Goblet Cell Membrane Differentiations in the Midgut of a Lepidopteran Larva

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Goblet Cell Membrane Differentiations in the Midgut of a Lepidopteran Larva Jf. Cell Set. ao, 357-375 (1976) 357 Printed in Great Britain GOBLET CELL MEMBRANE DIFFERENTIATIONS IN THE MIDGUT OF A LEPIDOPTERAN LARVA N. E. FLOWER Physics and Engineering Laboratory, D.S.I.R., Private Bag, Lower Hutt, New Zealand AND B. K. FILSHIE Division of Entomology, C.S.I.R.O., P.O. Box 1700, Canberra, Australia SUMMARY So-called goblet cells are present in the midgut of lepidopteran larvae. They are thought to be involved in the active transport of potassium out of the haemolymph and into the gut lumen. A number of plasma membrane differentiations within the goblet cell cavity has been investi- gated using conventional staining, lanthanum tracer and freeze-etch techniques. Of particular interest are junction-like inter- and intra-membrane differentiations found on the villus-like cytoplasmic projections present at the apical tip of the goblet cell cavities. These cytoplasmic projections appear to act as a valve; in some cases they seem to close off the top of the goblet cell cavity, so isolating it from the gut lumen, while in other cases they are spread apart leaving a wide channel from the cavity into the lumen. The junction-like structures on these cytoplasmic projections are different in structure from the septate-type junctions which seal the midgut cells together at their apical borders, and the 2 types are present on the same plasma membrane, often within one micron of each other. The need for a different type of junction may possibly be related to the fact that it occurs between 2 areas of the same plasma membrane. The morph- ology of this unusual junction-like structure is discussed and 2 diagrams are presented to illustrate our interpretation of its structure. INTRODUCTION The midgut of plant-eating species of lepidopterous and tricopterous insects has been shown to be involved in the active transport of potassium out of the haemolymph and into the gut lumen, a function normally carried out in insects by the Malpighian tubules (Harvey & Nedergaard, 1964). The midgut of these insects contains a third cell type, the goblet cell, as well as the normal columnar and regenerative cells (Shinoda, 1927; Anderson & Harvey, 1966). Anderson & Harvey (1966) suggested that these goblet cells were responsible for the potassium transport. They also found that 3 different types of microvillus-like cytoplasmic projections were present in the goblet cell cavity. Towards the base of the cavity were large numbers of cytoplasmic projec- tions, most of which contained mitochondria. They thus appeared very similar to the mitochondria-containing microvillus-like projections present on the lumen surface of cells in insect Malpighian tubules. Towards the apical end of the goblet cell cavity the cytoplasmic projections were shown to become smaller, not to contain mito- chondria, and to be present in lesser numbers. At the tip of the cavity where it opens into the gut lumen, a number of projections, each further subdivided into many 358 N. E. Flower and B. K. Filshie villus-like units, were found. These seemed to act as a valve at the top of the cavity and in many sections appeared almost to close off the cavity from the gut lumen. In a previous paper one of the present authors had shown that in freeze-etch replicas of the light organ of Arachnocampa luminosa non-junctional complementary membrane fracture faces were observed, in the sense that the number of particles on the A faces were matched by the number of pits or holes on the B faces (Flower, 1973). This effect was only present in plasma membranes through which small molecules were being actively transported into the gland lumen. The present investigation was under- taken to see if such a membrane differentiation was also present in the goblet cell and to investigate the difference, if any, between the membranes of the different types of microvillus-like projections present in the goblet cell cavity. MATERIALS AND METHODS The guts of caterpillars of the two lepidopteran species Ephestia kuhniella Zeller, Pyralidae, and Spodoptera litura (Fabricius), Noctuidae, were dissected and the midgut portions isolated. For conventional electron microscopy, material was fixed with 2-5 % glutaraldehyde in 0-05 M cacodylate buffer at pH 7-2 for 2 h at room temperature, washed in several changes of cacodylate buffer for 2 h, postfixed in 1 % osmium tetroxide for 2 h at room temperature, dehydrated, and embedded in Araldite. Thin sections were stained with uranyl acetate and lead citrate before examination. Some material was block stained in uranyl acetate for 12 h at 50 °C, after which sections were usually post-stained with lead citrate. Lanthanum incorporation into the tissue was achieved by the addition of either 1 % lanthanum nitrate or a lanthanum hydroxide colloidal suspension (Revel & Karnovsky, 1967) to