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The effects of cell ageing on protein synthesis in rainbow trout (Oncorhynchus mykiss) red blood cells
S.G. Lund, M.C. Phillips, C.D. Moyes, B.L. Tufts
Journal of Experimental Biology 2000 203: 2219-2228;

Summary

The effects of cell age on protein synthesis were examined in the nucleated red blood cells of rainbow trout (Oncorhynchus mykiss). Total DNA content was unaffected by cell age, whereas total RNA content in young red blood cells was roughly ten times as high as that in old red blood cells. The mRNA levels for haemoglobin, carbonic anhydrase and the chloride/bicarbonate (Cl(−)/HCO(3)(−)) exchanger were also approximately tenfold higher in young red blood cells. Although young red blood cells synthesized roughly five times more protein under steady-state conditions, total protein concentration was not affected by cell age. Despite large reductions in mRNA levels with red blood cell ageing, the concentrations and/or activities of the respiratory proteins were largely preserved. In contrast, the ability to mount a heat shock response was greatly reduced in older red blood cells. Young red blood cells produced 13 times more heat shock protein 70 mRNA following heat shock and four times more 70 kDa protein after recovery. They also transcribed much more heat shock cognate 71 and heat shock factor mRNA than did older red blood cells under steady-state conditions.

REFERENCES

    1. Becker, J. and
    2. Craig, E. A.
    (1994). Heat-shock proteins as molecular chaperones. Eur. J. Biochem 219, 11–.
    OpenUrlPubMedWeb of Science
    1. Betke, K. and
    2. Savelsberg, W.
    (1950). Stufenphotometrische hämoglobinstimmung mittels cyanhämoglobin. Biochem. Z 320, 431–.
    OpenUrlPubMed
    1. Boutilier, R. G. and
    2. Ferguson, R. A.
    (1989). Nucleated red cell function: metabolism and pH regulation. Can. J. Zool 67, 2986–.
    OpenUrl
    1. Chomczynski, P. and
    2. Sacchi, N.
    (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate—phenol—chloroform extraction. Analyt. Biochem 162, 156–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Cohen, N. S.,
    2. Ekholm, J. E.,
    3. Luthra, M. G. and
    4. Hanahan, D. J.
    (1976). Biochemical characterization of density-separated human erythrocytes. Biochim. Biophys. Acta 419, 229–.
    OpenUrlPubMed
    1. Currie, S. and
    2. Tufts, B. L.
    (1997). Synthesis of stress protein 70 (Hsp70) in rainbow trout (Oncorhynchus mykiss) red blood cells. J. Exp. Biol 200, 607–.
    OpenUrlAbstract
    1. Currie, S.,
    2. Tufts, B. L. and
    3. Moyes, C. D.
    (1999). Influence of bioenergetic stress on heat shock protein gene expression in nucleated red blood cells of fish. Am. J. Physiol 276, 990–.
    OpenUrl
    1. Denton, J. E. and
    2. Yousef, M. K.
    (1975). Seasonal changes in hematology of rainbow trout, Salmo gairdneri. Comp. Biochem. Physiol 51, 151–.
    OpenUrlCrossRef
    1. Härdig, J.
    (1978). Maturation of circulating red blood cells in young Baltic salmon (Salmo salar L.). Acta Physiol. Scand 102, 290–.
    OpenUrlPubMed
    1. Hartl, F. U.
    (1996). Molecular chaperones in cellular protein folding. Nature 381, 571–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Henry, R. P.,
    2. Tufts, B. L. and
    3. Boutilier, R. G.
    (1993). The distribution of carbonic anhydrase type I and II isozymes in lamprey and trout: possible co-evolution with erythrocyte chloride/bicarbonate exchange. J. Comp. Physiol 163, 380–.
    OpenUrl
    1. Hevesy, G.,
    2. Lockner, D. and
    3. Sletten, K.
    (1964). Iron metabolism and erythrocyte formation in fish. Acta Physiol. Scand 60, 256–.
    OpenUrlPubMed
    1. Houston, A. H. and
    2. Murad, A.
    (1991). Hematological characterization of goldfish, Carassius auratus L., by image analysis: effects of thermal acclimation and heat shock. Can. J. Zool 69, 2041–.
    OpenUrl
    1. Hubner, S.,
    2. Michel, F.,
    3. Rudloff, V. and
    4. Appelhans, H.
    (1992). Amino acid sequence of band-3 protein from rainbow trout erythrocytes derived from cDNA. Biochem. J 285, 17–.
    1. Keen, A. M.,
    2. Steele, C. and
    3. Houston, A. H.
    (1989). The circulating erythrocytes of rainbow trout. Comp. Biochem. Physiol 94, 699–.
    OpenUrlCrossRef
    1. Laemmli, E. K.
    (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Lane, H.
