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The presence of proximal tubulelike cells in the kidney parietal epithelium in response to unilateral nephrectomy.

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T H E ANATOMICAL RECORD 200:61-65 (1981)
The Presence of Proximal Tubulelike Cells in the
Kidney Parietal Epithelium in Response to
Unilateral Nephrectomy
Department of Anatomy, Georgetown University, School of Medicine,
Washington, D.C. 20007
Five months following unilateral nephrectomy, the parietal epithelia in the remaining kidneys of Sprague-Dawley rats were examined by light
and electron microscopy. Compared with controls, the kidneys from uninephrectomized rats exhibited a dramatic increase in mass characteristic of compensatory hypertrophy. Approximately 20% of the renal corpuscles in the hypertrophied kidneys had parietal epithelia lined by tall cells which possessed a brush
border and other morphological characteristics of proximal tubule cells. In some
instances proximal tubulelike cells made up over half of the cells lining the parietal epithelium. The possible significance of this finding is discussed.
In response to unilateral nephrectomy, the
remaining kidney undergoes a series of adaptive changes which result in a dramatic increase in its mass and functional capacity
(Malt, 1969). In rats older than 2 months, the
compensatory hypertrophic growth of kidneys
appears to result from hypertrophy of existing
nephrons rather than from an increase in the
number of nephrons (Bonvalent et al., 1972).
Investigations have indicated that this growth
involves some hyperplasia but mainly hypertrophy (Malt, 1969).
In this brief report, an additional morphological change in the parietal epithelium is noted
in the compensatory hypertrophied kidneys of
rats. This change involves the presence of variable numbers of tall columnar cells which possess a brush border and other morphological
characteristics of proximal tubule cells. I t is
suggested that the presence of these cells may
represent an attempt by the nephron to increase its functional capacity in response to an
increased work load resulting from contralateral nephrectomy.
and control rats were fixed in situ by intravascular perfusion of phosphate-buffered 2% glutaraldehyde (pH 7.2; 410 mOsM).
Preparation of samples for light and electron
microscopic observation
For scanning electron microscopy, glutaraldehyde-fixed samples were dehydrated
through graded acetones, dried by the criticalpoint method (Anderson, 1951), mounted on
stubs, and coated with a thin layer of palladium-gold in a sputter coater. The samples
were then examined in an ETEC Autoscan
operating at 20 kV.
For light and transmission electron microscopy, glutaraldehyde-fixed samples were
rinsed in buffer and postfixed in phosphatebuffered 1%osmium tetroxide. The samples
were stained en bloc in 2% aqueous uranyl acetate for 3 hours, dehydrated through graded
acetones, and embedded in a mixture of Epon
and Araldite resins. Thick sections (1-2 pm)
were stained with toluidine blue and examined
using a Zeiss light microscope model RA38
equipped with a 35-mm camera. Thin sections
(50-80 nm) poststained with uranyl acetate
A unilateral nephrectomy was performed on and lead citrate (Reynolds, 1963) were exthree Sprague-Dawley male rats weighing be- amined using an AEI EM 801 operating a t 60
tween 230 and 250 grams. A sham operation kV.
was conducted on three control rats. After 5
Received September 4, 1980; accepted October 6. 1980.
months, the kidneys of the nephrectomized
0003-276)(181/2001-0061$02.000 1981 ALAN R. LISS, INC.
these cells sometimes comprise over half of the
parietal epithelium and exhibit irregular patUpon visual examination, the kidneys from terns of distribution, it seems likely that this
the uninephrectomized rats appeared approxi- alteration involves a transformation of parietal
mately two times larger than those from sham- epithelial cells rather than an expansion of the
operated controls. A light and electron micro- initial segment of the proximal tubule to acscopic survey indicated a significant alteration comodate a hypertrophied glomerulus. Whethof the parietal epithelium in the kidneys from er or not such a transformation might also inall three nephrectomized rats. This alteration volve the mitotic division of parietal cells is not
involved the presence of tall cells which have known.
the morphological characteristics of proximal
When found in man, the significance of this
tubule cells (Figs. 1, 2 , 3 , 4 ) .These characteristransformation is often difficult to rationalize
tics include a dense microvillous brush border,
(Ward, 1970). During compensatory hypertroapical invaginations and apical vesicles of va- phy, however, the kidney undergoes a number
rying size, extensive infoldings of the plasmaof morphological transformations which are
lemma, and numerous rod-shaped mitochondesigned to increase its work-load capacity
dria which were often orientated parallel to and
(Malt, 1969). It therefore seems not unlikely
within the plasmalemma folds (Fig. 3). These that the presence of proximal tubulelike cells
proximal tubulelike cells were found in both in the parietal epithelium of unilaterally nephouter cortical and juxtamedullary regions in rectomized rats may also represent an attempt
approximately 20% of the renal corpuscles of
the hypertrophied kidneys and were in sharp by the nephron to increase its capacity to uptake and modify the constituents of the glomcontrast to the typically squamous and relaerular filtrate. As such, these observations
tively smooth-surfaced parietal epithelial cells.
should probably be kept in mind if noted in biProximal tubule-like cells made up anywhere
from a very small portion to well over half of opsy samples in that they may also indicate a
the cells lining the parietal epithelium. In most compensatory response to a damaged or diseased kidney.
cases these cells were continuous with the
proximal tubules at the urinary pole of the reACKNOWLEDGMENTS
nal corpuscle. Scanning electron microscopy,
however, revealed that proximal tubulelike
This investigation was supported by the Nacells were often irregularly arranged around tional Institute of Health grant AM25417 and
and displaced to one side of the urinary pole or- in part by a grant from the National Kidney
ifice (Fig. 4). In addition, cells were often noted Foundation.
which could be interpreted as being in the process of acquiring the morphological characterLITERATURE CITED
istics of proximal tubule cells (Fig. 5).
