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Development and regeneration of the zebrafish maxillary barbel: a novel study system for vertebrate tissue growth and repair.

LeClair EE, Topczewski J - PLoS ONE (2010)

Bottom Line: Barbels are integumentary sense organs found in fishes, reptiles and amphibians.Finally, we show that the maxillary barbel can regenerate after repeated injury and also in senescent fish (>2 years old).Although the teleost barbel has no human analog, the cell types it contains are highly conserved.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, DePaul University, Chicago, Illinois, United States of America. eleclair@depaul.edu

ABSTRACT

Background: Barbels 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 findings: We 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 ( approximately 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 ( approximately 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/significance: Although 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.

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Position and growth of the paired barbels in zebrafish.A) Location of the nasal and maxillary barbels (nb and mb) on a wild type adult zebrafish (AB strain). B) Growth curve for the maxillary barbel in a wild type AB strain reared at 28°C. Barbel length (n = 183) was measured in 135 zebrafish of different standard lengths (SL+/−0.5 mm). Each data point represents a single barbel (the right and/or left appendage). The growth curve is similar to that shown in [60].
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pone-0008737-g001: Position and growth of the paired barbels in zebrafish.A) Location of the nasal and maxillary barbels (nb and mb) on a wild type adult zebrafish (AB strain). B) Growth curve for the maxillary barbel in a wild type AB strain reared at 28°C. Barbel length (n = 183) was measured in 135 zebrafish of different standard lengths (SL+/−0.5 mm). Each data point represents a single barbel (the right and/or left appendage). The growth curve is similar to that shown in [60].

Mentions: 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 28°C [31] and grow throughout the lifespan (Fig. 1B). In adult wild type zebrafish in our facility (2–3 cm standard length, SL) the maxillary barbel is approximately 200–300 microns wide at the base, 50 microns wide at the tip, and 2–4 millimeters long. Although both nasal and maxillary barbels contain similar cell types, the larger maxillary barbel is easier to manipulate and visualize, making it the focus of our current study. By convention, we describe the maxillary barbel as though it were oriented horizontally with the distal end pointing caudally. In this orientation, the upper surface of the barbel is called dorsal and the lower surface ventral.


Development and regeneration of the zebrafish maxillary barbel: a novel study system for vertebrate tissue growth and repair.

LeClair EE, Topczewski J - PLoS ONE (2010)

Position and growth of the paired barbels in zebrafish.A) Location of the nasal and maxillary barbels (nb and mb) on a wild type adult zebrafish (AB strain). B) Growth curve for the maxillary barbel in a wild type AB strain reared at 28°C. Barbel length (n = 183) was measured in 135 zebrafish of different standard lengths (SL+/−0.5 mm). Each data point represents a single barbel (the right and/or left appendage). The growth curve is similar to that shown in [60].
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2806924&req=5

pone-0008737-g001: Position and growth of the paired barbels in zebrafish.A) Location of the nasal and maxillary barbels (nb and mb) on a wild type adult zebrafish (AB strain). B) Growth curve for the maxillary barbel in a wild type AB strain reared at 28°C. Barbel length (n = 183) was measured in 135 zebrafish of different standard lengths (SL+/−0.5 mm). Each data point represents a single barbel (the right and/or left appendage). The growth curve is similar to that shown in [60].
Mentions: 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 28°C [31] and grow throughout the lifespan (Fig. 1B). In adult wild type zebrafish in our facility (2–3 cm standard length, SL) the maxillary barbel is approximately 200–300 microns wide at the base, 50 microns wide at the tip, and 2–4 millimeters long. Although both nasal and maxillary barbels contain similar cell types, the larger maxillary barbel is easier to manipulate and visualize, making it the focus of our current study. By convention, we describe the maxillary barbel as though it were oriented horizontally with the distal end pointing caudally. In this orientation, the upper surface of the barbel is called dorsal and the lower surface ventral.

Bottom Line: Barbels are integumentary sense organs found in fishes, reptiles and amphibians.Finally, we show that the maxillary barbel can regenerate after repeated injury and also in senescent fish (>2 years old).Although the teleost barbel has no human analog, the cell types it contains are highly conserved.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, DePaul University, Chicago, Illinois, United States of America. eleclair@depaul.edu

ABSTRACT

Background: Barbels 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 findings: We 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 ( approximately 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 ( approximately 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/significance: Although 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.

Show MeSH
Related in: MedlinePlus