Transport proteins in rats renal corpuscle and tubules

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Medicina (Kaunas) 2004; 40(7)
EKSPERIMENTINIAI TYRIMAI
Transport proteins in rats’ renal corpuscle and tubules
Piret Hussar, Toivo Suuroja1, Ülo Hussar, Tiit Haviko2
Department of Anatomy, University of Tartu, 1Department of Morphology, Estonian Agricultural University
2
Department of Traumatology and Orthopedics, University of Tartu, Estonia
Key words: renal corpuscle, tubuli nephroni, transepithelial transport proteins.
Summary. The localization of transepithelial transport proteins for glucose and water
reabsorption in renal corpuscle and tubules epithelium was observed.
Material and methods. Immunohistochemistry of normal male Wistar rats’ kidney has been
performed. Facilitated diffusion glucose transporter GLUT4, Na(+)-dependent glucose cotransporter SGLT1, a cargo transporter TGN38, and water transporter aquaporin-2 (AQP2)
were used.
Results. An intensive GLUT4 expression in renal proximal tubules and in convoluted segment
of distal tubules has been observed. The intensive SGLT1 expression was marked in all renal
tubules, and also in the glomerulus of the renal corpuscle. TGN38 was expressed mainly in the
S1 of proximal tubules and a bit weaker in the distal tubules. The most intensive AQP2 expression
in the proximal tubules and in the thin part of Henle’s loop has been detected. In some cases
AQP2 expression in the collecting tubules has been observed. The same tubules nephroni are
marked heterogeneously. The distribution of transepithelial transport proteins in different parts
of nephroni is also greatly heterogeneous because of weak determination of urinary system.
Conclusion. The comparable transport-proteins distribution with technique of fluorescence
immunohistochemistry in rats’ renal corpuscle and tubules was elucidated. Data suggest that
expression of glucose and water transepithelial transporter proteins is heterogeneous in all parts
of nephron, and, probably, is in accordance with recycling of transport proteins.
Introduction
Two types of transepithelial glucose transporters
have been identified: facilitated-diffusion glucose
transporters (GLUT family), and Na(+)-dependent
glucose co-transporters (SGLT family). These transporters play important roles in the sugar reabsorption
in renal tubular cells (1–3). GLUT4 is localized in
the proximal and distal tubules, connected with renal
juxtaglomerular apparatus (JGA) (4), and in medullary
thick ascending limbs of Henle, not far from distal
tubules (5). SGLT1, an isoform of Na(+)-dependent
glucose transporters, is localized at the apical plasma
membrane of the proximal tubules (6, 7) and of the
thin segment of loop of Henle (portio conducens nephroni) (1, 8). TGN38 (trans-Golgi network) plays a role
as a cargo transporter in cells, also a role of evaluation
of the glucose transport (9). Aquaporin-2 (AQP2) is a
member of water channel proteins expressed mainly
in the kidney collecting duct cells and stored in the
intracellular compartment. Upon stimulation of anti-
diuretic hormone (ADH), AQP2 is recruited to the
plasma membrane, and plays a critical role in urine
concentration (10). The renal collecting duct principal
cells contain the AQP2 and small amount of the AQP3.
They are localized differently: AQP3 at the basolateral
plasma membranes and AQP2 in the intracellular vesicles and moves to the apical plasma membranes
when stimulated by vasopressin (11). AQP2 is specifically expressed in the renal tubules (12–14).
The aim of the present work is to perform the comparable fluorescence immunohistochemistry of renal
corpuscle and tubules epithelium in male Wistar rats
in order to observe the localization of transepithelial
transport proteins for glucose and water ultrafiltration
and reabsorption.
Material and methods
Tissue preparation
Male Wistar 4-week-old rats (supplied by the Animal Breeding Facility, Gunma University, Japan) were
Correspondence to Ü. Hussar, Department of Anatomy, University of Tartu, Arhitekti 28, 50407 Tartu, Estonia
E-mail: ulo.hussar@ut.ee
Transport proteins in rats’ renal corpuscle and tubules
anesthetized and killed with intraperitoneal injection
of sodium pentobarbital. In experiments 7 animals
were used. The renal cortical and medullary specimens
were taken with sharp scissors and scalpel under the
dissecting microscope. The renal specimens were removed at room temperature. Specimens were cut into
pieces, fixed in 3% formaldehyde in 0.1 M sodium
phosphate buffer, pH 7.4, for 3 hours on ice. Before
cryostat sectioning specimens were infused with 20%
sucrose in phosphate-buffered saline overnight, embedded in Tissue-Tek OCT compound (Sakura Fine
Technical, Tokyo, Japan) and frozen with liquid nitrogen. Cryostat sections of 3–7 mm thickness were cut,
mounted on poly-L-lysine-coated glass slides and fixed in ethanol for 30 minutes, thereafter rinsed with
PBS (15).
Antibodies
Primary antibodies anti-GLUT4, anti-SGLT1 and
anti-TGN38 were raised in a rabbit and characterized
as previously described (16–19). Oligopeptide corresponding to the COOH terminal amino acids of rat
AQP2 was synthesized with a model 431A peptide
synthesizer (Applied Biosystems; Foster, CA). Secondary antibodies Alexa 546 and rhodamine red Xlabeled donkey anti-rabbit IgG were products of Jackson Immunoresearch (West Grove, PA).
