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Some morphological aspects of the resorption of carbohydrates in the renal tubules of the goldfish (Carassius auratus).

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SOME MORPHOLOGICAL A S P E C T S
03' T H E RESORPTIOK O F CARBOHYDRATES I N
THE R E S A L TUBUILES O F THE GOLDFISH
(CARASSIUS AURATUS)
OSCAE C H A R L E S JAFFEE
Departm en t o f Anatomy, University of Arkansas
School of Medicine, Little Rock, Arkansas
N I N E FIGURES
The studies of Smith and his co-workers have shown that
glucose resorptioii is a n active, physiological process characterized by maximal rates (Smith, '51). Very little information is available with regard to the cellular mechanisms involved in this process, however. Oliver has shown that mitochondria a r e involved in the renal resorption of proteins (cf.
Oliver et al., '54) and Zingg ('51) has presented evidence that
a relationship exists between mitochondria and the resorption of sugars. I n a previous study (Jaffee, '56) the role of
mitochondria in protein resorption has been demonstrated in
in v i t r o preparations of isolated nephrons of the goldfish kidney and this technique has been utilized in a study of glucose
resorption in an attempt to define the cellular basis f o r this
process.
Ohservations of' the effects of sucrose arid inulin have been
inclucled in the present report. The use of sucrose as a diuretic had led to a controversy with regard to the effects of
this substance on the tubule cells (cf. Smith, '51) and the use
of inulin as a measure of the glomerular filtration rate has
posed the problem as to whether this substance had any effect
on the tubule cells (ibid.). The experiments with sucrose and
inulin also serve a s a comparison for the results obtained in
the experiments with glucose.
* Present address : Cliroriie Disease Research Institute, University of Buffalo,
Buffalo 14, N. Y .
153
?IIiriinial quantities of 0.5 gm of glucose were found necessary to produce droplets in the tubules with a single injection
(fig. 2) but one injection of 0.2 gm of sucrose readily produced droplet laden tubules (fig. 3 ) . Inulin was injected in
0.2 gm per milliliter doses (the solubility limit of this s u b
stance) and three consecutive injections at 1 2 hour intervals
were needed to produce droplets (fig. 4).
At minimal doses droplets were first noted in the middle
third of the proximal tubules, and droplets were found in
the proximal third of this segment as the dosage levels were
raised. A t still higher dosages the entire proximal tubules
were found to contain droplets. This droplet distribution was
similar to that reported during the process of protein resorption (Jaff ee, '56).
Supravital staining of the droplets with J a n u s green B
revealed that the droplets took up this dye with the smaller
droplets appearing to take the dye more intensely than the
larger ones.
Iron hematoxylin staining of the glucose injected tissues
revealed that the droplets were demoristrahle with a minimum
of staining and that the ground substance of the cells was
well preserved (fig. 5) ; in this figure the brush border is
stained very lightly although this structure takes u p the
stain very readily. Similar staining of sucrose injected tissues (fig. 6) revealed that the droplets took up the stain
poorly and that it was necessary to ovcrstain the brush border in order to demonstrate the droplets. The poor preservation of the ground substance may also be noted in figure 6.
The degree of intensity of staining of the droplets and ground
substance preservation after inulin injections was found to
be intermcrliate between that of glucose and sucrose and is
illustrated in figure 7.
Formalin fixation gave poor results in the present study,
as compared with Champy fixation. Again the droplets were
best demonstrated and tlic tubule cells loest preserved with
glucose injected tissues. Glucose produced droplets stained
ivith periodic acid-Schiff stain a r e illustrated in figure 8 and
156
OSCAR C H A R L E S J A F F E B
similar droplets stained with fast green a r e shown in figure 9.
When the renal tuhules of fish were examined one week
after the time normally required to produce droplets it was
found that the glucose produced droplets had disappeared
wliile the sucrose arid innlin produced droplets were still
1)re se 11t .
I)JSCURSIOS
The role of mitochoiitlria in the resorption of proteins
has been demonstrated hy Oliver et al. (’54). Protein produced droplets have been demonstrated in the present species
in in vitro preparations of the intact nephrons of the goldfish and the presence of a mitochoiidrial component indicated
by the J a n u s green B supravital staining of these droplets
(Jaffee, ’56). The pi-oduction of similar droplets after glucose administration is liere intci*pretcrl similarly, i.e., that thc
glucose droplets a r e formed in part by mitochondria ; the iron
hematoxylin staining of these d r o p k t s is further evidence in
the same direction.
The better fixation u i i d staining of the glucose produced
droplets, as compared to those pi-oduced by sucrose and inulin, is interpeted to mean that the glucose droplets comprised more of a physiological entity in the tubule cells than
the other substances tested. Tlie histological picture produced in the sucrose injected tissues can well he compared
with the descriptions of “liyclropic degeneration” noted in
some cases where patients have heen treated with hypertonic
sucrose.
