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EDITORIAL FOCUS
3-Adrenergic receptors—studies on rainbow trout reveal ancient evolutionary origins and functions distinct from the thermogenic response
Department of Biology, University of Turku, FIN-20014 Turku, Finland
FOR MOST PHYSIOLOGISTS it is clear that the major function for
3-adrenergic receptors is to mediate metabolic and
thermogenic responses in adipose tissue
(12). Thus one would expect
their distribution to be restricted to homeothermic animals. However, in this
issue of the American Journal of Physiology-Regulatory, Integrative and
Comparative Physiology, Nickerson et al.
(5) report the presence of two
different 3-adrenergic receptors in the tissues of a teleost
fish, rainbow trout. In evolutionary terms, this means that
3-receptor has differentiated from other -adrenergic
receptors before the division of teleost and tetrapod lineages that is
estimated to have happened 350-400,000,000 years ago
(2). Also, the presence of
3-adrenergic receptors in the cells of teleost fish indicates
that this receptor subtype has important functions independent of the
thermogenic response. Although the functions of the
3-adrenergic receptor subtype found in the heart and gill
tissues were not clarified, detailed studies by Nickerson and coworkers
(5) indicate that the red blood
cell type 3-adrenergic receptor controls the function of
adrenergically regulated sodium/proton exchange present in the erythrocytes of
teleost fish. The physiological role of adrenergic stimulation of
sodium/proton exchange in teleost fish has been clarified, as detailed below,
but the adrenergic receptors involved have remained uncharacterized until now.
Pharmacological studies suggested that the receptor subtype involved could be
1 (14).
However, on the basis of earlier studies and those of Nickerson et al.
(5), the mammalian
pharmacological classification does not fit the teleost receptors. Thus the
molecular characterization of the receptor with unique pharmacological
properties is a significant step forward also in this regard.
With regard to the physiological role of the 3-adrenergic
receptor in teleost erythrocytes, in the early 1980s it was discovered that
catecholamines (epinephrine and norepinephrine) could very rapidly increase
the hemoglobin-oxygen affinity as a result of an increase in erythrocyte pH
(6,
7). The increase in erythrocyte
pH was shown to be due to -adrenergic activation of sodium/proton
exchange across the erythrocyte membrane
(1,
10), using cAMP as a second
messenger (4). The adrenergic
response augments oxygen transport by increasing erythrocyte pH when oxygen
availability in ambient water is reduced
(13) and protects oxygen
loading in gills in exhaustive exercise by maintaining erythrocyte pH when
blood plasma is acidified (9,
11). The erythrocyte response
to catecholamines presents a new type of stress response that is observed in
physiological conditions in many teleost fishes, but not in cyclostomes, most
amphibians, birds, or mammals
(8). In birds, another ion
transport pathway, the sodium/potassium/2 chloride cotransport
(3), is -adrenergically
activated. Interestingly, the -receptor subtype of bird erythrocyte
membrane, termed 4, also belongs to the
3-adrenergic receptor family. Thus, because effects on ion
transport occur in evolutionarily distant species, it is tempting to speculate
that the initial function of 3-receptor is related to ion
transport.
The study by Nickerson et al. (5) shows the strengths of comparative physiology: experiments on teleost fish shed light on both the evolution and the initial functions of a receptor, which has evolved to a very specific system in homeothermic mammals. Clearly, as indicated by the present studies, a combination of molecular methodology and the comparative approach is a very useful tool for future investigations of physiological regulation.
FOOTNOTES
Address for reprint requests and other correspondence: M. Nikinmaa, Dept. of
Biology, Univ. of Turku, FIN-20014 Turku, Finland (E-mail:
miknik{at}utu.fi).
REFERENCES
-adrenergic Na+/H+ exchanger in trout erythrocytes
is controlled by a novel 3-AR subtype. Am J
Physiol Regul Integr Comp Physiol 285:
R526-R535, 2003.-adrenergic responses. J
Comp Physiol [B] 154:
365-369, 1984.
3-adrenergic receptor. Annu Rev Pharmacol
Toxicol 37:
421-450, 1997.[ISI][Medline]
-adrenergic proton extrusion from red cells of rainbow trout,
Salmo gairdneri. J Exp Biol
134: 267-280,
1988.
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