the epithelia lining the renal pelvis in the rat

J. Anat. (1974), 118, 3, pp. 561-569 561With 6 figuresPrinted in Great Britain

The epithelia lining the renal pelvis in the rat

M. R. KHORSHID* AND D. B. MOFFAT

Department of Anatomy, University College, Cardiff

(Accepted 1 July 1974)

INTRODUCTION

The shape and structure of the renal pelvis is a good deal more complicated than isgenerally realized, even in a unilobar kidney such as that of the rat (Fig. 1). Near thehilum, where it is surrounded by the connective tissue of the renal sinus, the pelvis islined with transitional epithelium continuous with that of the upper end of theureter. Deeper in, however, the epithelium is thinner: over the papilla (inner medulla)it is only one cell thick, while over the outer medulla it is one, or at the most, twocells thick. In this last situation only the thinnest of epithelial barriers separates thepelvic urine from the rich vascular plexuses of the medulla.

In addition, in many species, processes of outer medullary tissue, hitherto knownas secondary pyramids (Fig. 1), invaginate the pelvis, giving rise to secondaryfornices which lie between these processes and the main part of the outer medulla(Pfeiffer, 1968; Khorshid et al. 1969). These processes have the effect of greatlyincreasing the surface area of the pelvic lining. In fact, the appearance of the secon-dary pyramids in sections is misleading, since they are not papilla-like projections,but are flaps of outer medullary tissue which overlap each of the interlobar vessels,and their true form cannot be seen in sections, but only in dissections of the wholekidney (Cartwright, personal communication). On account of their form and the factthat they are composed of outer rather than inner medullary tissue, Cartwrightsuggested that they should be called opercula rather than pyramids and this terminologywill be used here. Even in those species, such as the dog, cat and rabbit, in which a pelvicseptum is present (Sheehan& Davis, 1959), an extension ofthe pelvic cavity passes deepto the septum to come into close and extensive contact with the outer medulla.The relationship between the pelvis and the kidney substance is of great practical

importance owing to the possibility of direct exchanges of water and solutes betweenthe pelvic urine and the renal tissue. Gertz, Schmidt-Nielsen & Pagel (1966), byperfusing the pelvis with fluids of different composition, were able to demonstratethe exchange of water, sodium and urea between the urine and the inner and outermedulla while, more recently, Schutz & Schnermann (1972) have collected urinedirectly from the collecting ducts of the papilla during perfusion of the pelvis withsolutions of different composition and osmolarity. It was found that changing theosmolarity of the perfusing fluid caused parallel changes in urine osmolarity.

Since the epithelia across which these exchanges take place had not previously beenstudied in detail, it was decided to investigate their structure in the rat by electron

* Present address: Department of Anatomy, Faculty of Medicine, Ain Shams University, Cairo,Egypt.

M. R. KHORSHID AND D. B. MOFFAT

Fig. 1. A transverse paraffin section through a rat kidney to show the position of the three typesof pelvic epithelium. Transitional epithelium (A) is present in relation to the renal sinus. A verythin epithelium (B) covers the outer medulla. A single layer of cells (C) covers the papilla. Anoperculum (0) of outer medullary tissue has a secondary fornix (F) lateral to it. x 9.

microscopy, after fixation by intravascular perfusion. During the preparation of thispaper, a short account of a similar investigation appeared in another journal(Silverblatt, 1974). Details of the epithelia which have been mentioned by the latterauthor will therefore only be described briefly in the present paper.

