The mammalian heart is characterized by its relative intolerance to injury or the lack of oxygen. This is in part related to its high metabolic demand relative to its glycolytic ability, and in part to the fact that post-neonatal cardiac growth is primarily, but not exclusively (Anversa, 2000
), through hypertrophy. Fish hearts differ in the manner in which they grow, and it appears that the rainbow trout heart grows through both hyperplasia and hypertrophy during ontogeny (Farrell et al., 1988), and by hyperplasia, hypertrophy or both, depending on the environmental or physiological challenge. While mammalian researchers continue to search for ways to stimulate cardiac growth to replace damaged myocardial tissue, it seems that fish never lose this ability (perhaps these researchers should be looking at fish models too!), and it is likely that the high degree of intraspecific plasticity that we describe may well be related to the fact that fish retain hyperplastic as well as hypertrophic myocardial growth. Further, it appears that cardiac remodeling is not restricted to myocytes, but may be a general characteristic of cells that comprise the fish heart. Egginton and Cordiner (1997) showed that myocardial capillary density is maintained in fish acclimated to 4 vs 11°C despite cardiac hypertrophy, and is increased by ~75% in fish acclimated to 18°C. Clark and Rodnick (1998) showed that capillary growth matches cardiac growth associated with sexual maturation in males. Research on rainbow trout indicates that new vessel growth can reestablish coronary blood flow following coronary artery ablation (Daxboeck, 1982; Farrell et al., 1990). Finally, we have observed major remodeling of the bulbus and ventral aorta of Atlantic cod, to allow for the maintenance of cardiac output past the feeding appendages of the haematophagus parasite Lernaeocera branchialis (e.g. see Fig. 7).
Recently, we have shown that a preconditioning-like phenomenon exists in fishes, that there is a significant degree of intraspecific variation in myocardial hypoxia tolerance and the ability to be preconditioned among rainbow trout, and that the spongy myocardium of cod can be preconditioned. These findings strongly suggest that protective pathways can still be stimulated in myocardium that is normally perfused by blood of low oxygen partial pressure, and that preconditioning and acquired hypoxia tolerance in trout are mediated by the same or similar cellular mechanisms. Further, we provide substantial indirect evidence that trout myocytes are not permanently damaged by exposure to prolonged periods (15 min to 4 h) of severe hypoxia, even though contractile function is diminished (Gamperl et al., 2004; Overgaard et al., 2004; J. Overgaard and J. A. W. Stecyk, unpublished). While this enhanced ability of rainbow trout hearts to tolerate long periods of severe hypoxia as compared with mammals is likely to be related in part to temperatures (10–15°C vs 37°C) and absolute workload, we suspect that there are also mechanistic reasons for this difference.
In this review we have demonstrated that the fish heart has tremendous capacity to respond to both short-term and long-term perturbations, and hint at mechanistic explanations of how this is accomplished. However, it is apparent that we have little understanding of the molecular and biochemical signaling pathways that mediate much of this plasticity. Important and obvious questions include: What cellular events are responsible for stimulating hyperplastic vs hypertrophic growth of the fish heart? Which signal transduction pathways and end-effectors mediate preconditioning and inherent hypoxia tolerance of the fish myocardium, and how do they compare with those in mammals? Why does the trout heart not experience permanent damage (necrosis) when exposed to severe hypoxia or anoxia for periods up to 4 h? Our challenge, therefore, is to design experiments that will provide insights into the novel control mechanisms that mediate myocardial plasticity and adaptation in fish.
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