Abstract
InMytilus edulis L., gametogenesis takes place in the mantle at the expense of the connective storage tissue. There are two main types of storage cells: vesicular (VC) cells storing large amounts of glycogen and adipogranular (ADG) cells containing large numbers of protein granules, lipid droplets and lesser amounts of glycogen. One of the ways in which stored reserves can be mobilized for gamete formation is by controlled autophagy, in which the cellular constituents are degraded by lysosomes. Mussels were collected from the Menai Strait, North Wales, and monthly measurements made, over two years (1984–1986), of the activities of lysosomal acid hydrolases (acid phosphatase,β-N-acetyl-D-glucosaminidase andβ-glucuronidase) and Cathepsins B and L in the mantle tissue, isolated ADG cells, low-density cells and, during spawning, in the mature oocytes of female mussels. The lysosomal proteinases, Cathepsins B, L and H, were further characterised by activation with thiol compounds and inhibition with thiol blockers and by leupeptin. Because of the low activity in the mantle tissue ofM. edulis, Cathepsin H was not assayed on a seasonal basis. There was a general increase in lysosomal enzyme activity during the winter, which can be related to increased autolysis in the storage cells and to the process of maturation in the developing oocytes. The activity of Cathepsin B was highest in the ADG and low-density cells, implying an important role in proteolysis within the ADG cells. By contrast, Cathepsin L displayed the highest activity in the mature oocytes, suggesting a major function of Cathepsin L in the development and maturation of the oocytes. Two differentα-glucosidase activities were measured in the monthly assays, one with a pH optimum of 4.5 (acid) and the other at pH 7.5 (neutral). Highest activities of the acidα-glycosidase were found in the low-density cells, but there were no significant seasonal changes in the mantle tissue as a whole. Activities of the neutralα-glucosidase were low in the ADG cells and mature oocytes, but showed high activities in the mantle tissue, with marked seasonal changes that corresponded to the mobilization of glycogen reserves in the VC cells.
Similar content being viewed by others
Literature cited
Alemany, M., Rosell-Pérez, M. (1973). Two different amylase activities in the sea mussel,Mytilus edulis L. Revta esp. Fisiol. 29: 217–222
Barrett, A. J., Heath, M. F. (1977). In: Dingle, J. T. (ed). Lysosomes: a laboratory handbook. 2nd ed. Elsevier North-Holland Biomedical, Amsterdam, p. 19–145
Barrett, A. J., Kirschke, H. (1981). Cathepsin B, Cathepsin H and Cathepsin L. In: Methods in enzymology: proteases of diverse origin and function. Vol. 80. Academic Press, New York, p. 535–561
Bayne, B. L., Bubel, A., Gabbott, P. A., Livingstone, D. R., Lowe, D. M., Moore, M. N. (1982). Glycogen utilization and gametogenesis inMytilus edulis L. Mar. Biol. Lett. 3: 89–105
Bayne, B. L., Gabbott, P. A., Widdows, J. (1975). Some effects of stress in the adult on the eggs and larvae ofMytilus edulis. J. mar. biol. Ass. U. K. 55: 675–689
Bayne, B. L., Holland, D. L., Moore, M. N., Lowe, D. M., Widdows, J. (1978). Further studies on the effects of stress in the adult on the eggs ofMytilus edulis. J. mar. biol. Ass. U. K. 58: 825–841
Bayne, B. L., Thompson, R. J. (1970). Some physiological consequences of keepingMytilus edulis in the laboratory. Helgoländer wiss. Meeresunters. 20: 525–552
Bayne, B. L. (1976). Aspects of reproduction in bivalve molluscs. In: Wiley, M. (ed.) Estuarine processes. Vol. 1. Academic Press, New York, p. 432–448
Bolognari, A., Albanese Carmignani, M. P., Zaccone, G., Minniti, F. (1979). Letter to the editor: cytochemical detection of some enzymes of the carbohydrate metabolism in the yolk of molluscan oocytes. Cell. molec. Biol. 24: 265–266
Chipperfield, P. N. J. (1953). Observations on the breeding and settlement ofMytilus edulis in British waters. J. mar. biol. Ass. U. K. 32: 449–476
Gabbott, P. A. (1983). Developmental and seasonal metabolic activities in marine molluscs. In: Hochachka, P. W. (ed.) The Mollusca. Vol. 2. Environmental biochemistry and physiology. Academic Press, New York, p. 165–217
Gabbott, P. A., Bayne, B. L. (1973). Biochemical effects of temperature and nutritive stress onMytilus edulis. J. mar. biol. Ass. U. K. 53: 269–286
Gabbott, P. A., Whittle, M. A. (1986). Glycogen synthetase in the sea mussel,Mytilus edulis. II. Seasonal changes in glycogen content and glycogen synthetase activity in the mantle tissue. Comp. Biochem. Physiol. 83B: 197–207
