Morphology Of Branchial Ionocytes Biology Essay

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Aristotle noted in his work Historia Animalia that the fish gill was indeed a special organ. However, it was not until the pioneering work of Homer Smith in the 1930's that an ionoregulatory function could be ascribe to the gills (see Evans DH 2000 and Hwang PP 2000). Since Keys and Willmer's identification in 1932 of presumptive chloride secreting cells with their greater affinity for eosin, ovoid shape and granular cytoplasm much effort has been put into the study of branchial ionocytes. Branchial ionocytes are found in all taxa of fish from the osmoconforming hagfish to the air-breathing lungfish and all manner of fish in between. Light and electron microscopic descriptions have been complemented by enzyme and immunohistochemistry to characterize the expression of ion transport proteins that make these cells ionocytes (see Evans DH 2000 and Hwang PP 2000). Two cell types potentially function as ionocytes in the fish gill, the pavement cell (PVC) and mitochondrion-rich cell (MRC) and their morphological attributes are the subject of this chapter. Functional consideration of these cell types in ion and acid-base regulation are detailed in contributions by Evans DH and Hwang PP.

<Figure 1>

Pavement cells (PVCs) are the squamous to cuboidal cells that cover much of the gill (>90% of the surface area; Figure 1A,B; see Olson K). The apical surface of PVCs is usually large and polygonal and may be smooth or have microvilli (finger like projections) or microridges which typically form concentric rings (referred to microplicae when viewed in cross section). A double ridge generally marks the boarder of neighboring PVCs. The types of apical features present show variation between species and also within and between the different gill epithelia (lamellar versus filament). Pavement cells typically have low mitochondrial densities and unelaborated basolateral membranes (Figure 2A). The nucleus in squamous pavement cells is compressed while in cuboidal pavement cells it is rounded. Pavement cells have the typical intracellular organelles, rough and smooth endoplasmic reticulum, Golgi apparatus, lysosomes, and vesicles with contents of various electron densities. In the non-teleost fishes, pavement cells display abundant mucous secretory granules in the apical cytoplasm (Figure 3). Pavement cells are joined by desmosomes and the peripheral cytoplasm contains microfilaments. The tight junctions associated with pavement cells have multiple strands and are not characterized as leaky, minimizing paracellular fluxes of ions. In the hagfish and lamprey, communicating gap junctions have been found between neighboring pavement cells, and pavement cells and undifferentiated cells, however not with MRCs. The presence of communicating gap junctions is significant because they allow the electrochemical coupling of the cells of the epithelium which is important in co-ordinating cell growth, differentiation and function. No studies have been undertaken in other fishes to specifically determine the presence of gap junctions.

PVCs have been shown to be involved in the covering and uncovering of MRCs during acid-base and ionoregulatory disturbances, but the role of the PVC in the process is somewhat secondary to that of the MRC in the functional response. Generally PVCs themselves have been shown to be morphologically unresponsive to changes in environmental conditions. However, part of the problem stems from the fact that the MRCs are generally the focus of attention in morphological studies and the changes in PVCs may be overlooked. It also might be difficult to recognize these changes if they only occur in a subpopulation of PVCs since there are proportionally many more PVCs (90% of epithelial cells). With that said, there have been a few studies that have shown that PVCs increase apical surface area (densities of microvilli and microplicae) in response to hypercapnia and alkaline exposure which induce acid-base disturbances. It has also been found that there are studded subapical vesicles that resemble the proton pump containing vesicles from other animals. These morphological characteristics of PVCs help to support the hypothesis that they are the site of proton pump driven sodium uptake at least in some species (see Hwang PP 2000). Perhaps more attention focused on these cells will reveal more adaptational changes of this somewhat underrated cell type.

MITOCHONDRION-RICH CELLS (MRCs) OR CHLORIDE CELLS (CCs)

The descriptive morphological study of the gill has been dominated by the mitochondrion-rich chloride cell and its subtypes (see Evans DH 2000 and Hwang PP 2000 and additional reading list). In general, the numerous mitochondria in these cells are thought to supply the ATP for ion transport proteins to drive the vectorial transport of ions as part of ion and acid-base regulation (see Goss GG).

