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Life-cycle and functional cytology of the hepatopancreatic cells of Astacus astacus (Crustacea, Decapoda)

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Summary

The hepatopancreas of the freshwater crayfish Astacus astacus was reinvestigated by means of light and electron microscopy using refined techniques of tissue preservation. The results contribute significantly to the solution of controversial problems of the decapod hepatopancreas such as cell genealogy, cellular interdependences, elimination of senescent cells and functional interpretation of the cell types. The three mature cell types of the organ, R-, F- and B-cells, are shown to originate independently from embryonic E-cells which are located at the blind-ending tips of the hepatopancreatic tubules. The less abundant M-cells are supposedly of non-hepatopancreatic origin since they are also found in other epithelia of the digestive tract. Differentiating cells can be assigned at an early stage to one of the three hepatopancreatic cell lines if the ultrastructural appearance and distribution pattern of their organelles are used as distinguishing features. The most sensitive markers are the Golgi bodies which have a cell-specific architecture and secretion product not only in mature cells but also in early differentiating stages. Later conversion of one cell type into another, as has often been proposed in literature, does not occur. Senescent cells are preferably expelled from the epithelium at the junction of neighbouring hepatopancreatic tubules and at the antechamber which links the hepatopancreas to the main digestive tract. Cellular discharge in the antechamber occurs by sliding of the oldest parts of the hepatopancreatic epithelium across a particular antechamber epithelium that was thus far unknown. New ultrastructural findings are described with respect to the absorptive apparatus of nutrient absorbing R-cells, the formation of Golgi vesicles and retrieval of membranes in digestive enzyme synthesizing F-cells, and the involvement of Golgi body and endoplasmic reticulum in the formation of heterophagic vacuoles in B-cells. The discovery of these ultrastructural features enables a more sophisticated functional interpretation of the hepatopancreatic cells of Decapoda.

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References

  • Ahearn GA (1987) Nutrient transport by the crustacean gastrointestinal tract: recent advances with vesicle technique. Biol Rev 62:45–63

    Google Scholar 

  • Al-Mohanna SY, Nott JA (1986) B-cells and digestion in the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda). J Mar Biol Assoc UK 66:403–414

    Google Scholar 

  • Al-Mohanna SY, Nott JA (1987) R-cells and the digestive cycle in Penaeus semisulcatus (Crustacea: Decapoda). Mar Biol 95:129–137

    Google Scholar 

  • Al-Mohanna SY, Nott JA (1989) Functional cytology of the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda) during the moult cycle. Mar Biol 101:535–544

    Google Scholar 

  • Al-Mohanna SY, Nott JA, Lane DJW (1985a) Mitotic E- and secretory F-cells in the hepatopancreas of the shrimp Penaeus semisulcatus (Crustacea: Decapoda). J Mar Biol Assoc UK 65:901–910

    Google Scholar 

  • Al-Mohanna SY, Nott JA, Lane DJW (1985b) M ‘midget’ cells in the hepatopancreas of the shrimp, Penaeus semisulcatus De Haan, 1844 (Decapoda, Natantia). Crustaceana 48:260–268

    Google Scholar 

  • Andersen JT, Baatrup E (1988) Ultrastructural localization of mercury accumulations in the gills, hepatopancreas, midgut, and antennal glands of the brown shrimp, Crangon crangon. Aquatic Toxicol 13:309–324

    Google Scholar 

  • Böck P (1989) Romeis, Mikroskopische Technik. 17. Auflage. Urban und Schwarzenberg, München

    Google Scholar 

  • Dall W, Moriarty DJW (1983) Functional aspects of nutrition and digestion. In: Mantel LH (ed) The biology of crustacea, vol 5: Internal anatomy and physiological regulation. Academic Press, New York, pp 215–261

    Google Scholar 

  • Elofsson R, Hessler RR, Hessler AY (1992) Digestive system of the cephalocarid Hutchinsoniella macracantha. J Crustac Biol 12:571–591

    Google Scholar 

  • Geuze JJ, Kramer MF (1974) Function of coated membranes and multivesicular bodies during membrane regulation in stimulated exocrine pancreas cells. Cell Tissue Res 156:1–20

    Google Scholar 

  • Gibson R, Barker PL (1979) The decapod hepatopancreas. Oceanogr Mar Biol Ann Rev 17:285–346

