Skip to main content
SpringerLink
Log in

Selective changes in the protein-turnover rates and nature of growth induced in trout liver by long-term starvation followed by re-feeding

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

We report upon the effects of a cycle of long-term starvation followed by re-feeding on the liver-protein turnover rates and nature of protein growth in the rainbow trout (Oncorhynchus mykiss). We determined the protein-turnover rate and its relationship with the nucleic-acid concentrations in the livers of juvenile trout starved for 70 days and then re-fed for 9 days. During starvation the total hepatic-protein and RNA contents decreased significantly and the absolute protein-synthesis rate (AS) also fell, whilst the fractional protein-synthesis rate (KS) remained unchanged and the fractional protein-degradation rate (KD) increased significantly. Total DNA content, an indicator of hyperplasia, and the protein:DNA ratio, an indicator of hypertrophy, both fell considerably. After re-feeding for 9 days the protein-accumulation rates (KG, AG) rose sharply, as did KS, AS, KD, protein-synthesis efficiency (KRNA) and the protein-synthesis rate/DNA unit (KDNA). The total hepatic protein and RNA contents increased but still remained below the control values. The protein:DNA and RNA:DNA ratios increased significantly compared to starved fish. These changes demonstrate the high response capacity of the protein-turnover rates in trout liver upon re-feeding after long-term starvation. Upon re-feeding hypertrophic growth increased considerably whilst hyperplasia remained at starvation levels.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. García-Salguero L, Lupiáñez JA: Metabolic adaptation of the renal carbohydrate metabolism. I. Effects of starvation on the gluconeogenic and glycolytic fluxes in the proximal and distal renal tubules. Mol Cell Biochem 83: 167–178, 1988

    Google Scholar 

  2. García-Salguero L, Lupiáñez JA: Long-term control on renal carbohydrate metabolism. II. Effect of starve-feed cycle on renal tubule glycolysis. Comp Biochem Physiol 92: 67–74, 1989

    Google Scholar 

  3. Moon TW, Foster GD, Plisetskaya EM: Changes in peptide hormones and liver enzymes in the rainbow trout deprived of food for 6 weeks. Can J Zool 67: 2189–2193, 1989

    Google Scholar 

  4. Gutiérrez J, Pérez J, Navarro I, Zanuy S, Carrillo M: Changes in plasma glucagon and insulin associated with fasting in sea bass (Dicentrarchus labrax). Fish Physiol Biochem 9: 108–112, 1991

    Google Scholar 

  5. Matty AJ, Lone KP: Hormonal control of protein deposition. In: CB Cowey, AM MacKie, JG Bell (eds). Nutrition and Feeding in Fish. Academic Press, London, 1985, pp 147–167

    Google Scholar 

  6. Cherrington AD, Vranic M: Hormonal utilization of nutrients and the effect of insulin in fish. Comp Biochem Physiol 88: 701–711, 1986

    Google Scholar 

  7. Walton MJ, Cowey CB: Aspect of intermediary metabolism in salmonid fish. Comp Biochem Physiol 73: 59–79, 1982

    Google Scholar 

  8. De la Higuera M, Cárdenas P: Influence of dietary composition on gluconeogenesis from L-(U-14C)-glutamate in rainbow trout Salmo gairdneri. Comp Biochem Physiol 81: 391–395, 1985

    Google Scholar 

  9. Walton MJ: Metabolic effects of feeding of a high protein/low carbohydrate diet as compared to a low-protein/high carbohydrate diet to rainbow trout Salmo gairdneri. Fish Physiol Biochem 1: 7–15, 1986

    Google Scholar 

  10. Renaud JM, Moon TW: Characterization of gluconeogenesis in hepatocytes isolated from the American eel, Anguilla rostrata. J Comp Physiol 135: 115–125, 1980

    Google Scholar 

  11. Himms-Hagen J: Cellular thermogenesis. Ann Rev Physiol 38: 315–351, 1976

    Google Scholar 

  12. Houlihan DF, Waring CP, Mathers E, Gray C: Protein synthesis and oxygen consumption of the shore crab Carcinus maenas after a meal. Physiol Zool 63: 735–756, 1990