<Figure 2>

MRCs tend to be concentrated in the afferent region of the filament epithelium and have an intimate association with the arteriovenous circulation, notably the central venous sinus, although in the interlamellar region MRCs also are associated with the basal channels of the lamellar arterioarterial circulation (see Olson K 2000). The defining morphological feature of this cell type is a high mitochondrial density. However, MRCs also generally have an amplification of their basolateral membrane either through folding forming a basal labyrinth or the presence of a tubular system (Figure 2,4,5,7), although basolateral amplification can be less developed as in lamprey intercalated cell (IC)-type MRCs (Figure 6) and lacking in mitochondrion-rich pavement cells. Associated with the basolateral membrane amplification is the important ionoregulatory enzyme Na+/K+-ATPase (see Goss GG 2000). The presence of Na+/K+-ATPase has been observed by freeze-fracture electron microscopy as dense studding of the tubular elements (Figure 2D). In the apical region of MRCs is a collection of tubules and vesicles (tubulovesicular system) which is distinct from the tubular system (Figure 3). The apical membrane can be quite variable in appearance ranging from concave to convex, sometimes forming deep crypts. In addition, the surface topography has been shown to be smooth, or having microvilli of varying densities and lengths as well as highly branched, to give a sponge-like appearance (Figure 1D,2A,3-7). The use of morphological features has led to the classification of different types of MRCs.

<Figure 3>

The term "chloride cell" relates to the function of the MRC in Cl- elimination. In seawater teleosts, the MRCs have quite convincingly been shown to be sites of active Cl- elimination and hence the name is fitting (see Evans DH 2000). In the agnathans, chondrichthyans, chondrosteans, holosteans, and freshwater teleosts, the evidence the MRCs are involved in Cl- fluxes is limited to the few teleosts and elasmobranchs. So in order to avoid any confusion on the matter we will only use the term chloride cell when referring to the seawater teleost MRC unless otherwise noted.

The teleost MRC is characterized by its elaborate intracellular system of branching tubules that is continuous with the basolateral membrane (tubular system; Figure 2A-D). This network of anastomosing tubules is closely associated with the mitochondria and is only excluded from the area of the Golgi apparatus and the band immediately beneath the apical membrane. The elements of the tubular system can be found alongside the endoplasmic reticulum making identification somewhat problematic. Extracellular space markers such as horseradish peroxidase and ruthenium red have been used to clearly establish the basolateral continuity of the tubular system and its separation from the ER. The Karnovsky potassium ferrocyanide reduced osmium stain has also been used to unambiguously differentiate the membrane elements of the tubular system from the ER without the need of extracellular markers. The selective heavy staining of the tubular system contrasted markedly with the poorly stained endoplasmic reticulum (Figure 2A,B). Environment ionic conditions have a marked effect on the morphology of the teleost MRCs, which of course relates to the role of these cells in active ion transport (see Evans DH 2000). In seawater, the gill is involved in active ion elimination while in freshwater active ion uptake takes place.

The mitochondrion-rich chloride cell (CC) and accessory cell (AC) are two types of MRC that are universally expressed in seawater teleosts (Figure 1D-F). These cells form multicellular complexes in the filament epithelium. The larger chloride cell may be elongate, ovoid or cuboidal in shape, which depends upon the species. The tubular and the tubulovesicular systems are highly developed and the cell is packed with mitochondria. High densities of Na+/K+-ATPase is associated with the CC tubular system. The apical membrane of a CC is recessed from the surface of neighboring PVCs and may be further deepened through invagination (Figure 1B-D). The smaller accessory cell is superficially located, semi-lunar or pear shaped and generally has a less extensive tubular system and a poorly developed tubulovesicular system. Notably, they have low levels of Na+,K+-ATPase unlike the CCs. The AC sends cytoplasmic processes into the larger CC which emerge at the apical surface to form a complex mosaic. Notably, the tight junctions found between CC and AC contain fewer strands than do tight junctions formed with PVCs. Therefore, the AC interdigitations within the CC apical membrane would greatly increase the linear distance of leaky tight junction which is functionally important for the paracellular sodium efflux. There is also ample evidence that Cl- efflux occurs transcellularly through the CC (see Goss GG 2000 and Evans DH 2000).