    Google Scholar 

  • Glass HJ, MacDonald NL, Moran RM, Stark JR (1989) Digestion of protein in different marine species. Comp Biochem Physiol 94B:607–611

    Google Scholar 

  • Hallberg E, Hirche H-J (1980) Differentiation of mid-gut in adults and over-wintering copepodids of Calanus finmarchicus (Gunnerus) and C. helgolandicus Claus. J Exp Mar Biol Ecol 48:283–295

    Google Scholar 

  • Hopkin SP, Nott JA (1980) Studies on the digestive cycle of the shore crab Carcinus maenas (L) with special reference to the B cells in the hepatopancreas. J Mar Biol Assoc UK 60:891–907

    Google Scholar 

  • Icely JD, Nott JA (1992) Digestion and absorption: digestive system and associated organs. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates, vol 10: Decapod crustacea. Wiley-Liss, New York, pp 147–201

    Google Scholar 

  • Iida H, Shibata Y, Yamamoto T (1986) The endosome-lysosome system in the absorptive cells of goldfish hindgut. Cell Tissue Res 243:449–452

    Google Scholar 

  • Jamieson JD, Palade GE (1971) Synthesis, intracellular transport, and discharge of secretory proteins in stimulated pancreatic exocrine cells. J Cell Biol 50:135–158

    Google Scholar 

  • Johnson PT (1980) Histology of the blue crab, Callinectes sapidus. Praeger, New York

    Google Scholar 

  • Lawrence BP, Brown WJ (1992) Autophagic vacuoles rapidly fuse with pre-existing lysosomes in altered hepatocytes. J Cell Sci 102:515–526

    Google Scholar 

  • Loizzi RF (1971) Inerpretation of crayfish hepatopancreatic function based on fine structural analysis of epithelial cell lines and muscle network. Z Zellforsch 113:420–440

    Google Scholar 

  • Loret SM, Devos PE (1992) Structure and possible functions of the calcospherite-rich cells (R* cells) in the digestive gland of the shore crab, Carcinus maenas. Cell Tissue Res 267:105–111

    Google Scholar 

  • Lyon R, Simkiss K (1984) The ultrastructure and metal-containing inclusions of mature cell types in the hepatopancreas of a crayfish. Tissue Cell 16:805–817

    Google Scholar 

  • Malcoste R, van Wormhoudt A, Bellon-Humbert C (1983) La caractérisation de l'hépatopancréas de la Crevette Palaemon serratus Pennant (Crustacé Décapode Natantia) en cultures organotypiques. C R Acad Sci Paris Série III 296:597–602

    Google Scholar 

  • Novikoff AB, Quintana N, Mori M (1978) Studies on the secretory process in exocrine pancreas cells. II. C57 black and beige mice. J Histochem Cytochem 26:83–93

    Google Scholar 

  • Ogura K (1959) Midgut gland cells accumulating iron or copper in the crayfish, Procambarus clarkii. Annot Zool Jap 32:133–142

    Google Scholar 

  • Powell RR (1974) The functional morphology of the fore-guts of the thalassinid crustaceans, Callianassa californiensis and Upogebia pugettensis. Univ Calif Berkley Publ Zool 102:1–41

    Google Scholar 

  • Sagristà E, Durfort M (1991) Membranous tubular system in R-cells of decapod hepatopancreas investigated using electronopaque tracers. Cell Tissue Res 266:585–590

    Google Scholar 

  • Sedlmeier D (1987) The role of hepatopancreatic glycogen in the action of the crustacean hyperglycemic hormone (CHH). Comp Biochem Physiol 87A:423–425

    Google Scholar 

  • Speck U, Urich K (1970) Das Schicksal der Nährstoffe bei dem Flußkrebs Orconectes limosus. II. Resorption U-14C-markierter Nährstoffe und ihre Verteilung auf die Organe. Z Vergl Physiol 68:318–333

    Google Scholar 

  • Stöcker W, Wolz R, Zwilling R, Strydom DJ, Auld DS (1988) Astacus protease — a zinc metalloenzyme. Biochemistry 27:5026–5032

    Google Scholar 

  • Stöcker W, Gomis-Rüth F-X, Bode W, Zwilling R (1993) Implications of the three-dimensional structure of astacin for the structure and function of the astacin family of zinc-endopeptidases. Eur J Biochem 214:215–231

