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First published online December 10, 2003
Journal of Experimental Biology 207, 357-367 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00747

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Seasonality of the red blood cell stress response in rainbow trout (Oncorhynchus mykiss)

P. Koldkjær^1,*, T. G. Pottinger², S. F. Perry³ and A. R. Cossins¹

¹ School of Biological Sciences, University of Liverpool, The Biosciences Building, Crown Street, Liverpool L69 7ZB, UK
² CEH Windermere, The Ferry House, Far Sawrey, Ambleside, Cumbria LA22 0LP, UK
³ Department of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5

^* Author for correspondence (e-mail: piak{at}liv.ac.uk)

Accepted 9 October 2003

The ß-adrenergic stress response in red blood cells (RBCs) of rainbow trout shows seasonal changes in expression. We have explored the mechanisms underpinning this response by following, over a period of 27 months, changes in ß-adrenergic receptor (ß-AR) binding characteristics, ß-adrenergically stimulated RBC Na⁺/H⁺ exchanger (ßNHE) activity, together with ß-AR and ßNHE mRNA levels and plasma steroid hormone and lactate levels. These parameters were measured at approximately monthly intervals in a single population of fish held under semi-natural conditions. Membrane-bound, high-affinity ß-ARs were present in RBCs at all sampling times, varying from 668±112 receptors cell^-1 to 2654±882 receptors cell^-1 (mean ± S.E.M.; N=8). ßNHE activity, however, was reduced by 57% and 34% in December 1999 and February 2001, respectively, compared with an otherwise sustained influx that averaged 110.4±2.3 mmol l^-1 RBCs h^-1 (N=119). Only one reduction coincided with a spawning period but both were preceded by transient increases in circulating testosterone. ßNHE activity measured under standard conditions was not correlated with the number or affinity of ß-ARs nor with water temperature, but both ß-AR numbers and ßNHE activity were positively related to their respective mRNA levels (P=0.005 and 0.038, respectively). Pharmaceutical intervention in the transduction cascade linking the ß-AR and ßNHE failed to indicate any failure of the transduction elements in RBCs displaying low ßNHE activity. Similarly, we failed to demonstrate any link between seasonal cortisol fluctuations and seasonally reduced ßNHE activity. However, the ßNHE activity of age-separated RBC fractions showed that younger RBCs had a significantly higher ßNHE response than older RBCs, consistent with the seasonal reductions in ßNHE being linked to turnover of RBCs and erythropoiesis. Testosterone is known to induce erythropoiesis and we conclude that seasonal reductions in ßNHE are not caused by changes in ß-AR numbers but may be linked to testosterone-induced erythropoiesis.

Key words: adrenergic receptor, Na⁺/H⁺ exchanger, oestradiol, testosterone, cortisol, seasonal changes, rainbow trout, Oncorhynchus mykiss

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