Abstract
BackgroundBarbels are integumentary sense organs found in fishes, reptiles and amphibians. The zebrafish, Danio rerio, develops paired nasal and maxillary barbels approximately one month post fertilization. Small in diameter and optically clear, these adult appendages offer a window on the development, maintenance and function of multiple cell types including skin cells, neural-crest derived pigment cells, circulatory vessels, taste buds and sensory nerves. Importantly, barbels in other otophysan fishes (e.g., catfish) are known to regenerate; however, this capacity has not been tested in zebrafish.Methodology/Principal FindingsWe describe the development of the maxillary barbel in a staged series of wild type and transgenic zebrafish using light microscopy, histology and immunohistochemistry. By imaging transgenic zebrafish containing fluorescently labeled endothelial cells (Tg(fli1a:EGFP)), we demonstrate that the barbel contains a long (∼2–3 mm) closed-end vessel that we interpret as a large lymphatic. The identity of this vessel was further supported by live imaging of the barbel circulation, extending recent descriptions of the lymphatic system in zebrafish. The maxillary barbel can be induced to regenerate by proximal amputation. After more than 750 experimental surgeries in which approximately 85% of the barbel's length was removed, we find that wound healing is complete within hours, followed by blastema formation (∼3 days), epithelial redifferentiation (3–5 days) and appendage elongation. Maximum regrowth occurs within 2 weeks of injury. Although superficially normal, the regenerates are shorter and thicker than the contralateral controls, have abnormally organized mesenchymal cells and extracellular matrix, and contain prominent connective tissue “stumps” at the plane of section—a mode of regeneration more typical of mammalian scarring than other zebrafish appendages. Finally, we show that the maxillary barbel can regenerate after repeated injury and also in senescent fish (>2 years old).Conclusions/SignificanceAlthough the teleost barbel has no human analog, the cell types it contains are highly conserved. Thus “barbology” may be a useful system for studying epithelial-mesenchymal interactions, angiogenesis and lymphangiogenesis, neural pathfinding, wound healing, scar formation and other key processes in vertebrate physiology.
Highlights
Development and regeneration are often studied in tandem, and share much in common
Location and Growth of the Zebrafish Maxillary Barbel The maxillary barbel is an elongated whisker-like structure extending from the posterior ventral corner of the zebrafish maxilla (Fig. 1A)
Both pairs emerge as epithelial buds approximately 30–40 days post-fertilization at 28uC [31] and grow throughout the lifespan (Fig. 1B)
Summary
Development requires local coordination of cell division, distribution, differentiation, and death. Regeneration recapitulates these processes after injury or amputation, restoring some or all of the missing tissue. Not every organ in this species has the same regenerative capacity Solving this puzzle within the context of the zebrafish genome is an important step towards more effective regenerative medicine in highly refractory species, including our own. In this investigation, we explore the development and regeneration of the zebrafish maxillary barbel, an adult appendage that has received little research attention. Barbels in other otophysan fishes (e.g., catfish) are known to regenerate; this capacity has not been tested in zebrafish
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