In freshwater teleost fishes there is less consensus about clear MRC subtypes which might relate to the instability and variability of the freshwater environment itself. Pisam and co-workers, however, have described α and β sub-types

of MRCs with electron lucent (light or pale) and electron dense (dark) cytoplasms, respectively, in a number of species. It should be noted that this naming system is unrelated to that used to describe acid and base secreting cells in other epithelia (kidney collecting duct, bladder). In addition to a pale cytoplasm, a cells were found at the edges of the interlamellar space (ILS) in contact with the basal lamina opposite the arterioarterial circulation. The b cells, on the other hand were generally observed in the ILS in contact with basal lamina associated with the arteriovenous circulation. Also a manganese-lead (Mn-Pb) stain was found that selectively stained the contents of a population of variably sized membrane bound bodies in the apical cytoplasm of only the b-cell type. The material in the apical vesicles of the b-cell has been shown to include carbohydrate material and binding of the lectin WGA (wheat germ agglutinin: sialic acid and N-acetylglucosaminyl residues) to the apical vesicles of a subpopulation of MRCs has also been found in tilapia (presumably b-cells). In the guppy (L. reticulatus), it was shown that the a-cell has high levels of Na+,K+-ATPase immunoreactivity while the b-cell has only weak labeling. In a study on rainbow trout (O. mykiss), and an earlier study on Atlantic salmon, differentiation of these two subtypes was not made.

Transfer to seawater of euryhaline freshwater fishes, results in the degeneration of the α -cell through apoptosis and hypertrophy of the β -cell. The β -cell is transformed into what is recognized as the seawater chloride cell (CC). The transformation consisted of an increase in the size of the β -cell, density of the cytoplasm, number of mitochondria, the tubular system network with a tighter polygonal mesh size, and the apical tubulovesicular system. A mitochondrion-poor cell type has been described that possesses a well-developed tubular system but has relatively few mitochondria. This cell increases in frequency following seawater acclimation and infrequently contacts the water. No function was suggested for this cell type.

Although typically associated with marine fishes the accessory cell type has also been described in some freshwater euryhaline species. These cells are associated with the a-cell type in tilapia and Atlantic salmon but b-cell type in brown trout (Salmo trutta) and are similar to the AC described in the seawater fish gill, but they are less common and do not send cytoplasmic processes into the apical cytoplasm of the CC. Upon transfer to seawater or in anticipation of transfer (smolting), their numbers increase and interdigitations are present. The AC are presumably present in fishes living in freshwater in order to facilitate the rapid switch to NaCl elimination. In the tilapia (Alcolapia grahami) of extremely alkaline (pH 10) brackish water Lake Magadi in Kenya, seawater ACs associated with larger CC type MRCs have also been found. The lake water has very high HCO3- and CO32- concentrations of 40 and 265 mEq·l-1, respectively with Na+ and Cl- at 342 and 108 mEq·l-1, respectively. In the proposed model, the CC-AC complex facilitates paracellular Na+ efflux via the leaky tight junction while HCO3- is pumped out by the CC.