    Google Scholar 

  13. Smith RW, Houlihan DF, Nilsson GE, Brechin JG: Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol 40: R897–R904, 1996

    Google Scholar 

  14. McMillan DN, Houlihan DF: The effect of re-feeding on tissue protein synthesis in rainbow trout. Physiol Zool 61: 429–441, 1988

    Google Scholar 

  15. McMillan DN, Houlihan DF: Protein synthesis in trout liver is stimulated by both feeding and fasting. Fish Physiol Biochem 10: 23–34, 1992

    Google Scholar 

  16. Lyndon AR, Houlihan DF, Hall SJ: The effect of short-term fasting and a single meal on protein synthesis and oxygen consumption in cod, Gadus morhua. J Comp Physiol B 162: 209–215, 1992

    Google Scholar 

  17. Waterlow JC, Garlick PJ, Millward DJ: Protein turnover in mammalian tissues and in the whole body. Elsevier Sciences Publishers, Amsterdam, New York, Oxford, 1978

    Google Scholar 

  18. Mathers EM, Houlihan DF; McCarthy ID, Burren LJ: Rates of growth and protein synthesis correlated with nucleic acid content in fry of rainbow trout, Oncorhynchus mykiss: Effects of age and temperature. J Fish Biol 43: 245–263, 1993

    Google Scholar 

  19. Barroso JB, Peragón J, Contreras-Jurado C, García-Salguero L, Corpas FJ, Esteban FJ, Peinado MA, De la Higuera M, Lupiáñez JA: Impact of starvation-refeeding on kinetics and protein expression of trout liver NADPH-production systems. Am J Physiol 274: R1578–R1587, 1998

    Google Scholar 

  20. Peragón J: Infuencias nutricionales y del peso corporal sobre las velocidades fraccionarias de síntesis y degradación proteicas y su relación con las velocidades de crecimiento en el hígado y músculo blanco de la trucha arco iris (Oncorhynchus mykiss). Ph.D. Thesis. University of Granada, Spain, 1993, p 246

    Google Scholar 

  21. Lowry OH, Rosebrough NJ, Farr JL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275, 1951

    Google Scholar 

  22. Breft JR, Groves TDD: Physiological energetics. In: WS Hoar, DJ Randall, JR Brett (eds). Fish Physiology, Vol. 8. Academic Press, New York, 1979, pp 280–351

    Google Scholar 

  23. Association of Official Analytical Chemists. In: S. Williams (ed). Official Methods of Analysis of the Association of Official Analytical Chemists, 14th ed. AOAC, Washington, DC., 1984, pp 52–160

  24. Garlick PJ, McNurlan MA, Preedy VR: A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H]Phenylalanine. Biochem J 192: 719–723, 1980

    Google Scholar 

  25. Peragón J, Barroso JB, de la Higuera M, Lupiáñez JA: Relationship between growth and protein turnover rates and nucleic acids in the liver of rainbow trout (Oncorhynchus mykiss) during development. Can J Fish Aquat Sci 55: 649–657, 1998

    Google Scholar 

  26. Suzuki O, Yagi K: A fluorometric assay for β-phenylethylamine in rat brain. Anal Biochem 75: 192–200, 1976

    Google Scholar 

  27. Munro HN, Fleck A: The determination of nucleic acids. In: D Glick (ed). Methods of Biochemical Analysis, Vol. XIV. John Wiley and Sons, New York, London, Sidney, 1966, pp 113–176

    Google Scholar 

  28. Ashford A, Pain VM: Effect of diabetes on the rates of synthesis and degradation of ribosomes in rat muscle and liver in vivo. J Biol Chem 261: 4059–4065, 1986

    Google Scholar 

  29. Ceriotti G: A microchemical determination of desoxyribonucleic acid. J Biol Chem 198: 297–301, 1952

    Google Scholar 

  30. Mommsen TP, French CJ, Hochachka PW: Sites and patterns of protein and amino acid utilisation during the spawning migration of salmon. Can J Zool 58: 1785–1799, 1980