MATERIALS AND METHODS

Six Wistar rats were used for this study. They were anaesthetized with ether, theabdominal aorta cannulated just above its bifurcation and, after opening the leftrenal vein, the vascular system was perfused with 4% glutaraldehyde in cacodylatebuffer, the aorta being clamped above the level of the renal artery immediately afterthe beginning of the perfusion. After satisfactory perfusion, indicated by the imme-diate blanching of the kidney (Osvaldo & Latta, 1966), the pelvic wall was exposedby hemisecting the kidney in a coronal plane through the hilum and the papillawas removed. Small portions of the thick transitional epithelium and of the thin

562

Pelvic epithelium of the rat

Fig. 2. Superficial cells of the transitional epithelium. The cells contain characteristic fusiform(F) and spherical (S) vesicles. Bundles of filaments (B) are prominent and lysosomes (L) andmultivesicular bodies (M) are also present. The surface of the superficial cells shows festooning.x 12000.

epithelium which covers the outer medulla were taken for further fixation, as werepieces of the surface layer of the papilla. The specimens were post-fixed in osmiumtetroxide, embedded in Epon and the sections stained with uranyl acetate and leadcitrate. They were examined with an AEI EM 801 A.

RESULTS

The thick epithelium which lined the pelvis in the region of the renal sinus was atypical transitional epithelium and we agree with Silverblatt (1974) that it was closelysimilar to the epithelium of the ureter which has been described by Hicks (1965). Themost important features can be seen in Fig. 2, which shows the characteristicfestooned luminal surface bounded by a thick, asymmetrical unit membrane.Fusiform and spherical cytoplasmic vesicles, dense bundles of filaments, multi-vesicular bodies and lysosomes were also present and there were junctional complexesbetween the luminal borders of the cells. The intercellular spaces followed a tortuouscourse and the cell membranes which bounded them were mostly parallel and closetogether, although dilated irregular intercellular spaces were sometimes seen, par-ticularly near the basal lamina. No 'bundle cells' (Hicks, 1965) were seen but no

563


F

I

PC

V., L ,0Z,,

DVR

DVR

Fig. 3. The thin epithelium covering a vascular bundle of the outer medulla and separating it fromthe cavity of the pelvis (PC). One of the epithelial cells has a festooned surface (F) but the othersare relatively smooth. The bundle consists of ascending (AVR) and descending (DVR) vasa recta.x 3000 approx.

I

I

3

4

564

I..am

ffl


Cap4

Fig. 4. The single layer of epithelium which covers the papilla. The intercellular spaces (S) aresomewhat dilated. The papillary tissue contains a medullary interstitial cell (M) with a lipiddroplet and a fenestrated capillary (Cap.). x 18900.

special search was made for them (in the ureter they form only 01-0-5% of the totalcell population). Occasionally cells containing a small number of lipid droplets wereseen. The tissue lying deep to the epithelium was very vascular and the most super-ficial capillaries occupied bays in the deep surface of the transitional epithelium sothat they were separated from the lumen by only one or two cells.The thin epithelium which covered the outer medullary tissue and the opercula

(Fig. 1) was only one or, at the most, two cells thick. One of themost striking featuresof this epithelium is shown in Fig. 3, namely its very close relationship to the vascularbundles of the outer medulla; these lie directly beneath the epithelium, which thusalone separates the ascending and descending vasa recta and some descending limbs

36 ANA II8

565


f~~~( ' N ..S

4~~~~~~~~~~~~~41

Fig. 5. A junctional complex from the papillary epithelium. x 54000.

Fig. 6. The surface of a papillary epithelial cell to show the fuzz coat andasurfacevesicle(V). x 75000.

of the loops of Henle from the pelvic urine. The epithelial cells themselves mostlyhad a relatively flat luminal surface but there were many short blunt microviJli. Thesurface was covered with a fuzz coat. In places, however, the cells resembled thesuperficial cells of the transitional epithelium in having a festooned surface andfusiform and spherical vesicles in the cytoplasm, although the fusiform vesicleswere not seen as frequently as they were in relation to the festooned surface of truetransitional epithelium. Both types of cell are seen in Fig. 3. The cells with a flatsurface contained only the spherical vacuoles, which occurred frequently. Lysosomeswere occasionally seen but bundles of filaments were relatively uncommon. Scatteredsmall round or oval mitochondria were seen. The lateral borders of the cells were veryoblique so that the extensive overlapping of cells sometimes gave the false impressionthat two layers of cells were present. The intercellular spaces were usually closed butwere sometimes dilated. Near the lumen the cells were attached by junctionalcomplexes, in which all three components could sometimes be recognized; elsewherethere were scattered desmosomes. The bases of the cells were irregular and theirregularities were followed closely by the basal lamina, except where occasionalmicropinocytotic vesicles were present.The epithelium which covered the papilla consisted of a single layer of rather

regularly shaped cuboidal cells (Fig. 4). The lateral cell boundaries tended to bevertical, but some overlapping of cells took place here and there. The cells were heldtogether by junctional complexes at the luminal surface (Fig. 5) and by infre-quentdesmosomes elsewhere. The intercellular spaces were mostly widely dilated and