In freshwater tilapia (O. mossambicus), three MRC types according to the apical membrane appearance by SEM and categorised them as either wavy-convex, shallow-basin, or deep-hole. The "wavy-convex" type has a convex apically exposed area with variable ornamentation with microvilli and a relatively large two-dimensional area. The surface of the "shallow-basin" type MRCs are flat but recessed below neighboring PVCs. The density of the "wavy-convex" type MRCs increases in low NaCl and the "shallow-basin" type MRCs increase in low Ca2+ water suggesting roles in Na+,Cl- and Ca2+ uptake, respectively. Results which have been corroborated by IHC (see Hwang PP 2000). The "deep-hole" MRCs are also recessed between PVCs like the "shallow-basin" type but they form a deeper apical crypt characteristic of seawater CCs. In the fathead minnow (Pimephales promelas), the "deep-hole" MRCs are associated with exposure to acid conditions suggesting a role in acid excretion. However, in other species, like the rainbow trout, this system of classification is not applicable, and an alternative system using lectin histochemistry has arisen using PNA (peanut agglutinin; terminal b-galactose residues) +/- staining to identify functionally different MRC subtypes in trout (see Goss GG 2000). Lectins bind to specific glycoproteins and differential staining patterns have been used to identify subtypes with concanvalin A (Con-A; a-mannopyranosyl and a-glucopyranosyl glycoprotein residues), and wheat germ agglutinin (WGA; N-acetylglucosamine and N-acetylneuraminic acid (sialic acid) residues) as well.

Although MRCs tend not to be as frequently found in the lamellae as in the filament epithelium in freshwater and especially seawater fishes, acclimation of trout to ion poor (< 0.01 mM [Na+]) conditions, elicits a massive proliferation of MRCs in the lamellar epithelium (see ). The number and area of exposed surface of these cells both increase dramatically. The effects of ion poor water on MRC proliferation can also be reproduced using hormone treatments with cortisol and growth hormone (see McCormick SD). Since MRC are generally quite large, proliferation on the lamellae results in the thickening of the epithelium and consequently, the blood to water diffusion distance is increased. This has negative consequences for gas exchange as blood PO2 and hypoxia tolerance are reduced in fish with lamellar MRC proliferation. It should be noted, however, that ion poor conditions are not always associated with the such massive numbers of lamellar MRC as is evident in the neon tetra (Paracheirodon innesi) which is native to the ion poor waters of the Amazon.

In the other Osteichthyans, which includes the Chondrosteans (e.g. sturgeon and paddlefish), Holosteans (e.g. Amia, and gars), Dipnoans (lungfishes) and Coelacanth, MRC have all been described (see Figure 3). However, in marine or euryhaline forms evidence for AC-CC complexes is still lacking.

<Figure 4>

The chondrichthyan (elasmobranchs and chimaeras) the salt secreting rectal gland replaces the gill as the dominate salt secretory organ, and yet branchial MRCs are still present in the gills in significant numbers. However, the important ionoregulatory enzymes Na+/K+-ATPase and H+-ATPase are associated with distinct subpopulations of these cells and have been implicated in acid-base regulation rather than NaCl secretion (see Evans DH 2000). Branchial MRCs are generally found singly in the filament epithelium and are cuboidal or ovoid in shape with a basally located nucleus (Figure 4). In addition to their high mitochondrial densities, they have a basolateral membrane amplified through heavy folding into basal labyrinth, and a densely packed sub-apical tubulovesicular system. The tight junctions between MRCs and neighboring PVCs consist of many strands and are not considered leaky. The apical surfaces of elasmobranch MRCs range from being deeply invaginated to convex and are covered by microvilli of varying densities.

<Figure 5>

The agnathans or jawless fishes represent the most primitive group of fishes consisting of the osmoconforming marine hagfishes and the osmoregulating lampreys. These differences in osmoregulatory abilities are reflected in the differences in MRC morphology in the agnathans. In freshwater lamprey three different types of MRC have been described, one of which is associated with the preadaptation to seawater and is the dominant type found in the seawater adapted lamprey. The seawater type is commonly referred to as the chloride cell due to its morphological similarities with the teleost chloride cell (Figure 5). In seaward migrating freshwater lamprey, the seawater-type MRCs are found in a continuous row along the length of the interlamellar space of the filament epithelium. The swMRCs are disk shaped and covered over by neighboring PVCs with the apically exposed surface containing microvilli. Following acclimation to seawater, the overlying PVCs retract and the apical surface increases to extend the full width of the interlamellar space. The surface bulges slightly, and is relatively smooth with few microvilli. The number of strands in the tight junction between neighboring swMRCs also decreases following seawater transfer. The shallow tight junction is an important morphological characteristic that gives a good indication of the cell's function, namely NaCl elimination.

