Skip to main content
Log in

Dynamics of activity of intracellular cysteine-dependent proteases and some peptidases in embryogenesis of Atlantic salmon Salmo salar L.

  • Embryogenesis and Carcinogenesis
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The dynamics of the activity of cysteine-dependent enzymes involved in intracellular proteolysis was studied in freshwater salmon Salmo salar L. during its early development: in the period from the blastodisc formation to hatching and in eggs before fertilization. The Ca2+-activated proteolytic activity of calpains, the activity of acidic lysosomal protease cathepsin B, and the activity of several peptidases that use the chromogenic component p-nitroaniline-containing peptides (L-Ala-pNA, L-Pro-pNA, L-Arg-pNA, N-Bzl-L-Arg-pNA, L-Phe-pNA, N-Glu-L-Phe-pNA, and Z-Gly-Pro-pNA) as substrates were analyzed. It is shown that the activity of the enzymes of interest increases at the stage of late blastula and early gastrula. The next increase in the activity of cathepsin B and calpain is observed at the stage of eye pigmentation, and the activity of peptidases and cathepsin B increases in eggs before hatching. The functional role of changes in intracellular proteolytic enzymes in the processes of protein metabolism associated with the Atlantic salmon embryo is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anzenbacherová, E., Barth, T., Barthová, J., et al., Measures for Success, European Aquaculture Society Special Publication, Oostende (Belgium), 1994, no. 21, pp. 137–138.

    Google Scholar 

  • Barrett, A.J. and Heath, M, Lysosomal enzymes, in Lysosomes. A Laboratory Handbook, Amsterdam, 1977, pp. 19–27.

    Google Scholar 

  • Barth, T., Barthova, J., Vacek, J., et al., Towards predictable quality, Belgium European Aquaculture Society Special Publication, Oostende (Belgium), 1999, no. 27, pp. 8–11.

    Google Scholar 

  • Ben-Aharon, I., Ben-Yosef, D., Amit, A., et al., Expression and immunolocalization of the calpain–calpastatin system in the human oocyte, Fertil. Steril., 2005a, vol. 83, no. 6, pp. 1807–1813.

    Article  CAS  PubMed  Google Scholar 

  • Ben-Aharon, I., Brown, P.R., Etkovitz, N., et al., The expression of calpain 1 and calpain 2 in spermatozoa of the mouse, Reproduction, 2005b, vol. 129, no. 4, pp. 435–442.

    Article  CAS  PubMed  Google Scholar 

  • Ben-Aharon, I., Haim, K., Shalgi, R., et al., Expression and possible involvement of calpain isoforms in mammalian egg activation, Reproduction, 2005c, vol. 130, no. 2, pp. 165–175.

    Article  CAS  PubMed  Google Scholar 

  • Bohley, P, Intracellular proteolysis, in Hydrolytic Enzymes, Elsevier, Biomedical Division, 1987, pp. 307–332.

    Chapter  Google Scholar 

  • Bondareva, L.A., Nemova, N.N., and Kyaivyaryainen, E.I., Vnutrikletochnaya Ca2+-zavisimaya proteoliticheskaya sistema zhivotnykh (Intracellular Ca2+-Dependent Proteolytic System of Animals), Moscow: Nauka, 2006.

    Google Scholar 

  • Bradford, M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Brashe, Zh., Biokhimicheskaya embriologiya (Biochemical Embryology), Moscow: Inostr. Liter., 1961.

    Google Scholar 

  • Cao, Y., Zhao, H., and Grunz, H., XCL-2 is a novel m-type calpain and disrupts morphogenetic movements during embryogenesis in Xenopus laevis, Dev. Growth Differ., 2001, vol. 43, pp. 563–571.

    Article  CAS  PubMed  Google Scholar 

  • Detlaf, T.A., Brodskii, V.Ya., and Gauze, G.G., Metody biologii razvitiya (Methods of Developmental Biology), Moscow: Nauka, 1974.

    Google Scholar 

  • Duan, W.R., Ito, M., Lee, E.J., et al., Estrogen regulates a tissue-specific calpain in the anterior pituitary, Biochem. Biophys. Res. Commun., 2002, vol. 295, pp. 261–266.

    Article  CAS  PubMed  Google Scholar 

  • Epel’, D, Initiating development during fertilization, Ontogenez, 1992, vol. 23, pp. 213–227.

    Google Scholar 

  • Epel, D., Nishioka, D., and Perry, G, The role of Ca2+ in triggering development at fertilization, Biol. Cell, 1978, vol. 32, pp. 135–140.

