Rodlet cells and the sensory systems in zebrafish (Danio rerio)
Article first published online: 7 MAR 2007
Copyright © 2007 Wiley-Liss, Inc.
The Anatomical Record
Volume 290, Issue 4, pages 367–374, April 2007
How to Cite
Dezfuli, B. S., Capuano, S., Simoni, E., Previati, M. and Giari, L. (2007), Rodlet cells and the sensory systems in zebrafish (Danio rerio). Anat Rec, 290: 367–374. doi: 10.1002/ar.20507
- Issue published online: 26 MAR 2007
- Article first published online: 7 MAR 2007
- Manuscript Accepted: 18 JAN 2007
- Manuscript Received: 2 NOV 2006
- Italian Ministry of the University and Scientific Research and Technology
- rodlet cells;
- sensory systems;
- Danio rerio
This preliminary work was designed to study, using routine procedures for light and transmission electron microscopy, the presence of rodlet cells (RCs) in or near the sensory systems of 12 adult specimens (4.0 ± 1.2 cm, LT ± SD) of zebrafish, Danio rerio Hamilton, 1822. Rodlet cells, characterized by a distinctive cell cortex (range, 0.4–1.5 μm in thickness) and conspicuous inclusions named “rodlets,” have a round to ovoid nucleus with irregular outline. Mature RCs are 11.5 ± 1.2 μm (mean ± SD) long and 7.8 ± 1.1 μm (mean ± SD) wide. These cells are more numerous near neuromasts enclosed by an epithelial roof and/or ossified canal wall. In contrast, very few RCs were noticed near superficial neuromasts. Based on the presence of RCs around the two cranial neuromasts of each fish, a variable number from 1 to 15 rodlet cells was found (10.4 ± 3.6, mean ± SD). The RCs were located 1.5 μm (minimal) to 73.3 μm (maximal) from the neuromast (27.9 ± 17.2, mean ± SD). Moreover, RCs were found in olfactory epithelium and in proximity to some taste buds. Interestingly, RCs were absent in the inner ear, eye, and brain. Anat Rec, 2007. © 2007 Wiley-Liss, Inc.
Neuromasts are known as superficial mechanosensory organs occurring in the lateral line of fishes. They function to facilitate schooling, avoid predators, capture prey, and detect vibration in the surrounding environment (Webb, 1989; Uchiyama et al., 1991; Gompel et al., 2001). The inner ear and lateral systems are closely related to each other developmentally, functionally, and evolutionary (Williams and Holder, 2000). They form mechanosensory organs of vertebrates, the inner ear occurring in all vertebrates while neuromasts occurring only in aquatic anamniotes (Song et al., 1995).
Two types of neuromasts have been recognized and named depending on their position: canal and superficial (Coombs et al., 1988; Münz, 1989). In most fishes, the canal neuromasts are enclosed within a structure such as open grooves, bony canals (Metcalfe, 1989), or scales. In contrast, the so-called superficial or free neuromasts are not enclosed in a structure and are detectable on the surface of the epidermis (Song et al., 1995). Structurally, neuromasts are comprised of a ring of supporting cells encircling a central cluster of sensory hair cells.
Olfactory and gustative structures are a portion of the chemoreception organs, which play an important role in fish behavior (Hara, 1971; Oliveira Ribeiro et al., 1995; Mandal et al., 2005). These chemical sense organs (olfactory epithelium and taste buds) are involved in many life-sustaining events such as sex recognition, defense against predators, parental behavior, spatial orientation, and food procurement (Døving, 1986; Hara, 1994).
During this investigation, a special type of fish cell, namely rodlet cells (RCs), was noticed adjacent to neuromasts and within the olfactory epithelium of D. rerio. For over a century, fish histologists and pathologists have attempted to determine the origin and functions of these RCs. Morphologically, they are characterized by a distinctive cell cortex and conspicuous inclusions, called rodlets; hence their namesake. Since their discovery, RCs have been encountered in a wide range of tissues of freshwater and marine teleosts (Leino, 1974; Morrison and Odense, 1978; Dezfuli et al., 1998, 2000, 2007; Bielek, 2005; Mazon et al., 2007). Rodlet cells have been associated most often with epithelia, e.g., skin (Iger and Abraham, 1997), gill (Leino, 1974; Dezfuli et al., 2003a), intestine (Paterson and Desser, 1981; Dezfuli et al., 1998, 2003b; Bielek, 2002), kidney tubule (Leino, 1996; Bielek, 2002; Kramer and Potter, 2002), endothelia (Smith et al., 1995; Koponen and Myers, 2000; Manera et al., 2001), and mesothelia (Dezfuli et al., 2000).