566

Pelvic epithelium of the ratirregular. The luminal surface showed scattered short microvilli and there was aprominent fuzz coat (Fig. 6). The cytoplasm contained relatively few mitochondria,but small vesicles were common, some of them opening on to the surface (Figs. 4, 6).Membrane-limited lysosome-like bodies were sometimes seen, as were basal micro-pinocytotic vesicles.

DISCUSSION

When the lateral walls of the pelvis were inspected, after having been exposed asdescribed above, the thick transitional epithelium, with its underlying muscle andconnective tissue, was seen to line the main part of the pelvis and to extend along eachof the interlobar vessels like the fingers of an outstretched hand. Between theseprolongations the bright red outer medullary tissue bulged inwards and overlappedeach of the interlobar vessels from either side to form the opercula, so that in orderto see the vessels the opercula had to be pulled apart. Occasionally only one largeoperculum was present on one side of an interlobar vessel, but typically there weretwo (Cartwright, personal communication).The structure and the functional significance of the transitional epithelium has

been described previously by Silverblatt (1974) and will not be further discussedhere, apart from the observation that it is, perhaps, fortunate that relatively im-permeable transitional epithelium separates the sometimes highly concentratedurine from the cortical tissue (which has a normal osmolarity) so that no interchangeof water or solute can occur in this region.

Silverblatt described the thin epithelium covering the outer medulla as beingtransitional in type. We cannot fully agree with this: although cells with a festoonedsurface and containing fusiform vesicles were often seen (Fig. 3), most of the cellswere not of this type and none of them showed all the features of true transitionalepithelium. The epithelium was typically only one cell thick and did not have thethick asymmetrical unit membrane of transitional epithelium; this, together withthe close relationship of the epithelium to the vascular bundles, and the presence ofdilated intercellular spaces, suggests that it is essentially an epithelium across whichtransport of water and solutes can take place. The papillary epithelium, too, appearsto be permeable, although its structure is not identical with that of the epitheliumcovering the outer medulla and, in particular, the majority of its intercellular spacesare widely dilated.According to Dixon & Gosling (1970) the papillary epithelium is transitional in

type, with fusiform vesicles and a festooned surface. These authors, however, onlyexamined the papilla in the region of the fornix (personal communication) so that it isnot surprising that cells of this description were encountered and Dixon and Goslingdo not disagree with our conclusion, and that of Silverblatt, that the epitheliimcovering the whole of the free part of the papilla is of a simple cubical type.From a functional point of view the epithelia which have been described above

must be of considerable importance. During the process of concentrating urine asteep osmotic gradient is built up in the inner medulla by means of a countercurrentmultiplier system operated by the loops of Henle. This effect is helped by counter-current exchanges between the vasa recta in the vascular bundles and by a recircula-tion of urea in the papilla. In the normal rat, even when it is allowed a normal supply

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568 M. R. KHORSHID AND D. B. MOFFAT

of drinking water, the urine osmolarity is in the region of 1000-1500 mOsm com-pared with a normal tissue osmolarity of about 300 mOsm.Thereisamarked osmoticgradient in the medulla, rising from the cortico-medullary junction to the tip of thepapilla where it approximates to that of the urine, so that there may well be verysteep gradients in osmolarity and concentration of solutes between pelvic urine andthe medullary tissue, particularly when a concentrated urine is being produced. Theexperiments of Gertz et al. (1966) and Schutz & Schnermann (1972) have shown thatdirect exchanges of sodium, water and urea between pelvic urine and renal tissue cantake place, and that such exchanges can influence the composition of the final urine.It is interesting that the concentrating ability of the kidney falls sharply when thepelvis is opened so that urine is no longer retained within the pelvis (Horster &Thurau, 1968).