    (1984). Nucleoside triphosphate changes during the peripheral lifespan of erythrocytes of rainbow trout (Salmo gairdneri). J. Exp. Zool 231, 57–.
    OpenUrlCrossRefPubMed
    1. Leary, S. C.,
    2. Battersby, B. J.,
    3. Hansford, R. G. and
    4. Moyes, C. D.
    (1998). Interactions between bioenergetics and mitochondrial biogenesis. Biochim. Biophys. Acta 1365, 522–.
    OpenUrlPubMed
    1. Lee, Y.-K.,
    2. Manalo, D. and
    3. Liu, A. Y.-C.
    (1996). Heat shock response, heat shock transcription factor and cell ageing. Biol. Signals 5, 180–.
    OpenUrlPubMedWeb of Science
    1. Liu, A. Y.-C.,
    2. Lin, Z.,
    3. Choi, H.-S.,
    4. Sorhage, F. and
    5. Li, B.
    (1989). Attenuated induction of heat shock gene expression in ageing diploid fibroblasts. J. Biol. Chem 264, 12037–.
    OpenUrlAbstract/FREE Full Text
    1. Mestril, R. and
    2. Dillman, W. H.
    (1995). Heat shock proteins and protection against myocardial ischemia. J. Mol. Cell. Cardiol 27, 45–.
    OpenUrlPubMedWeb of Science
    1. Morimoto, R. I.
    (1993). Cells in stress: transcriptional activation of heat shock genes. Science 259, 1409–.
    OpenUrlFREE Full Text
    1. Murphy, J.
    (1973). Influence of temperature and method of centrifugation on the separation of erythrocytes. J. Lab. Clin. Med 82, 334–.
    OpenUrlPubMedWeb of Science
    1. Nadeau, K.,
    2. Das, A. and
    3. Walsh, C. T.
    (1993). Hsp 90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem 268, 1479–.
    OpenUrlAbstract/FREE Full Text
    1. Pahlavani, M. A.,
    2. Harris, M. D.,
    3. Moore, S. A.,
    4. Weindruch, R. and
    5. Richardson, A.
    (1995). The expression of heat shock protein 70 decreases with age in lymphocytes from rats and rhesus monkeys. Exp. Cell Res 218, 310–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Parsell, D. A. and
    2. Lindquist, S.
    (1993). The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet 27, 437–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Perry, S. F.
    (1986). Carbon dioxide excretion in fish. Can. J. Zool 64, 565–.
    OpenUrlCrossRef
    1. Perry, S. F. and
    2. Gilmour, K.
    (1993). An evaluation of factors limiting carbon dioxide excretion by trout red blood cells in vitro. J. Exp. Biol 180, 39–.
    OpenUrlAbstract/FREE Full Text
    1. Peterson, R. E.,
    2. Tu, C. and
    3. Linser, P. J.
    (1997). Isolation and characterization of a carbonic anhydrase homologue from the zebrafish (Danio rerio). J. Mol. Evol 44, 432–.
    OpenUrlCrossRefPubMed
    1. Phillips, M. C. L.,
    2. Moyes, C. D. and
    3. Tufts, B. L.
    (2000). The effects of cell ageing on metabolism in rainbow trout (Oncorhynchus mykiss) red blood cells. J. Exp. Biol 203, 1039–.
    OpenUrlAbstract
    1. Rabindran, S. H.,
    2. Giorgi, G.,
    3. Clos, J. and
    4. Wu, C.
    (1991). Molecular cloning and expression of a human heat shock factor, HSF 1. Proc. Natl. Acad. Sci. USA 88, 6906–.
    OpenUrlAbstract/FREE Full Text
    1. Sekhon, S. S. and
    2. Beams, H. W.
    (1969). Fine structure of the developing trout erythrocytes and thrombocytes with special reference to the marginal band and the cytoplasmic organelles. Am. J. Anat 125, 353–.
    OpenUrlCrossRefPubMed
    1. Speckner, W.,
    2. Schindler, J. F. and
    3. Albers, C.
    (1989). Age-dependent changes in volume and haemoglobin content of erythrocytes in the carp (Cyprinus carpio L.). J. Exp. Biol 141, 133–.
    OpenUrlAbstract/FREE Full Text
    1. Stabeneau, E. K.,
    2. Vanoye, C. G. and
    3. Heming, T. A.
    (1991). Characteristics of the anion transport system in sea turtle erythrocytes. Am. J. Physiol 261, 1218–.
    OpenUrl
    1. Tooze, J. and
    2. Davies, H. G.
    (1963). The occurrence and possible significance of haemoglobin in the chromosomal regions of mature erythrocyte nuclei of the newt Triturus cristanus cristanus. J. Exp. Biol 141, 133–.
    1. van Kampen, E. J. and
    2. Zijlstra, W. G.
    (1961). Standardization of hemoglobinometry. II. The hemoglobincyanide method. Clin. Chim. Acta 6, 538–.
    OpenUrlCrossRefPubMedWeb of Science
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Journal Articles
The effects of cell ageing on protein synthesis in rainbow trout (Oncorhynchus mykiss) red blood cells
S.G. Lund, M.C. Phillips, C.D. Moyes, B.L. Tufts
Journal of Experimental Biology 2000 203: 2219-2228;
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