<Figure 6>

In the lamprey, the freshwater MRC types are referred to as intercalated MRCs and one of the noticeable differences to the swMRC is the lack of a tubular system (Figure 6). One type is only present in the larval ammocoete and is characterized by electron dense mitochondria, small secretory mucus granules, short microvilli and/or microplicae and the presence of globular particles in its apical membrane (as shown by freeze fracture). They are found in both the lamellar and filament epithelia, and comprises approximately 60% of the total epithelium. The function of this ammocoete MRC type is not known, but it does not appear to be involved in ion regulation and disappears following metamorphosis. The second IC type is generally found singly or in pairs in the interlamellar region and at the base of the lamellae, where it intercalates with neighboring pavement cells and/or other MRC types. It is characterized by an apical membrane with elaborate microplicae, the absence of secretory mucous granules, the presence of numerous small vesicles and membranous tubules and the presence of rod-shaped particles in either the apical or lateral membranes (as determined by freeze fracture electron microscopy). These rod-shaped particles are similar to those described in the mitochondria-rich intercalated cells of other acid secreting epithelia. The plasma membrane domains having dense rod-shaped particle aggregates also show strong immunoreactivity for the proton pump (vacuolar type H+-ATPase) which has been demonstrated by immunohistochemistry. When the proton pumps are in the apical location these cells function in acid excretion while in cells in which the particles have a basal lateral location, the function is for base excretion.

<Figure 7>

In the hagfish, MRCs are restricted to the lateral wall of gill pouches and the lateral half of gill folds. All MRCs occur singly being separated by PVCs and lack leaky tight junctions. The hagfish MRC have abundant, large mitochondria and a tubular system continuous with the basolateral membrane along with a subapical vesiculotubular system (Figure 7). These cells also have perinuclear glycogen and high levels of carbonic anhydase, H+-ATPase, and Na+/K+-ATPase expression. Since hagfish are osmoconformers and therefore lack active NaCl regulation, their presence is linked to acid-base regulation. Communicating gap junctions are not found between hagfish MRCs and its neighbors (PVCs, non-differentiated cells). Their apical membrane contains microvilli and is usually convex and deep apical crypts are not common. Freeze-fracture electron microscopy has shown the presence of rod-shaped particles in the apical membrane which represent proton pumps as confirmed by IHC.

MCR identification

In addition to direct morphological analysis, MRCs have been identified by their affinity for eosin, and acid Fuschin stain, associated with abundant mitochondria and Champy-Maillet solution (ZnI-OsO4) which reacts specifically with membrane and thus the reaction with the abundant membrane systems of the MRC results in its selective blackening. Additional techniques are directed at the detection of the abundant mitochondria which results in a stronger signal than background. The mitochondrial vital stains DASPMI (dimethylaminostyrylmethylpyridiniumiodide), DASPEI (dimethylaminostyrylethylpyridiniumiodide) and Mitotrackerâ„¢ (Molecular Probes) as well as immunohistochemical techniques directed against mitochondria specific proteins have been used to this end.

Another approach has been to target the enzyme Na+/K+-ATPase, which has been shown to be expressed in high concentrations in MRCs. Ouabain specifically binds and inhibits the Na+/K+-ATPase and both 3[H] ouabain autoradiography and anthroylouabain fluorescence have been found to localise to MRCs. Enzyme histochemical and immunohistochemical methods have been used in the past to localize Na+/K+-ATPase to MRCs. The use of antibodies directed against the Na+/K+-ATPase have proven very useful as is evident in the large number of studies published recently using this approach (Figure 1F). Practically all of these studies make use of either the mouse monoclonal or rabbit polyclonal antibodies directed against conserved epitopes or regions of the Na+/K+-ATPase a subunit. The further study of MRC functional subtypes through the use of multiple immunohistochemical labelling with additional ion transporters is addressed in the contributions by Hwang PP and Evans DH.

