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Fine Structure and Differentiation of the Midgut

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Fine Structure and Differentiation of the Midgut Zoological Studies 47(2): 200-206 (2008) Fine Structure and Differentiation of the Midgut Epithelium of Allacma fusca (Insecta: Collembola: Symphypleona) Magdalena Maria Rost-Roszkowska* and Agnieszka Undrul Silesian University, Department of Animal Histology and Embryology, Bankowa 9, 40-007 Katowice, Poland (Accepted September 3, 2007) Magdalena Maria Rost-Roszkowska and Agnieszka Undrul (2008) Fine structure and differentiation of the midgut epithelium of Allacma fusca (Insecta: Collembola: Symphypleona). Zoological Studies 47(2): 200-206. Allacma fusca belongs to a less well known, primitive, wingless insect group. The aim of our study was to describe all changes which accompany midgut epithelium differentiation of adult specimens of A. fusca. The midgut epithelium of A. fusca is composed of columnar cells with an epithelial character. No regenerative cells, which are commonly responsible for midgut epithelium regeneration, were observed. Therefore the growth of the entire epithelium depends on an increase in the dimensions of epithelial cells. Epithelial cells are not able to proliferate, as was earlier suggested, in the 1st larval stage of this species. The characteristic regionalization in the organelle arrangement was observed like in all epithelia responsible for secretion, transport, and excretion. , However during the insect s lifespan, distinct differences appear between all epithelial cells. Allacma fusca does not have Malpighian tubules; thus the midgut epithelium is also responsible for excretion. This process is connected with urospherites which accumulate in epithelial cells. Their structure suggests that they might be identified with type A granules described for many Pterygota insects. http://zoolstud.sinica.edu.tw/Journals/47.2/200.pdf Key words: Midgut epithelium, Differentiation, Stem cells, Urospherites T he midgut epithelium of insects is Depending on the kind of food, it will differentiate responsible for enzyme production, digestion, during larval stages or in adult specimens. In the secretion, and in insects devoid of Malpighian majority of insect species, the midgut epithelium tubules, excretion (Paclt 1956, Anderson is composed of columnar cells with an epithelial and Harvey 1966, Humbert 1979, Chapman character and regenerative cells. Endocrine and 1998). These functions are possibly due to the goblet cells have been described in some insect characteristic ultrastructure of epithelial cells which groups. Regenerative cells form groups called form the midgut epithelium. In the majority of regenerative nests or crypts. They may also be insects, their cytoplasm has distinct regionalization located singly among epithelial cells (Billingsley in organelle arrangements, and as a consequence, 1990, Sadrud-Din et al. 1996, Diaz et al. 2000 basal, perinuclear, and apical regions appear (Klag 2003, Garcia et al. 2001, Silva-Olivares et al. 2003, et al. 2002, Rost 2006a b, Rost-Roszkowska et al. Rost et al. 2005, Rost-Roszkowska et al. 2007a). 2007a). The midgut epithelium is formed during They are regarded as stem cells. However, in embryogenesis or less commonly, during larval some cases, the lack of regenerative cells among stages (Dallai 1966, Krzysztofowicz et al. 1973, epithelial cells has been described (Krzysztofowicz Rost et al. 2005, Rost-Roszkowska et al. 2007a b). et al. 1973, Lauga-Reyrel 1980). In those cases, In the middle of larval development, together with the regeneration process seems to be problematic. the growth of insect bodies, the midgut epithelium There are only a few studies concerning the is formed by an increasing number of cells. ultrastructure, development, and differentiation * To whom correspondence and reprint requests should be addressed. Tel: 48-32-3591376. E-mail:[email protected] 200 Rost-Roszkowska and Undrul - Midgut Epithelium of A. fusca (Collembola) 201 of the midgut epithelium in primitive, wingless 1). Regenerative cells were not observed. The insects and they mainly refer to species belonging epithelium is separated from the midgut lumen to Zygentoma, Arthropleona (Collembola), or by a peritrophic membrane (Fig. 2). Distinct Protura (Dallai 1966 1975 1977, Krzysztofowicz regionalization in organelle distribution in the et al. 1973, Biliński and Klag 1979, Klag et al. cytoplasm of epithelial cells was observed. 