    CAS  Google Scholar 

  • Fan, T., Wang, J., Yuan, W., et al., Purification and characterization of hatching enzyme from brine shrimp Artemia salina, Acta Biochim. Biophys. Sin. (Shanhay), 2010, vol. 42, no. 2, pp. 165–171.

    Article  CAS  Google Scholar 

  • Gwatkin, R.B.L., Williams, D.T., Hartmann, J.F., et al., The zona reaction of hamster and mouse eggs production in vitro by a trypsin-like protease from cortical granules, J. Reprod. Fertil., 1973, vol. 32, pp. 259–265.

    Article  CAS  PubMed  Google Scholar 

  • Haim, K., Ben-Aharon, I., and Shalgi, R, Expression and immunolocalization of the calpain calpastatin system during parthenogenetic activation and fertilization in the rat egg, Reproduction, 2006, vol. 131, pp. 35–43.

    Article  CAS  PubMed  Google Scholar 

  • Kronovetr, J., Barthová, J., Barth, T., et al., Pol. Arch. Hydrobyol., 1998, vol. 45, pp. 331–335.

  • Li, Z.J. and Kim, S.M., A novel hatching enzyme from starfish asterias amurensis: purification, characterization, and cleavage specificity, Appl. Biochem. Biotechnol., 2013, vol. 169, no. 4, pp. 1386–1396.

    Article  CAS  PubMed  Google Scholar 

  • Lysenko, L.A., Nemova, N.N., and Kantserova, N.P., Proteoliticheskaya regulyatsiya biologicheskikh protsessov (Proteolytic Regulation of Biological Processes), Petrozavodsk: Kar NTs RAN, 2011.

    Google Scholar 

  • Matsuda, K. and Musaka, E, Studies on cathepsin d of rat liver lysosomes. I. Purification and multiple form, Biochemistry, 1974, vol. 76, pp. 639–649.

    Article  CAS  Google Scholar 

  • Matsuk, V.E, The study of some physiological and biochemical characteristics of the earliest periods of life of the rainbow trout, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow, 1976.

    Google Scholar 

  • McDonald, I. and Schwabe, C, Intracellular exopeptidases, in Proteinases in Mammalian Cells and Tissues, Amsterdam, 1977, pp. 311–391.

    Google Scholar 

  • Mellgren, R.L. and Murachi, T, Intracellular Calcium- Dependent Proteolysis, Boca Raton (FL): CRC, 1990.

    Google Scholar 

  • Mizote, A., Okamoto, S., and Iwao, Y, Activation of Xenopus eggs by proteases: possible involvement of a sperm protease in fertilization, Dev. Biol., 1999, vol. 208, pp. 79–92.

    Article  CAS  PubMed  Google Scholar 

  • Mommsen, T.P, Salmon spawning migration and muscle protein metabolism: the august krogh principle at work, Comp. Biol. Physiol. B. Biochem. Mol. Biol., 2004, vol. 139, no. 3, pp. 383–400.

    Article  Google Scholar 

  • Murachi, T., Hatanaka, M., Yasumoto, Y., et al., A quantitative distribution study on calpain and calpastatin in rat tissues and cells, Biochem. Int., 1981, vol. 2, no. 6, pp. 651–658.

    CAS  Google Scholar 

  • Nagasawa, T., Kawaguchi, M., Sano, K., et al., Sturgeon hatching enzyme and the mechanism of egg envelope digestion: insight into changes in the mechanism of egg envelope digestion during the evolution of ray-finned fish, J. Exp. Zool. B Mol. Dev. Evol., 2015, vol. 324, no. 8, pp. 720–732.

    Article  CAS  PubMed  Google Scholar 

  • Neifakh, A.A. and Timofeeva, M.Ya., Molekulyarnaya biologiya protsessov razvitiya (Molecular Biology of Development Processes), Moscow: Nauka, 1977.

    Google Scholar 

  • Nemova, N.N., Vnutrikletochnye proteoliticheskie fermenty u ryb (Intracellular Proteolytic Enzymes in Fish), Petrozavodsk: Kar. NTs RAN, 1996.

    Google Scholar 

  • Nemova, N.N., Lysenko, L.A., and Kantserova, N.P, Proteases of the calpain family: structure and functions, Russ. J. Dev. Biol., 2010, vol. 41, no. 5, pp. 318–325.

    Article  Google Scholar 

  • Otto, K, Cathepsin B1 and B2, in Tissue Proteinases, Amsterdam, 1971, pp. 1–28.

    Google Scholar 

  • Ozernyuk, N.D., Energeticheskii obmen v rannem ontogeneze ryb (Energy Metabolism in the Early Ontogeny of Fish), Moscow: Nauka, 1985.