Further Reading

Bartels, H. and Potter., C. 2004. Cellular composition and ultrastrucutre of the gill epithelium of larval and adult lampreys. Implications for osmoregulation in fresh and seawater. Journal of Experimental. Biology 207, 3447-3462.

Evans, D. H., Piermarini, P. M. and Choe, K. P. 2005. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation and excretion of nitrogenous waste. Physiological Reviews 85, 97-177.

Keys A and Willmer EN. 1932. "Chloride secreting cells" in the gills of fishes, with special reference to the common eel. Journal of Physiology 76: 368-378.

Laurent P: 1984. Gill internal morphology. In Hoar W, Randall DJ (eds): Fish Physiology. Academic Press, New York, p. 73.

Perry SF 1997. The Chloride Cell: Structure and function in the gills of freshwater fishes. Ann Review of Physiology 59:325-347.

Pisam M and Rambourg A. 1991.Mitochondria-rich cells in the gill epithelium of teleost fishes: An ultrastructural approach. International Review of Cytology 130: 191-232.

Wilson, J. M. and Laurent, P. 2002. Fish gill morphology: inside out. Journal of Experimental. Zoology 293, 192-213.

Figure Legend

FIGURE 1. Characterization of chloride cell (CC) and accessory cell (AC) apical crypts in marine teleost fishes. (A,B) SEM images of a seahorse (Hippocampus kuda) gill filament lamellae. Note that the surface of the lamellae is pitted with CC apical crypts. (C) A thick (0.5 μm) section stained with toluidine blue of afferent edge lamellae showing CC apical crypt (arrows) corresponding to pitting. (D) TEM sections through the apical crypt showing clear evidence of sharing by more than one cell (CC and AC) as is evident from the appearance of multiple shallow tight junction complexes (arrows) in contrast to the CC-PVC junctions (arrowheads). (E) Schematic illustrating the relative locations of the ion transport proteins involved in NaCl excretion. (F) Representative IHC staining of CC (Na+/K+-ATPase Ab α5, green) -AC (NHE2 Ab 597 red) complex in seawater adapted tilapia (Oreochromis mossambicus). Scale bars (A) 50, (B) 10, (C) 25, (D) 1μm (J.M. Wilson, unpublished data)

FIGURE 2 (A,B) TEMs of the MRC of the freshwater chum salmon larvae (Oncorrhynchus keta) using the potassium ferrocyanide-reduced osmium stain that preferentially stains the tubular system (ts) and the plasma membrane while other membrane systems remain weakly stained. (C) TEM showing the connections of the tubular system with the basolateral membrane (indicated by arrows) in the neon tetra (Paracheirodon innesi) MRC using conventional heavy metal staining. (D) Freeze fracture replicas of the seawater mullet MRC showing studded appearance of the tubular elements. Scale bars: (A) 1 μm; (B,C) 0.5 μm

(A,B,C) Adapted with permission from Figure 8 in Wilson, J.M. and Laurent, P. (2002). FISH GILL MORPHOLOGY: INSIDE OUT. Journal of Experimental Zoology 293:192-213. Wilmington, Wiley-Liss.

(D) Adapted with permission from Figure 4 in Sardet C (1980) FREEZE FRACTURE OF THE GILL EPITHELIUM OF EURYHALINE TELEOST FISH. American Journal of Physiology (Regulatory, Integrative and Comparative Physiology) 238: R207-R212. Bethesda, American Physiological Society.

FIGURE 3 TEMs of the apical regions of the MRCs of (A) Raja erinacei, (B) Acipenser beari, (C) Perca fluviatilis, and (D) Protopterus annectens showing the tubulovesicular system. Scale bars 1 μm.

Reproduced with permission from Figure 9 in Wilson, J.M. and Laurent, P. (2002). FISH GILL MORPHOLOGY: INSIDE OUT. Journal of Experimental Zoology 293: 192-213. Wilmington, Wiley-Liss..

FIGURE 4. TEM micrograph montage of the interlamellar region of the primary filament from the gill of a dogfish Squalus acanthias. Note the mitochondria-rich (MR) cells identified by their ovoid shape, numerous mitochondria, dense subapical tubulovesicular system (TVS) and extensive basal labyrinth (BL). The apical surface is covered with microvilli. Scale bar 5 μm.