Glaumann, H., Ericsson, J. L. E., Marzella, L. (1981). Mechanism of intralysosomal degradation with special reference to autophagocytosis and heterophagocytosis of cell organelles. Int. Rev. Cytol. 73: 149–182
Greeley, M. S., Calder, D. R., Wallace, R. A. (1986). Changes in teleost yolk proteins during oocyte maturation: correlation of yolk proteolysis with oocyte hydration. Comp. Biochem. Physiol. 84B: 1–9
Houtteville, P. (1974). Contribution a l'etude cytologique et experimentale du cycle annuel du tissu de reserve du manteau deMytilus edulis. Thèse Doctorat IIIieme Biologie, Université de Caen, France
Knook, D. L., Sleyster, E. C. (1980). Isolated parenchymal, kupffer and endothelial rat liver cells characterized by their lysosomal enzyme content. Biochem. biophys. Res. Commun. 96: 250–257
Koehn, R. K., Bayne, B. L., Moore, M. N., Siebenaller, J. F. (1980). Salinity related physiological and genetic differences between populations ofMytilus edulis. Biol. J. Linn. Soc. 14: 319–334
Lowe, D. M., Moore, M. N., Bayne, B. L. (1982). Aspects of gametogenesis in the marine musselMytilus edulis. J. mar. biol. Ass. U. K. 62: 133–145
Lubet, P. (1959). Recherches sur le cycle et l'émission des gametes chez les Mytilidea et les Pectinides. Revue Trav. Inst. (scient. tech.) Pêch. marit. 23: 389–548
Lubet, P., Herlin, P., Mathieu, M., Collin, F. (1976). Tissu de réserve et cycle sexuel chez les lamellibranchs. Haliotis, Paris 7: 59–62
Moore, M. N. (1976). Cytochemical demonstration of latency of lysosomal hydrolases in digestive cells of the common mussel,Mytilus edulis, and changes induced by thermal stress. Cell. Tissue Res. 175: 279–287
Okada, S., Aikawa, T. (1986). Cathepsin D-like acid proteinase in the mantle of the marine mussel,Mytilus edulis. Comp. Biochem. Physiol. 84B: 333–341
Pasteels, J. J. (1973). Yolk and lysosomes. In: Dingle, J. T. (ed.) Lysosomes in biology and pathology. Vol. 3. Elsevier North-Holland Biomedical, Amsterdam, p. 216–234
Peek, K. (1987). Some biochemical characteristics of isolated adipogranular cells from the musselMytilus edulis L. PhD thesis, University of Wales, Bangor
Peek, K., Gabbott, P. A. (1989). Adipogranular cells from the mantle tissue ofMytilus edulis L. I. Isolation, purification and biochemical characteristics of dispersed cells. J. exp. mar. Biol. Ecol. 126: 203–216
Peek, K., Gabbott, P. A., Runham, N. W. (1989). Adipogranular cells from the mantle tissue ofMytilus edulis L. II. Seasonal changes in the distribution of dispersed cells in a preformed Percoll density gradient. J. exp. mar. Biol. Ecol. 126: 217–230
Pipe, R. K. (1987a). Oogenesis in the marine musselMytilus edulis: an ultrastructural study. Mar. Biol. 95: 405–414
Pipe, R. K. (1987b). Ultrastructural and cytochemical study on interactions between nutrient storage cells and gametogenesis in the musselMytilus edulis. Mar. Biol. 96: 519–528
Pipe, R. K., Moore, M. N. (1985). The ultrastructural localization of lysosomal acid hyrolases in developing oocytes of the common marine musselMytilus edulis. Histochem. J. 127: 939–949
Seymour, C. A., Peters, T. J. (1977). Enzyme activities in human liver biopsies — assay methods and activities of some lysosomal and membrane bound enzymes in control tissues and serum. Clin. Sci. molec. Med. 52: 229–239
Snedecor, G. W., Cochran, W. G. (1980). Statistical methods. 7th ed. Iowa State University Press, Ames, Iowa
Wallace, R. A. (1985). Vitellogenesis and oocyte growth in nonmammalian vertebrates. In: Browder, L. W. (ed.) Developmental biology: a comprehensive synthesis. Vol. 1. Oogenesis. Plenum Press, New York, p. 127–177
Wourms, J. P. (1987). Oogenesis. In: Giese, A. C., Pearse, J. S., Pearse, V. B. (eds.) Reproduction of marine invertebrates. IX. General aspects: seeking unity in diversity. Blackwell Scientific Publications and The Boxwood Press, California, p. 49–178
Zaba, B. N. (1981). Glycogenolytic pathways in the mantle tissue ofMytilus edulis. Mar. Biol. Lett. 2: 67–74
Author information
Authors and Affiliations
Additional information
Communicated by J. Mauchline, Oban
Rights and permissions
About this article
Cite this article
Peek, K., Gabbott, P.A. Seasonal cycle of lysosomal enzyme activities in the mantle tissue and isolated cells from the musselMytilus edulis . Mar. Biol. 104, 403–412 (1990). https://doi.org/10.1007/BF01314343
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01314343