Previous authors have maintained that such exchanges take place through theepithelium of the papilla, but it seems more likely that the outer medulla is the mainsite of exchange, although some direct exchange with the papilla cannot be excluded.The surface area exposed to the pelvic urine is greater over the outer medulla,particularly in those species which have secondary fornices, and the very closerelationship between the medullary vascular bundles and the pelvic urine mustsurely be significant. We therefore suggest that the medullary osmotic gradient,induced by the counter current system in the loops of Henle, is augmented by a recir-culation of sodium and urea from urine to papillary tissue via the descending vasarecta and perhaps by the osmotic absorption of water from the urine by the medullaryinterstitial tissue and the vascular bundles, these exchanges taking place through thethin epithelium which covers the outer medulla. The presence of dilated intercellularspaces in the epithelium that covers both outer and inner medulla suggests thattrans-epithelial transport of water and/or solute is taking place and further evidencethat such exchanges are likely will be the subject of a further report.

SUMMARY

The epithelia which line the renal pelvis have been examined in 6 rats. A normaltransitional epithelium lines the pelvis near the renal hilum. A thin epithelium whichis one or, at most, two cells thick, covers the outer medullary tissue, and alone sepa-rates its vascular bundles from the pelvic urine. A single layer of cuboidal cellscovers the papilla. It is inferred that exchanges of water and solute occur across thetwo thin types of epithelium, and that the vascular bundles play an important partin such exchanges.

We are happy to thank Miss Lynda Jenkins for skilled technical assistance. Thiswork was supported by grants from the World Health Organisation and the Well-come Trust to M. R. K. The latter has pleasure in expressing his thanks to ProfessorJ. D. Lever for allowing him to use the research facilities of the Department ofAnatomy.


REFERENCES

DIXON, J. S. & GOSLING, J. A. (1970). Electron microscopic observations on the renal caliceal wall inthe rat. Zeitschrift fur Zellforschung und mikroskopische Anatomie 103, 328-340.

GERTZ, K.-H., SCHMIDT-NIELSEN, B. & PAGEL, D. (1966). Exchange of water, urea and salt between themammalian renal papilla and the surrounding urine. Federation Proceedings 25, 327.

HICKS, R. M. (1965). The fine structure of the transitional epithelium of rat ureter. Journal of CellBiology 26, 25-48.

HORSTER, M .& THURAU, K. C. W. (1968). Micropuncture studies on the filtration rate of single super-ficial and juxtamedullary glomeruli in the rat kidney. Pflugers Archiv fur die gesamte Physiologie desMenschen und der Tiere 301, 162-181.

KHORSHID, M. R., SABBOUR, M. S., SALEH, A.-L., MAHRAN, Z. & EL-MAHALLAWI, M. N. (1969). A com-parative structural study of the kidney in different mammals with particular reference to desert rodents.Proceedings of the Egyptian Academy of Sciences 22, 69-75.

OSVALDO, L. & LATTA, H. (1966). The thin limbs of the loop of Henle. Journal of UltrastructureResearch, 15, 144-168.

PFEIFFER, E. W. (1968). Comparative anatomical observations of the mammalian renai pelvis and medulla.Journal ofAnatomy 102, 321-331.

SCHUTZ, W. & SCHNERMANN, J. (1972). Pelvic urine composition as a determinant of inner medullarysolute concentration and urine osmolarity. Pfliigers Archiv fur die gesamte Physiologie des Menschenund der Tiere 334, 154-166.

SHEEHAN, H. L. & DAVIS, J. C. (1959). Anatomy of the pelvis in the rabbit kidney. Journal of Anatomy93, 499-502.

SILVERBLATT, F. J. (1974). Ultrastructure of the renal pelvic epithelium of the rat. Kidney International5. 214-220

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