    Google Scholar 

  • Post, L.L., Shuel, R., and Shuel, N, Evidence that hatching enzyme of the sea urchin Strongylocentrotus purpuratus is a chymotrypsin-like protease, Biochem. Cell Biol., 1988, vol. 66, no. 11, pp. 1200–1209.

    Article  CAS  PubMed  Google Scholar 

  • Purintrapiban, J., Wang, M.C., and Forsberg, N.E, Degradation of sarcomeric and cytoskeletal proteins in cultured skeletal muscle cells, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2003, vol. 136, pp. 393–401.

    Article  PubMed  Google Scholar 

  • Ral’nikova, E.S., Sulfhydryl groups and the reactivity of fish embryos, in Problemy sovremennoi embriologii (Problems of Modern Embryology), Moscow: Nauka, 1973, pp. 258–263.

    Google Scholar 

  • Ryzhkov, L.P., Morfofiziologicheskie zakonomernosti i transformatsii veshchestva i energii v rannem ontogeneze presnovodnykh lososevykh ryb (Morphological and Physiological Patterns and Transformation of Matter and Energy in the Early Ontogeny of Freshwater Salmon), Petrozavodsk: Kareliya, 1976.

    Google Scholar 

  • Salem, M., Kenney, B., Rexroad, C., et al., Molecular characterization of muscle atrophy and proteolysis associated with spawning in rainbow trout, Comp. Biochem. Physiol. Part D. Genomics Proteomics, 2006, vol. 1, pp. 227–237.

    Article  PubMed  Google Scholar 

  • Salem, M., Nath, J., Rexroad, C.E., et al., Identification and molecular characterization of the rainbow trout calpains (Capn1 and Capn2): their expression in muscle wasting during starvation, Comp. Biochem. Physiol. B, 2005, vol. 140, no. 1, pp. 63–71.

    Article  PubMed  Google Scholar 

  • Saris, N.-E. and Karafoli, E., A historical review of cellular calcium handling, with emphasis on mitochondria, Biochemistry (Moscow), 2005, vol. 70, no. 2, pp. 187–194.

    Article  CAS  Google Scholar 

  • Seiliez, I., Gabillard, J.C., Riflade, M., et al., Amino acids downregulate the expression of several autophagyrelated genes in rainbow trout myoblasts, Autophagy, 2012, vol. 8, pp. 364–375.

    Article  CAS  PubMed  Google Scholar 

  • Seiliez, I., Dias, K., and Cleveland, B.M, Contribution of the autophagy-lysosomal and ubiquitin-proteasomal proteolytic systems to total proteolysis in rainbow trout (oncorhynchus mykiss) myotubes, Am. J. Physiol. Regul. Inter. Comp. Physiol., 2014, vol. 307, pp. R1330–R1337.

    Article  CAS  Google Scholar 

  • Shi, Z.P., Fan, T.J., Cong, R.S., et al., Purification and characterization of hatching enzyme from flounder Paralichthys olivaceus, Fish Physiol. Biochem., 2006, vol. 32, no. 1, pp. 35–42.

    Article  CAS  PubMed  Google Scholar 

  • Webb, S.E., Fluck, R.A., and Miller, A.L, Calcium signaling during the early development of medaka and zebrafish, Biochimie, 2011, vol. 93, no. 12, pp. 2112–2125.

    Article  CAS  PubMed  Google Scholar 

  • Webb, S.E. and Miller, A.L., Ca2+ signaling during activation and fertilization in the eggs of teleost fish, Cell Calc., 2013, vol. 53, no. 1, p. 24.

    Article  CAS  Google Scholar 

  • Whitaker, M, Calcium signalling in early embryos, Philos. Trans R Soc. Lond B Biol. Sci., 2008, vol. 363, no. 1495, pp. 1401–1418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitaker, M, Calcium at fertilization and in early development, Physiol. Rev., 2006, vol. 86, no. 1, pp. 25–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zotin, A.I, The hatching enzyme in embryos of Acipenseridae, Dokl. Akad. Nauk SSSR, 1953, vol. 92, pp. 685–687.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. N. Nemova.

Additional information

Original Russian Text © N.N. Nemova, E.I. Kyaivyaryainen, M.Yu. Krupnova, 2017, published in Ontogenez, 2017, Vol. 48, No. 4, pp. 308–314.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nemova, N.N., Kyaivyaryainen, E.I. & Krupnova, M.Y. Dynamics of activity of intracellular cysteine-dependent proteases and some peptidases in embryogenesis of Atlantic salmon Salmo salar L.. Russ J Dev Biol 48, 263–268 (2017). https://doi.org/10.1134/S1062360417040075

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360417040075

Keywords

Navigation