Differing points of view on the nature of rodlet cells have been proposed since their first description by Thélohan (1892). After 1895, several authors held the view that RCs are parasites (Laguesse, 1895; Bannister, 1966; Mayberry et al., 1979; Viehberger and Bielek, 1982; Richards et al., 1994). The main arguments of those claiming RCs are parasites include: they vary in number from fish to fish; they often cannot be found in all individuals of the same species; they occur in different tissues of the same species; they possess a distinct capsule; and they have sporozoite-like inclusions. For a long time, authors favoring the view that RCs are parasites believed that RCs belonged to the Apicomplexa (Bannister, 1966; Mayberry et al., 1979; Viehberger and Bielek, 1982).
The literature supporting the view that RCs are in fact endogenous fish cells and not parasites is extensive. There are several points that favor the argument for the endogenous nature of these cells. First, the wide distribution of RCs within fish tissues and among fish species is not a feature of Apicomplexa, a group of parasites noted for having strict tissue and host specificity (Flood et al., 1975). Second, in studies involving vast numbers of individual fish, no evidence of disruption or inflammation of surrounding tissue by RCs could be found (Manera and Dezfuli, 2004). Third, RCs have been found in neonate or very young laboratory-reared fish, in embryos of viviparous teleosts, and in newly hatched fish (Leino, 1974; Calzada et al., 1998; Kramer and Potter, 2003; Mazon et al., 2007). All of the fish in these above-mentioned instances were obtained under pathogens-free controlled conditions.
Catton (1951) and Bullock (1963), among others, suggested that RCs resembled a type of fish granular leukocyte. In contrast, other researchers (Barrington, 1957; Bishop and Odense, 1966; Wilson and Westerman, 1967) concurred with Plehn's (1906a, 1906b) original suggestion that RCs are of a glandular nature. In fact, ultrastructural study of these cells in several freshwater and marine teleosts supports the latter suggestion (Leino, 1974, 1996; Flood et al., 1975; Reite, 1998, 2005; Dezfuli et al., 2000, 2003a). Functionally, RCs have been considered regulatory elements related to unique functions such as osmoregulation (Fernhead and Fabian, 1971; Mattey et al., 1979) and ion transportation (Morrison and Odense, 1978). They have been identified as fish blood cells (Weinreb and Bilstad, 1955), secretory cells (Leino, 1974, 1996; Grünberg and Hager, 1978; Mattey et al., 1979), transport units for genetic material (Viehberger and Bielek, 1982), and nonspecific immune cells (Sulimanovic et al., 1996; Iger and Abraham, 1997; Dezfuli et al., 1998, 2000, 2002, 2003a, 2003b, 2007; Imagawa et al., 1998; Manera et al., 2001; Mazon et al., 2007). Currently, there is only one published study in which the authors attributed a sensory function to the RCs (Wilson and Westerman, 1967). However, the results of our previous and present study rule out this latter suggestion.
Our present study is the first to document the presence of RCs near the neuromasts in fish. This site was unexpected. A hypothesis about RC function will be presented because our current knowledge is far too limited to provide a concrete explanation.
MATERIALS AND METHODS
Twelve adult specimens of zebrafish (mean LT ± SD, 4.0 ± 1.2 cm) from the same parent stock were obtained from a local supplier. The fish were killed by a blow to the head, subsequently pithed and dissected.
