriers were quite different in the different experimental conditions, the transfer coefficients from lumen to columnar cell, from columnar to goblet cell and from both cells across the basal membrane were the same. The only transfer coefficient that changed between short-circuit and open-circuit conditions was that from goblet cell cytoplasm to goblet cavity. This value was high under short-circuit conditions (when K+ transport activity is high), but low under open-circuit conditions (when K+ transport activity is low). The model suggests a hypothesis in which TMA+ enters the goblet cavity by an indirect route across the cell membrane of columnar cells, and thence passes to the goblet cell cytoplasm through intercellular junctions. Results from experiments with cytochalasin E suggest that the actin-based cytoskeleton is involved in limiting cell­cell coupling. In this model, TMA+ passes from the goblet cell cytoplasm to the goblet cavity via the K+/nH+ antiport believed to mediate active transepithelial K+ transport. However, although actively transported K+ is believed to pass from goblet cavity to lumen, TMA+ cannot.