The presence of proximal tubulelike cells in
the parietal epithelium has been reported a
number of times in the past, especially as a
metaplastic change in man (Macpherson, 1963;
Nachman, 1962; Reidbord, 1968; Ward, 1970)
and in both normal (Melis et al., 1974) and experimental mice (Melis and Orci, 1967; Melis et
al., 1972). There have even been reports that
the parietal epithelium can transform into the
morphologically elaborate glomerular epithelial cells in certain pathological states (Evan and
Gardner, 1976; Wilson, 1977). The present
findings of proximal tubulelike cells in rat kidneys which have undergone compensatory hypertrophy therefore further exemplify the pluripotency of this otherwise thin and inactiveappearing epithelium. In view of the facts that
Anderson, T.F. (1951)Techniques for preservation of three
dimensional structure in preparing specimens for the electron microscope. Trans. N.Y. Acad. Sci., 13: 130-134.
Bonvalet, J., M. Champion, F. Wanstok, and G. Berjal
(1972)Compensatory renal hypertrophy in young rats: Increase in the number of nephrons. Kidney Int., 1: 391 -396.
Evan, A.P., and K.D. Gardner Jr, (1976)Comparison of human polycystic and medullary cystic kidney disease with
diphenylamine-induced cystic disease. Lab. Invest., 35:
Macpherson, D.J. (1963)Metaplasia of renal glomerular capsular epithelium. J. Clin. Pathol., 16: 220-222.
Malt, R.A. (1969) Compensatory growth of the kidney. N.
Engl. J. Med., 280: 1446-1459.
Melis, M., F. Carpino, D. Palermo, and P. Motta (1974)Scanning and transmission electron microscopic observations
on the columnar cells of the parietal layer of Bowman's
capsule in normal mice. J. Microscopie, 19; 247-252.
Melis, M., F. Carpino, D. Palermo and P. Motta (1972)Modificazioni dell' epitelio parietale della capsula di bowman
in corso di nefrosi osmotica da saccarosio nel t o p . Boll.
It. Biol. Sper., 48; 294-297.
Melis, M., and L. Orci (1967)Inclusions cytoplasmatiques lamellaires dans les tubes collecteurs du rein au cows de la
nephrose osmotique. 2. Zellforsch.. 77; 425-434.
Fig. 1. Light microscopic view of a renal corpuscle from the hypertrophied kidney of a rat 5 months following contralateral nephrectomy. Although typical squamous parietal epithelial cells can be seen between the arrows, most of the cells making up the parietal epithelium appear similar to proximal tubule cells. Note the proximal tubule (PT)
evaginating from the
urinary pole (U)of the corpuscle. G. Glomerulus; S, capsular space of Bowman. x 250.
Fig. 2. Transmission electron microscopic view of proximal tubulelike cells (F'TL)lining the parietal epithelium in a hypertrophied rat kidney 5 months following contralateral nephrectomy. Note the similarity between these cells and those
lining the adjacent proximal tubules. DT, Distal tubule. x 1.100.
Fig. 3. Higher-magnificationview of the cells outlined in brackets in figure one above. Note the microvillous brush border
(MV). apical vesicles, numerous mitochondria, and folds of the plasmalemma. N, Nuclei. x 4,600.
Nachman, R.L. (1962) Metaplasia of parietal capsular epielectron opaque stain in electron microscopy. J. Cell Biol..
thelium of renal glomerulus. Report of an autopsied case
17: 208-212.
of carcinoma of the liver. Arch. Pathol., 73;60-64.
Ward. A.M. (1970) Tubular metaplasia in Bowman’s capReidbord, H.E. (1968) Metaplasia of the parietal layer of
sule. J. Clin. Pathol., 23; 472-474.
Bowman’s capsule. Am. J. Clin. Pathol., 50; 240-242.
Wilson, R.B. (1977) Variations in the epithelial lining of
Reynolds, E.S. (1963)The use of lead citrate a t high pH a s an
Bowman’s capsule. SEMi1977.2; 541-546.
Fig. 4. Scanning electron microscopic view of proximal tubulelike cells lining the parietal layer of Bowman’s capsule. The
white arrows delineate the irregular pattern of distribution of these cells relative to the urinary pole orifice. Note the thickness of the proximal tubule cells (large black arrows) compared to the typical squamous parietal epithelial cells (small dark
arrows). x 900.
Fig. 5. Higher-magnification view of the area outlined in brackets in Figure 4.Note that some cells in the center of this
micrograph appear to be in the process of acquiring a denser population of tall microvillous projections (MV).A prominent
microvillous brush border (BB)is evident to the left of these microvilli, whereas to the right are cells exhibiting a sparse population of short microprojections which usually characterize the free surfaces of parietal epithelial cells. C, Cilia. X 5,300.
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presence, nephrectomy, epithelium, response, kidney, unilateral, parietal, tubulelike, proximal, cells
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