    Google Scholar 

  • Storch V, Anger K (1983) Influence of starvation and feeding on the hepatopancreas of larval Hyas araneus (Decapoda, Majidae). Helgol Wiss Meeresunters 36:67–75

    Google Scholar 

  • Storch V, Burkhard P (1984) Influence of nutritional stress on the hepatopancreas of Talitrus saltator (Peracarida, Amphipoda). Helgol Wiss Meeresunters 38:65–73

    Google Scholar 

  • Tartakoff A, Greene LJ, Palade GE (1974) Studies on the guinea pig pancreas. Fractionation and partial characterization of exocrine proteins. J Biol Chem 249:7420–7431

    Google Scholar 

  • Tsekos I, Schnepf E (1991) Acid phosphatase activity during spore differentiation of the red algae Gigartina teedii and Chondria tenuissima. Plant Syst Evol 176:35–51

    Google Scholar 

  • Van Deurs B, Holm PK, Kayser L, Sandvig K, Hansen SH (1993) Multivesicular bodies in HEp 2-cells are maturing endosomes. Eur J Cell Biol 61:208–224

    Google Scholar 

  • Vogt G (1985) Histologie und Cytologie der Mitteldarmdrüse von Penaeus monodon (Decapoda). Zool Anz 215:61–80

    Google Scholar 

  • Vogt G (1987) Monitoring of environmental pollutants such as pesticides in prawn aquaculture by histological diagnosis. Aquaculture 67:157–164

    Google Scholar 

  • Vogt G (1988) Histologische und immunhistochemische Untersuchungen zur Funktion der Decapodenmitteldarmdrüse. Dissertation, Universität Heidelberg

  • Vogt G (1992) Enclosure of bacteria by the rough endoplasmic reticulum of shrimp hepatopancreas cells. Protoplasma 171:89–96

    Google Scholar 

  • Vogt G (1993) Differentiation of B-cells in the hepatopancreas of the prawn Penaeus monodon. Acta Zool 74:51–60

    Google Scholar 

  • Vogt G, Quinitio ET (1994) Accumulation and excretion of metal granules in Penaeus monodon exposed to water-borne copper, lead, iron and calcium. Aquat Toxicol: in press

  • Vogt G, Storch V, Quinitio ET, Pascual FP (1985) Midgut gland as monitor organ for the nutritional value of diets in Penaeus monodon (Decapoda). Aquaculture 48:1–12

    Google Scholar 

  • Vogt G, Quinitio ET, Pascual FP (1986) Leucaena leucocephala leaves in formulated feed for Penaeus monodon: a concrete example of the application of histology in nutrition research. Aquaculture 59:209–234

    Google Scholar 

  • Vogt G, Stöcker W, Zwilling R, Storch V (1988) Synergetische Entwicklung von Verdauungstrakt und Verdauungsenzymen: ein Vergleich zweier konträrer Modelle (Säugetiere und dekapode Krebse). Verh Dtsch Zool Ges 81:193–194

    Google Scholar 

  • Vogt G, Quinitio ET, Pascual FP (1989a) Interaction of the midgut gland and the ovary in vitellogenesis and consequences for the breeding success: a comparison of unablated and ablated spawners of Penaeus monodon. In: de Pauw N, Jaspers E, Ackefors H, Wilkins N (eds) Aquaculture — a biotechnology in progress. European Aquaculture Society, Bredene, Belgium, pp 581–592

    Google Scholar 

  • Vogt G, Stöcker W, Storch V, Zwilling R (1989b) Biosynthesis of Astacus protease, a digestive enzyme from crayfish. Histochemistry 91:373–381

    Google Scholar 

  • Walker G (1970) The cytology, histochemistry, and ultrastructure of the cell types found in the digestive gland of the slug, Agriolimax reticulatus (Müller). Protoplasma 71:91–109

    Google Scholar 

  • Wilson JM, Whitney JA, Neutra MR (1991) Biogenesis of the apical endosome-lysosome complex during differentiation of absorptive epithelial cells in rat ileum. J Cell Sci 100:133–143

    Google Scholar 

  • Zwilling R, Neurath H (1981) Invertebrate proteases. Methods Enzymol 80:633–664

    Google Scholar 

Download references

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Vogt, G. Life-cycle and functional cytology of the hepatopancreatic cells of Astacus astacus (Crustacea, Decapoda). Zoomorphology 114, 83–101 (1994). https://doi.org/10.1007/BF00396642

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