Adapted with permission from Figure 1 in Wilson, J.M., Morgan, J.D., and Randall, D.J. (2002). Role of mitochondria-rich cells in the gills of an elasmobranch fish Squalus acanthias. Comparative Biochemistry and Physiology A: Molecular and integrative physiology 132(2):365-374. Amsterdam: Elsevier

FIGURE 5. Chloride cells in the gill epithelium of an adult Geotria australis in seawater. (A) SEM view of the filament epithelium afferent side. Arrows indicate the boarders of CC in a row extending beyond the interlamellar space. (B) Cross section of the filament, showing a row of chloride cells on each side of the central blood space. (C) Freeze fracture of a bundle of parallel membranous tubules, showing the helicoidally arranged particles (arrowheads). (D) Clusters of particles on the E face. Scale bars (A) 25, (B) 5 and (C) 0.1·µm.

Adapted with permission from Figure 7 in Bartels H and Potter I.C. (2004). CELLULAR COMPOSITION AND ULTRASTRUCTURE OF THE GILL EPITHELIUM OF LARVAL AND ADULT LAMPREYS. IMPLICATIONS FOR OSMOREGULATION IN FRESH AND SEAWATER. Journal of Experimental Biology 207, 3447-3462. Cambridge, Company of Biologists.

Adapted with permission from Figure 5 in Bartels, H., Moldenhauer, A. and Potter, I. C. (1996). CHANGES IN THE APICAL SURFACE OF CHLORIDE CELLS FOLLOWING ACCLIMATION OF LAMPREYS TO SEAWATER. American Journal of Physiology 270, R125-R133. Bethesda, American Physiological Society.

FIGURE 6 MRCs in the lamprey Geotria australis gill epithelium. (A) Intercalated MRC between two pavement cells in the gill epithelium of a downstream migrant (young adult). The apical surface is enlarged by slender microplicae and the apical cytoplasm contains large numbers of membranous tubules and vesicles. (B) Scanning electron micrograph of an intercalated MRC surrounded by ammocoete MRCs in the gill epithelium of a larva. (C) Gill epithelium in the interlamellar region of the filament and at the bases of the lamellae, showing Intercalated MRCs (arrows) intercalated between ammocoete MRCs (arrowheads) in ammocoetes maintained in ion poor water. Scale bars (A,B) 2·µm, (C) 5 μm.

(A,B) Adapted with permission from Figure 2 and 3 in Bartels H and Potter I.C. (2004). CELLULAR COMPOSITION AND ULTRASTRUCTURE OF THE GILL EPITHELIUM OF LARVAL AND ADULT LAMPREYS. IMPLICATIONS FOR OSMOREGULATION IN FRESH AND SEAWATER. Journal of Experimental Biology 207, 3447-3462. Cambridge, Company of Biologists.

(C) Adapted with permission from Figure 1 in Bartels H, Schmiedl A, Rosenbruch J, and Potter I.C. (2009). EXPOSURE OF THE GILL EPITHELIAL CELLS OF LARVAL LAMPREYS TO AN ION-DEFICIENT ENVIRONMENT: A STEREOLOGICAL STUDY. Journal of Electron Microscopy 58(4):253-260. Tokyo, Oxford University Press.

FIGURE 7 Epithelium covering a gill lamella of the Atlantic hagfish Myxine glutinosa. The following cell types can be distinguished: pavement cells (PC), mitochondrion-rich cells (asterisks), basal cells (BC), small granule cells (indicated by open arrowheads), and granulocytes (G). The arrow points to the microvilli-bordered apical surface of a MRC. Mag x 2000

Reproduced with permission from Figure 1 in Bartels H (1984) ORTHOGONAL ARRAYS OF PARTICLES IN THE GILL EPITHELIUM OF THE ATLANTIC HAGFISH, MYXINE GLUTINOSA. Cell and Tissue Research 238:657-659. Heidelberg, Springer-Verlag.

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