    Google Scholar 

  31. Moon TW: Metabolic reserves and enzyme activities with food deprivation in maturing American eel. Can J Zool 61: 802–811, 1983

    Google Scholar 

  32. Houlihan DF: Protein turnover in Ectotherms and its relationships to energetics. In: R Gilles (ed). Advances in Comparative and Environmental Physiology, Vol. 7. Springer-Verlag, Berlin, 1991, pp 1–43

    Google Scholar 

  33. Haschemeyer AEV: A comparative study of protein synthesis in nototheniids and icefish at Palmer Station, Antarctica. Comp Biochem Physiol 76B: 541–543, 1983

    Google Scholar 

  34. McNurlan MA, Tomkins AM, Garlick PJ: The effect of the starvation on the rate of protein synthesis in rat liver and small intestine. Biochem J 178: 373–379, 1979

    Google Scholar 

  35. Bulow FJ: RNA:DNA ratios as indicators of growth in fish: A review. In: RC Summerfelt, GE Hall (eds). Age and Growth of Fish. Iowa State University Press, 1987, pp 45–64

  36. Millward DJ, Garlick PJ, James WPT, Nnanyelugo DO, Ryatt JS: Relationship between protein synthesis and RNA content in skeletal muscle. Nature 241: 204–205, 1973

    Google Scholar 

  37. Enwonwu CO, Munro HN: Rate of RNA turnover in rat liver in relation to intake of protein. Arch Biochem Phys 138: 532–539, 1970

    Google Scholar 

  38. Enwonwu CO, Stambough R, Sreebny L: Synthesis and degradation of liver ribosomal RNA in fed and fasted rats. J Nutr 101: 337–345, 1970

    Google Scholar 

  39. López-Navarro AT, Ortega MA, Peragón J, Bueno JD, Gil A, Sánchez-Pozo A: Deprivation of dietary nucleotides decreases protein synthesis in the liver and small intestine in rats. Gastroenterology 110: 1760–1769, 1996

    Google Scholar 

  40. Scornick OA, Botbol V: Role of changes in protein degradation in the growth of regenerating livers. J Biol Chem 251: 2891–2897, 1976

    Google Scholar 

  41. Hilton JW, Plisetskaya EM, Leatherland JF: Does oral 3,5,3′, triiodo-L-thyronine affect dietary glucose utilization and plasma insulin levels in rainbow trout (Salmo gairdneri). Fish Physiol Biochem 4: 113–120, 1988

    Google Scholar 

  42. Jepson MM, Bates PC, Millward PJ: The role of insulin and thyroid hormones in the regulation of muscle growth and protein turnover in response to dietary protein. Br J Nutr 59: 397–415, 1988

    Google Scholar 

  43. De la Higuera M; Garzón A, Hidalgo MC, Peragón J, Cardenete G, Lupiáñez JA: Influence of temperature and dietary supplementation either with free or coated lysine on the fractional protein turnover rates in the white muscle of carp. Fish Physiol Biochem 18: 85–95, 1997

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Centre of Biological Sciences, University of Granada, Granada, E-1800, Spain

    Juan Peragón, Juan B. Barroso, Leticia García-Salguero & José A. Lupiáñez

  2. Department of Experimental Biology, Biochemistry and Molecular Biology Section, University of Jaén, E-2307, Jaén, Spain

    Juan Peragón, Juan B. Barroso & Fermín Aranda

  3. Department of Animal Biology and Ecology, Centre of Biological Sciences, University of Granada, Granada, E-1800, Spain

    Manuel de la Higuera

Authors
  1. Juan Peragón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan B. Barroso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leticia García-Salguero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fermín Aranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manuel de la Higuera
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. José A. Lupiáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peragón, J., Barroso, J.B., García-Salguero, L. et al. Selective changes in the protein-turnover rates and nature of growth induced in trout liver by long-term starvation followed by re-feeding. Mol Cell Biochem 201, 1–10 (1999). https://doi.org/10.1023/A:1006953917697

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006953917697

Search

Navigation