Seven whole individuals were designated for paraffin embedding and five heads were designated for resin embedding. For light microscopy, heads and bodies were fixed separately by immersion in Bouin's fluid for 8 hr, dehydrated, and embedded in paraffin. Tissue sections (5 μm) were stained with hematoxylin-eosin. For electron microscopy, heads were fixed at 4°C for 2 hr in 2% glutaraldehyde solution buffered with 0.1 M sodium cacodylate (pH 7.2). The pieces were rinsed for 12 hr in 0.1 M sodium cacodylate buffer containing 6% sucrose, then postfixed in 1% osmium tetroxide in the same buffer for 2 hr before dehydrating in a graded series of ethanol. Finally, pieces were transferred to propylene oxide and embedded in an Epon-Araldite mixture. Semithin sections (1.5 μm) were cut on a Reichert Om U2 ultramicrotome with glass knives. Ultrathin sections were stained with toluidine blue, contrasted in a 50% alcohol-uranyl acetate solution and lead citrate, and examined with a Hitachi H-800 electron microscope operated at 80 kV.
The numbers and dimensions of rodlet and mucous cells were registered using a computerized image analysis software (Lucia G 4.8; Laboratory Imaging, Praha, Czech Republic).
Neuromasts were observed mainly in the cranial region of each fish (Fig. 1). At this tissue site, the vast majority of the neuromasts were of the third type (Webb and Shirey, 2003), namely, those enclosed by epithelial roof (Figs. 1 and 2). Moreover, superficial or free neuromasts (Fig. 3) were rarely found in the head region.
The number of RCs ranged from 1 to 15 (10.4 ± 3.6, mean ± SD) in the epithelium around mainly the third type neuromast (Figs. 1, 2, and 4). The distance of RCs from the neuromast ranged from 1.5 to 73.3 μm (27.9 ± 17.2, mean ± SD). In some instances, the RC was very close (1.5 μm) to the peripheral-most support cell of the neuromast (Fig. 6), whereas the most distant RC (Fig. 8) was observed over 70 μm from neuromast. Often, clusters of RCs occurred within close proximity of the neuromast (Figs. 4 and 7). The number of RCs in the epithelium far from neuromasts (more than 200 μm) was lower and ranged from 0 to 5; the mean density of RCs ± standard deviation was 1.1 ± 1.0 per 15,000 μm2 tissue area. Almost all the RCs found around the neuromasts were mature, measuring 11.5 ± 1.2 μm (mean ± SD) long and 7.8 ± 1.1 μm (mean ± SD) wide. At higher magnification (40× objective), RCs were easily differentiated from adjacent cell types (e.g., mucous cells) based on the thickened cortex and dark spots (rodlets) within the cytoplasm (Figs. 2 and 4). In contrast, the epidermal mucous cells near the neuromast are largely ovoid, measuring 8.9 ± 1.5 μm (mean ± SD) long and 8.5 ± 1.0 μm (mean ± SD) wide. Moreover, the cytoplasm is completely filled with numerous mucus vesicles up to 1.2 μm in diameter (Figs. 4 and 8) and the nucleus is pushed in the deeper zone of the cytoplasm (Fig. 8). Mucus vesicles, as seen by electron microscopy, are electron-lucent or moderately lucent (Fig. 8).
Ultrastructurally, the inner part of the RC plasma membrane made contact with the cell cortex, which ranged in thickness from 0.4 to 0.7 μm. The cortex appeared to be composed of thin microfilaments. Nuclei occupied the basal part of the cell and were round to ovoid with an irregular outline (Figs. 8 and 9). Euchromatin was scattered in the nucleoplasm with heterochromatin ringing the periphery (Figs. 8 and 9). Several round, elongate mitochondria were observed in the apex of the cell. Some RCs contained translucent vesicles within the cytoplasm (Figs. 7 and 8). Club-shaped rodlets were arranged so that the globular part was oriented toward the basal nucleus with the narrow part oriented toward an opening in the cytoplasmic border of the RC's apex (Figs. 7 and 9). Each rodlet possessed an electron-dense core surrounded by a fine granular substance. In some instances, the core extended the full length of the RC (Figs. 7 and 9). Often, the apical cortex of a mature RC that had reached the epithelial surface was interrupted by an opening with RC contents poking through (Fig. 9).
The olfactory organ of Danio rerio consists of several lamellae (Fig. 5a) that insert into a midline raphe, thus forming an oval-shaped rosette. Sensory and nonsensory regions are located separately on each lamella (Hansen and Zeiske, 1998). Based on light microscopy and the aforementioned RC morphology, lamellae were distinguishable from the other components of zebra fish olfactory epithelium (Fig. 5). Olfactory epithelium of D. rerio contained from 3 to 19 RCs (9.2 ± 6.0, mean ± SD) per 22,000 μm2 tissue area. These RCs were of the same size as those near the neuromasts. The head epithelium of two fish contained 2–3 RCs near the taste buds (not shown). RCs were absent in the eye, inner ear, and brain of D. rerio.
