The area composita of adhering junctions connecting heart muscle cells of vertebrates. VI. Different precursor structures in non-mammalian species.
Recent studies on the formation and molecular organization of the mammalian heart have emphasized the architectural and functional importance of the adhering junctions (AJs), which are densely clustered in the bipolar end regions (intercalated disks, IDs) connecting the elongated cardiomyocytes of the adult heart. Moreover, we learned from genetic studies of mutated AJ proteins that desmosomal proteins, which for the most part are integral components of ID-specific composite AJs (areae compositae, AC), are essential in heart development and function. Developmental studies have shown that the bipolar concentration of cardiomyocyte AJs in IDs is a rather late process and only completed postnatally. Here we report that in the adult hearts of diverse lower vertebrates (fishes, amphibia, birds) most AJs remain separate and distinct in molecular character, representing either fasciae adhaerentes, maculae adhaerentes (desmosomes) or--less frequently--some form of AC. In the mature hearts of the amphibian and fish species examined a large proportion of the AJs connecting cardiomyocytes is not clustered in the IDs but remains located on the lateral surfaces where they appear either as puncta adhaerentia or as desmosomes. In many places, these puncta connect parallel cardiomyocytes in spectacular ladder-like regular arrays (scalae adhaerentes) correlated with--and connected by--electron-dense plaque-like material to sarcomeric Z-bands. In the avian hearts, on the other hand, most AJs are clustered in the IDs but only a small proportion of the desmosomes appears as AC, compared to the dominance of distinct fasciae adhaerentes. We conclude that the fusion and amalgamation of AJs and desmosomes to ACs is a late process both in ontogenesis and in evolution. The significance and possible functional implications of the specific junctional structures in vertebrate evolution and the class-specific requirements of architectural and molecular assembly adaptation during regeneration processes are discussed.
Pieperhoff
Sebastian
S
Division of Cell Biology, German Cancer Research Center (DKFZ), Im Neuenheimer Feld 280, D-69120 Heidelberg, Germany.
Franke
Werner W
WW
D022005:Adherens Junctions / Q000502:physiology*; D000663:Amphibians / Q000502:physiology; D000818:Animals; D000906:Antibodies / Q000494:pharmacology; D005075:Biological Evolution; D002478:Cells, Cultured; D002645:Chickens / Q000502:physiology; D010856:Columbidae / Q000502:physiology; D051180:Desmoplakins / Q000276:immunology / Q000378:metabolism; D004524:Eels / Q000502:physiology; D006321:Heart / Q000502:physiology; D008854:Microscopy, Electron; D008954:Models, Biological; D032383:Myocytes, Cardiac / Q000502:physiology* / Q000648:ultrastructure*; D017686:Oncorhynchus mykiss / Q000502:physiology; D051191:Plakophilins / Q000276:immunology / Q000378:metabolism; D013045:Species Specificity; D014714:Vertebrates / Q000502:physiology*; D015027:Zebrafish / Q000502:physiology
D000906:Antibodies; D051180:Desmoplakins; D051191:Plakophilins