Cellular and molecular changes in heart muscle structures of semelparous pacific salmonid fish species during development of sudden death cardiomyopathy
Final Report Abstract
Normal cardiac anatomy of salmonid fish and the heart muscle architecture of semelparous Pacific salmon (e.g., sockeye salmon, Oncorhynchus nerka and chum salmon, Oncorhynchus keta) close to the spawning event were investigated during the tenure of the funded project. Anadromous semelparous Pacific salmon migrate in schools of thousands of fish to their natal river streams to spawn and die suddenly thereafter. The causes for this massive postreproductive die-off is still controversely discussed. Previous studies highlighted degenerative changes in the cardiovascular system and possible rapid senescence of the affected semelparous fish species within the salmonid family. Interestingly, postspawning mortality is not common in the closely related anadromous but iteroparous salmonids, such as the Atlantic salmon or the Pacific steelhead trout (the anadromous form of the rainbow trout; Oncorhynchus mykiss). This project aimed to study if there are any signs of cardiac alterations in semelparous Pacific salmonid species which could contribute to sudden postreproductive death. Scanning electron microscopic studies combined with standard light- and immunofluorescence microscopy approaches revealed novel insights into normal salmonid fish heart structure. Salmonid fish hearts exhibit an inner highly trabeculated spongy myocardium and an outer encasing compact myocardium. The inner spongy myocardium was found to be composed of rather flattened sheets than of a more cylindric organization. Such tissue architectures may have evolved during evolution to minimize diffusion distance while maximizing surface area and contractility. Interestingly, investigations of cardiomyocyte adhering junctions, responsible for cell adhesion and force transmission during heart muscle contraction revealed an enrichment of typical desmosomal as well as fascia adhaerens components in the interface connecting spongy and compact myocardium. Studies by other research groups showed the occurrence of dissecting haemorrhages in hearts of seawater reared rainbow trout. Such cardiomyopathy cases were characterized by ruptures or lesions in the aforementioned interface between spongy and compact myocardium and obviously the inner spongy myocardium separated from the encasing compact myocardium resulting in sudden cardiac mortality. However, the interface between compact and spongy myocardium was often found to be a predilection site for alterations and disease suggesting cell adhesion defects in the affected fish when considering the aforementioned discoveries. Cardiomyopathies often result in preslaughter mortalities leading to annual high financial losses in countries such as Norway, Canada or Scotland where salmonids are intensely farmed and further investigations are needed to avoid spreading of such disease states. Studies on heart muscle of prespawning semelparous Pacific salmon then revealed minor fibrotic changes, often as well in the interface between spongy and compact myocardium. Using an implantable flow probe and acoustic ECG transmitters we were able to measure cardiac arrest events during the spawning bouts of anadromous, semelparous Pacific chum and sockeye salmon. Future studies will include anadromous but iteroparous Atlantic salmon or steelhead trout (the anadromous form of Oncorhynchus mykiss), as such species for the most part survive the spawning migration and spawning event. Possible reasons for the occurrence of semelparity in some fish species within the salmonid family may include a predisposition to cardiac sudden death, but further investigations are needed to answer this very important question.
Publications
- 2009. The intercellular organization of the two muscular systems in the adult salmonid heart, the compact and the spongy myocardium. J Anat 215, 536 - 547
Pieperhoff, S., Bennett, W., Farrell, A. P.
- 2009. The junctions that don’t fit the scheme: special symmetrical cell-cell junctions of their own kind. Cell and Tiss Res 338, 1-17
Franke, W. W., Rickelt, S., Barth, M., Pieperhoff, S.
- 2010. Constitutive desmosomal components in cardiac, epithelial and mesenchymally derived cells and their involvement in the development of heart and skin disease states in Desmosomes and desmosomal cadherin function in skin and heart diseases – advancements in basic and clinical research. Mahoney, M. G., Müller, E. J., Koch, P. J., Eds., Dermatology Research and Practice. Hindawi
Pieperhoff, S., Rickelt, S., Barth, M. and Franke, W. W.
- 2010. The area composita of adhering junctions connecting heart muscle cells of vertebrates. VII. The different types of lateral junctions between the special cardiomyocytes of the conduction system of ovine and bovine hearts. Eur J Cell Biol 89, 365-378
Pieperhoff, S., Borrmann, C., Grund, C., Barth, M., Rizzo, S., Franke, W. W.
- 2011. Load-reducing therapy prevents development of arrhythmogenic right ventricular cardiomyopathy in plakoglobin-deficient mice. J Am Coll Cardiol 57(6): 740-50
Fabritz L., Hoogendijk, M. G., Scicluna, B. P., van Amersfoorth, S. C., Fortmueller, L., Wolf, S., Laakmann, S., Kreienkamp, N., Piccini, I., Breithardt, G., Noppinger, P. R., Witt, H., Ebnet, K., Wichter, T., Levkau, B., Franke, W. W., Pieperhoff S., de Bakker, J. M., Coronel, R., Kirchhof, P.
