Abstract
Aquatic vertebrates possess diverse types of sensory cells in their skin to detect stimuli in the water. In the adult zebrafish, a common model organism, the presence of such cells in fins has only rarely been studied. Here, we identified scattered serotonin (5-HT)-positive cells in the epidermis of the caudal fin. These cells were distinct from keratinocytes as revealed by their low immunoreactivity for cytokeratin and desmosome markers. Instead, they were detected by Calretinin (Calbindin-2) and Synaptic vesicle glycoprotein 2 (SV2) antibodies, indicating a calcium-regulated neurosecretory activity. Consistently, electron microscopy revealed abundant secretory organelles in desmosome-negative cells in the fin epidermis. Based on the markers, 5-HT, Calretinin and SV2, we referred to these cells as HCS-cells. We found that HCS-cells were spread throughout the entire caudal fin at an average density of 140 cells per mm2 on each fin surface. These cells were strongly enriched at ray bifurcations in wild type fins, as well as in elongated fins of another longfin mutant fish. To determine whether hydrodynamics play a role in the distribution of HCS-cells, we used an interdisciplinary approach and performed kinematic analysis. Measurements of particle velocity with a fin model revealed differences in fluid velocities between bifurcated rods and adjacent non-bifurcated regions. Therefore the accumulation of HCS-cells near bone bifurcations may be a biological adaptation for sensing of water parameters. The significance of this HCS-cell pattern is reinforced by the fact, that it is reestablished in the regenerated fin after amputation. Regeneration of HCS-cells was not impaired by the chemical inhibition of serotonin synthesis, suggesting that this neurotransmitter is not essential for the restorative process. In conclusion, our study identified a specific population of solitary paraneurons in the zebrafish fin, whose distribution correlates with fluid dynamics.
Highlights
The skin is continuously exposed to environmental fluctuations and external signals
Epidermal sensors can be arranged into multicellular structures, e.g., taste buds and mechanoreceptive neuromasts, or they can occur as scattered cells, e.g., solitary chemosensory cells and Merkellike cells (Whitear, 1992; Kotrschal, 1996; Kasumyan, 2011; Coombs et al, 2013)
The caudal fin propels the fish during swimming. The surface of this locomotory appendage is exposed to water flows which carry mechanical and chemical information
Summary
The skin is continuously exposed to environmental fluctuations and external signals. In the epidermis, specialized cells recognize specific stimuli and transmit this information to the body through secretion of active compounds, such as hormones and neurotransmitters (Slominski et al, 2012). Sensory structures evolved distributions suitable for the types of stimuli and the environmental media Aquatic vertebrates, such as lampreys, fish, and amphibian tadpoles, can detect hydrodynamic parameters and dissolved chemicals through their epidermal sensors adapted for underwater conditions (Atema et al, 1988; von der Emde et al, 2004; Collin et al, 2008; Finger, 2009). Their mucuscovered epidermis contains various types of specialized chemoand mechanoreceptors. Epidermal sensors can be arranged into multicellular structures, e.g., taste buds and mechanoreceptive neuromasts, or they can occur as scattered cells, e.g., solitary chemosensory cells and Merkellike cells (Whitear, 1992; Kotrschal, 1996; Kasumyan, 2011; Coombs et al, 2013)
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