Very few available records on the presence of RCs in the olfactory epithelium of fishes were published (see review by Manera and Dezfuli, 2004). In this study, RCs were found in the olfactory epithelium of D. rerio in and near the taste buds of only two specimens. There were no RCs found in the inner ear, eye, or brain.
A literature review emphasizes that there are numerous published reports on the morphology and development of neuromasts of larval and adult zebrafish using light and electron microscopes (for references, see Webb and Shirey, 2003). However, these studies fail to provide adequate detailed information on the type of cells surrounding the neuromasts. This study is the first to document the occurrence of RCs near the neuromasts of zebra fish. The close proximity of these cells is the most interesting result of this study.
Rodlet cells are enigmatic cells exclusive to fish. After more than a century has passed since their discovery and documentation in the scientific literature, it is only recently that most investigators agree on the endogenous nature of RCs. Currently, the origin of these cells is the most poorly studied area. Additional research from the field of embryology is fundamental to advancing our understanding of RC. According to Mazon et al. (2007), RCs proliferate in the kidney and then migrate to the gills. While RC function has not been conclusively shown, a few recent experimental surveys have revealed the importance of these cells as biomarkers for environmental exposure and associated effects (Dezfuli et al., 2003b, 2006; Manera and Dezfuli, 2004; Giari et al., 2006). Rodlet cells appear to contribute to a fish's defense against pathogenic organisms (Leino, 1996; Dezfuli et al., 1998, 2000, 2003a; Mazon et al., 2007), representing an inflammatory cell closely related to other piscine inflammatory cells, such as mast cells (Reite, 2005; Reite and Evensen, 2006), epithelioid cells, and mesothelial cells (Dezfuli et al., 2000).
The view that RCs possess sensory function was expressed only by Wilson and Westerman (1967), although the authors did not provide any morphological evidence. Based on our current and previous investigations on RCs, we believe that RCs do not have any structural features indicative of cells belonging to a fish's sensory systems. Rodlet cells exhibit secretory activity (Leino, 1974, 1996). Moreover, they do not possess cilia. Thus, there is no connection between these cells and sensory neurons. More importantly, while RCs can be found in all regions of the fish body, occurrence of RCs around the neuromasts of D. rerio was unexpected. Thus, at present, we are only able to postulate the following hypothesis of their function at the neuromast location.
Neuromasts are superficial mechanosensory organs of fish involved in schooling, predator avoidance, prey capture, and vibration detection (Webb, 1989; Uchiyama et al., 1991; Gompel et al., 2001). According to a comparison between mast cells and rodlet cells of teleosts by Reite and Evensen (2006), the mast cells were defined as “standing force” in tissues consistently exposed to pathogens, while RCs were defined as “mobilization force” in tissues occasionally exposed to noxious agents. Indeed, exposure to heavy metals (Vickers, 1962; Hawkins, 1984; Giari et al., 2006) or thermal elevations (Iger and Abraham, 1997) induced an increase in the number of RCs in various target tissues. This suggests that RCs may have a function in stress physiology, allowing the quantity of RCs to be useful biomarkers (Smith et al., 1995; Dezfuli et al., 2003b). Moreover, RCs may represent a type of eosinophilic granulocyte that populates the tissues when immature, maturing in response to appropriate stimuli (Reite and Evensen, 2006). According to Mazon et al. (2007), the early appearance of RCs in the ontogeny of carp (Cyprinus carpio L.) combined with cell number regulation during stress and infection suggests that the RCs are key endogenous components of the fish defense system. In conclusion, it is reasonable to hypothesize that RCs are part of the piscine defense system, acting as “mobilization force.” Their occurrence around the neuromasts places RCs in a position to react quickly whenever the sensory system receives stress signals from the surrounding water.
The authors thank Dr. M. Manera from the University of Teramo, Teramo, Italy, for providing constructive comments and Dr. L.M. Duclos, Oxbow Pet Products, Murdock, Nebraska, for help with the English.
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