both the glutaraldehyde fixative and the buffer washings. Sections of tissues with lanthanum incorporated were examined without further staining. For freeze etching, midguts were placed for 1 h either in 20-30 % glycerol buffered to pH 7-4 with 007 M phosphate or in this solution to which 2-3 % glutaraldehyde had been added. Small annulae were then cut out from the midgut and placed upright on copper grids before being rapidly frozen in Freon 12 held at —150 °C. The freeze etching was carried out in a Balzers BA500 as described by Moor & Miihlethaler (1963). RESULTS The structure of goblet cells in the midgut epithelium of Lepidoptera has been described in detail for Hyalophora cecropia by Anderson & Harvey (1966) and in E. kuhniella by Smith et al. (1969). The main features are summarized in Fig. 1. The internal cavity of the cell occupies a considerable proportion of each cell volume, and large numbers of cytoplasmic processes project into the cavity. Most of these processes occur towards the base of the cavity and here they frequently contain long filamentous mitochondria within their cytoplasm. Towards the apex of the cavity these projections become sparse and do not contain mitochondria. At the apical tip, where the cavities open into the midgut lumen, are a number of somewhat different cytoplasmic projec- tions, each of which divides into a number of small villus-like units. These projections appear to act as a valve, being open and not readily visible in some cases, and tightly packed into a regularly organized array so as to close off the cavity in others (Figs. 1, 4). With the conventional fixing and staining procedures we normally used, i.e. glutar- aldehyde and osmium fixation followed by staining of sections with uranyl acetate and Lepidopteran membrane differentiations 359 lead citrate, a non-staining gap always existed between neighbouring projections (Fig. 4). This 'gap', which has a minimum width of about 11 nm, actually delineates a complex junctional structure which is most readily observed after lanthanum impregnation, as will be described later. Micrographs of goblet cells taken by B. L. Gupta and published in Berridge & Oschman (1972) show a dense, positively stained region between apposing apical projections, although details of the intermembrane structure cannot be discerned. Unfortunately the staining conditions were not recorded, and although we have been able to delineate the 'septa' by block staining with uranyl acetate followed by lead staining of sections (Fig. 5) we have been unable to obtain such dense staining. Columnar cell Fig. 1. Diagrammatic representation of a goblet cell in the midgut of a mature lepidop- teran larva. The goblet cell cavity occupies a large proportion of the cell volume. a si> g P junction; sj, septate-type junction; mvlt microvillus-like cytoplasmic projec- tions at the basal end of the cavity, many of which contain long thin mitochondria; mvt, microvillus-like cytoplasmic projections towards the apical end of the goblet cell which do not appear to contain mitochondria; mv3, columnar cell microvilli lining the midgut; cp, cytoplasmic projections at the apical tip of the cavity which appear to act as a valve between the cavity and the midgut lumen. When the membranes of the cytoplasmic projections near the base of the cavity are observed in freeze-etch replicas they show complementary fracture faces (Figs. 6, 7), in that the A faces are covered by a large number of particles and the B faces by an almost equivalent number of holes or depressions. As was evident from sectioning studies, these cytoplasmic projections, unlike microvilli, are not regular in shape, often bifurcating or bulging, the latter possibly occurring where mitochondria are enclosed. Measurement of a number of areas on both A and B faces has indicated that the particle density within the membrane is about 55 per ioo-nm square. The particles appear to be 10-12 nm in diameter. A somewhat different picture emerges when the fracture plane passes through the 360 N. E. Flower and B. K. Filshie cytoplasmic projections present at the apical tip of the cavity. These projections are more regularly arranged and appear to form a valve across the cavity which, as in sectioning studies, is sometimes seen closed (Fig. 8) and sometimes open (Fig. 9). Cytoplasmic filaments can be seen running along the length of some of the cytoplasmic projections (arrowed in Fig. 8). Examination of Figs. 8 and 9 shows that the mem- branes of some of the cytoplasmic projections are differentiated in that, depending on which face is examined, an array of grooves or an array of very closely packed rows of particles is present. The particles in these rows are so closely apposed that in many replicas they appear like continuous rods. The differentiations can be seen much more clearly in Fig. 10, where almost all the cytoplasmic projections are differentiated. The separation of the 'rods' or grooves is about 10 nm.
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