1981, Rost 2006a). We know even less about During midgut epithelium differentiation, these processes in insects of the collembolans numerous transitions of the epithelial cytoplasm suborder Symphypleona (Rost-Roszkowska et al. are set, until the time at which the functions of 2007b). Additionally it is worth mentioning that absorption, secretion, digestion, and excretion are due to a recent study, collembolans are thought fully developed. However, at the beginning of its to be a separate animal order, which developed differentiation, in the basal cytoplasm where the independently of insects (Nardi et al. 2003). basal membrane forms numerous folds, many Our studies have revealed the process of mitochondria and cisterns of rough endoplasmic midgut epithelium differentiation in adult specimens reticulum (RER) were observed (Fig. 3). The latter of Allacma fusca, a species which belongs to the forms both closed, circular structures and the Symphypleona (Collembola). Because of this typical lamellar arrangement (Fig. 4). Nuclei with process, the midgut epithelium in adult specimens heterochromatin clusters situated near the nuclear might be responsible for digestion and secretion, envelope have many nucleoli (Fig. 5). In the as well as excretion, because A. fusca does not perinuclear region, numerous cisterns of smooth. posses Malpighian tubules. Additionally, this endoplasmic reticulum (SER), Golgi complexes, species seems to be very interesting considering single mitochondria, and cisterns of RER were the lack of regenerative cells in its midgut observed (Fig. 6). In the apical cytoplasm, epithelium. abundant mitochondria, minor and major vesicles with electron-lucent content, and circular structures formed from cisterns of RER were present. During MATERIALS AND METHODS differentiation of the epithelium, mitochondria mainly accumulated in the apical cytoplasm (Fig. Animals for investigation were obtained 8). Electron-dense granules, which also appeared from the laboratory culture of A. fusca (Insecta: in this region, moved toward the apical membrane, Collembola: Symphypleona). Adults specimens where they removed their contents into the midgut were collected in Bieszczady mountains (Poland) lumen (Figs. 7, 8). Apical membranes formed from June to Aug. Adult specimens were fixed in microvilli with abundant cytoskeletal elements, 2.5% glutaraldehyde in 0.1 M phosphate buffer at which also protruded into the apical cytoplasm pH 7.4 (for 24 h at 4°C) and postfixed in 2% OsO4 forming characteristic roots (Figs. 7, 8). The entire (for 1.5 h at room temperature). After dehydration cytoplasm was rich in free ribosomes. Between in a graded series of alcohol (30%, 50%, 70%, the apical regions of adjacent epithelial cells, 90%, 95%, and 100% for 15 min each) and intercellular junctions of zonula continua (smooth acetone (15 min) the material was embedded in septate junctions) and macula adherens were Epon 812. Semi- and ultrathin sections were cut present (Fig. 9). Between the perinuclear and on a Leica Ultracut UCT25 ultramicrotome (Leica, basal regions, pleated septate and gap junctions Wetzlar, Germany). Semi-thin sections were could be observed (Fig. 10). stained with 1% methylene blue in 0.5% borax and At the beginning of midgut epithelium analyzed with an Olympus BX60 light microscope differentiation, urospherites appeared only in (Olympus, Tokyo, Japan). Ultrathin sections were the perinuclear cytoplasm (Figs. 3, 6, 7). Their stained with uranyl acetate and lead citrate. They number and volume greatly increased, so that they were examined with a Hitachi H500 transmission also began to occupy the basal (Figs. 11, 12) and electron microscope (Hitachi, Tokyo, Japan). apical cytoplasm of epithelial cells. Accumulation of RER cisterns could be observed during their formation (Fig. 13). When urospherites appeared RESULTS near the nuclear envelope, initially small and gradually larger lipid droplets occurred in the basal The midgut epithelium of adult specimens cytoplasm (Fig. 14). In the perinuclear region, of A. fusca is composed of columnar epithelial lamellar bodies arose, and nuclei often took on cells, which lie on a non-cellular basal lamina (Fig. lobular shapes. The numbers of RER cisterns in 202 Zoological Studies 47(2): 200-206 (2008) 1 3 l RER e m u 2 l 5 n mv e 4 u RER 6 RER g RER m m SER u 7 mv zc m RER u Figs. 1-7. 1. Midgut epithelium (e), composed of columnar cells resting on the non-cellular basal lamina (arrowhead). l, midgut lumen. Light microscopy, scale bar = 26 μm. 2. Peritrophic membrane (arrow) separating the midgut epithelium (e) from its lumen (l). mv, microvilli. Transmission electron microscopy, scale bar = 2.6 μm. 3. Basal membrane of epithelial cells forming numerous folds (arrow) between which mitochondria (m) and cisterns of RER (RER) can be observed. The beginning of urospherite (u) formation is evident. Transmission electron microscopy, scale bar = 2.5 μm. 4. Cisterns of rough endoplasmic reticulum (RER) forming numerous circular structures and the typical lamellar arrangement. m, mitochondria; u, urospherites. Transmission electron microscopy, scale bar = 2.63 μm. 5. Nuclei (n) possessing many clusters of heterochromatin situated near
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