The need for the administration of comparatively large
aniounts of glucose to produce droplets has indicated that
this substance is nornially resorbed without droplet formation
and that the droplets appear only when this mechanism becomes exhausted and this sugar is acciimnlated to a marlred
degree in the cells. Such a seauence of events in tubular
resorption have been postulated by Oliver et al. ( ’54). Sucrose
is poorly resorbed by the kidney but readily diffuses into the
R E X A L KESORPTION OF CAIIBOHYDRATES
157
tubule cells (Smith, '31 ). Sucrose thus accumulates in the
cells much more rapidly than glucose a s seen by the production of droplets with smaller quantities of sucrose. The effects of inulin on the tubule cells were found to be similar
to those of sucrose, but occurred much more slowly; the larger molecular weight of inuliri (5000) and its lower diffusahility (ibid.) probably account for these differences. This data
has also indicated that any substance present in the
lumina of the tubules can diffuse into the cells and that the
selective barrier of tubular resorption is probably at the
basement mernbrane.
The periodic acid-Schiff and fast green staining of the
droplets has raised the possibility that these structures have
a protein component. The PAS stain has been considered
specific for mucopolysaccharies (cf. Jaffee, '56) and the fast
green stain considered specific for basic proteins (Schrader
and Leuchtcnberger, ',jO). Thus, in the case of glucose, where
these stains were best demonstrated, evidence is found to the
effect that glucose may be transported in the tubule cells in
combination with a protein. This aspect of the present investigation is schedulecl for further study.
SllMMARY
The production of di*oplets lias beeii noted in the proximal
convoluted tubules of the isolated ncphrons of the goldfish
(Cnrcrssiu.~aurntus) in in i d r o preparations, following the
intrapei.itonea1 injections of glucose, sncrose and inulin. The
relationship of these substances to the mitochondria of the
tuhule cells h a s hwii suggested by tlie staining properties of
tlicse droplets, and cvideiiccl has hecw piweiited to the effect
that tlie glucoso pi.otluced tli.oplcts formed iiito a fiimcr union
Jvith tlie cellular cornI)oiicnts than did tlie droplets formed
by the otlicr substancc>s. The similarities between the morphological aspects of cai.l)ohydrate imorption and protein
resorption, a s slio\vn 1)y ii previous study (Jaffee, '56), a r e
discussed. $hitlciicc hits also 1 ) e c ~ l l pres('11tecl that c a ~ h o -
158
OSCAI;
C H A R L E S JAFFEE
hydrates are cornbiiicd wi tli protein substances in the renal
tubule cell.
LITEIIATUJtE CITED
FOKSTEK,
R.. 1’. 1948 Use of thiu kithiey slices a i d isolated rc~iial tuljules f o r
t h e direct study of ccxllular transport kinetics. Science, 108 : 65-67.
.JAFI”EE, 0. C. 1956 Sonic niorpliologicnl aspects of protein absorption iii isolattyl
renal tubules of the goldfisli (Camssius aftratits). Anat. Iiec., 125:
495-508.
ITCMANUS, J . 1’. A . 1946 Histological denionstration of niuciii a f t e r periodic
acid. Nature, 258: 202.
OLIVER, J., hf. MACDOWELLA S D Y . C. LEE 1954 ~ e l l u l a riiiecliaiiisnis of protein metabolism i n the ncphron. I. Tlie structural a s p w t s of proteiiiu r i a ; tubular absorptioii, droplet, and the tlisposal of protciiis. J.
EX^. &fed., 99: 589-604.
S C H K A D E K , h’., A X D c. LEUCH‘ BEKGER
1950 A cytochemic:il analysis of tlie
fuiictional iiiterre1:itioiis of the various cell structures i n Arcc’lifts alboptinclatits (tle G e e r ) . Esp. Cell Rcs., 1 : 421-252.
S H A N N O N , J. A., A N D 13. \v. SMITH 1935 The cxcretioii of iiiulin, xylosc, and
u r e a b y iiornial :ind pliloriziiiizcd inan. J. Cliii. Invest., 1.4 : 393-101.
SMITH, H. W. Tlir Kidiicy. Oxford Viiiversity Press, New York.
ZINGG,W. 1951 Uber espcriineiitelle rolireuckersp,cielieruiig i n der iiiitorliondrieir
der niprtnbulr. Sclireiz. Z. allg. Path. 11. Tiakt., 7 4 : l-l(i.
1
9
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renar, aspects, auratus, resorption, tubules, carbohydrate, morphological, carassius, goldfish
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