Immunofluorescence staining
Immunostaining procedures were performed basically as described previously (20). In short, sections
were first covered with 5% normal goat serum, then
sequentially incubated with the primary antibody and
the fluorescence labeled secondary antibody. In primary antibody solution F-phalloidin (1:50) was included. For nuclear counterstaining 4’,6-diamino-2-phenylindole dihydrochloride (DAPI; Boehringer-Mannheim, Mannheim, Germany) was added in the secondary antibody solution. Primary antibodies as well as
rhodamine red X were used at dilutions of 1:200; Alexa 546 at dilution of 1:1000.
Immunohistochemical controls
For immunohistochemical control primary antibody was replaced with normal rabbit serum. None of
the controls gave positive staining, confirming the specificity of the staining. These controls were carried
out in parallel with the experimental studies.
Specimens were examined with an AX-70 microscope equipped with Nomarski differential interference contrast and epifluorescence optics (Olympus,
Tokyo, Japan).
Results
An intensive facilitated-diffusion glucose transporMedicina (Kaunas) 2004; 40(7)
651
Fig. 1. Immunofluorescence localization of GLUT4
in the renal proximal S1 tubules and convoluted
segment of distal tubules (portio intermedia)
Fluorescence micrograph is shown by using rabbit antiGLUT4 as a primary antibody with Alexa 546 as a secondary antibody. Arrows and arrowheads indicate positive for
GLUT4 proximal S1 tubules and convoluted segments of
distal tubules respectively. Double arrowheads – negative
for GLUT4 thin and thick segments of Henle’s loop. CM –
corpusculum renis Malpighii, negative for GLUT4.
Bar: 150 µm.
ter GLUT4 expression in renal coiled segment (S1)
of proximal tubules (portio proximalis) and in convoluted segment of distal tubules (portio distalis), connected with JGA, was observed. By using rabbit antiGLUT4 as primary antibody with Alexa 546 as secondary antibody positive for GLUT4 were proximal S1
tubules and convoluted segments of distal tubules
respectively (Fig. 1). Negative for GLUT4 were thin
(portio conducens) and thick segments of Henle’s
loop, localized in medulla, and renal corpuscles (corpusculum renis Malpighii).
The intensive Na(+)-dependent glucose cotransporter SGLT1 expression was marked in all renal
tubules, and also in the glomerulus of the corpusculum
renis. By using rabbit anti-SGLT1 as primary antibody
with red-X as secondary antibody (Alexa 546 was too
weak in this case) glomeruli were positive for SGLT1
(it was not possible to differentiate endothelial barriercells from the cover cells - podocytes of visceral layer
of capsula glomeruli), coiled segments of proximal
and distal tubules, and Henle’s loop (Fig. 2).
TGN38 was expressed in all renal tubules, mainly
in the S1 of proximal tubules and a bit weaker in the
distal tubules to elevate the intracellular trans-Golgi
mechanisms for transporters. By using rabbit antiTGN38 as a primary antibody with Alexa 546 as a
secondary antibody, all tubules nephroni, mainly
proximal S1 tubules, were positive for TGN38 (Fig.
3). TGN38 is marked with different intensity in tubules
and localized heterogeneously.
652
Piret Hussar, Toivo Suuroja, Ülo Hussar, Tiit Haviko
Fig. 2. Immunofluorescence localization of SGLT1
in the renal corpuscle and all tubules of nephroni
Fluorescence micrograph is shown by using rabbit antiSGLT1 as a primary antibody with rhodamine red-X as a
secondary antibody. Arrows, arrowheads and double
arrowheads indicate positive for SGLT1 proximal and distal
tubules and thin segment of Henle’s loop (portio conducens
nephroni), respectively. GL – glomerulus of corpusculum
renis (consisting mainly of capillary endothelial cells, which
are covered with visceral layer cells of glomerular capsulapodocytes), positive for SGLT1. Bar: 200 µm.
Second part of our studies dealt with aquaporins
(AGPs) – water channel proteins serving in the water
permeation across cellular membrane. In our experiments the AQP2 was used. The most intensive AQP2
expression in the proximal tubules and in the thin part
of Henle’s loop has been detected. By using Rabbit
anti-AQP2 as primary antibody with Alexa 546 (Red-
X was too weak in this case) definite positive for
AQP2 were proximal tubules of nephroni and thin part
of Henle’s loop. In some cases aquaporin expression
in the collecting tubules has been observed (Fig. 4).
Renal corpuscles with ultrafiltration and hemato-renal
barrier cells lack the AQP2 marker.
In control group primary antibodies were replaced
with normal serum. Secondary antibodies Alexa 546
and red-X were used. All structures of nephroni and
collecting tubules lack positive specific staining. All
structures are indifferently colored red (Fig. 5).
The transport-proteins localization with various
techniques of fluorescence immunohistochemistry in
rats’ renal corpuscle and tubules was elucidated. These
data suggest that glucose and water transepithelial
transporter proteins expression have been observed
with different localization in tubules of nephroni.
SGLT1 expression also in the glomerulus of corpusculum renis Malpighii, and AQP2 expression still in
collecting tubules were noted. Probably, it is dependent on the weak determination of urinary organs.
Moreover, GLUT4 as well as TGN38 and AQP2 of
some tubules nephroni are marked heterogeneously
(with different intensity). Some ductuli at the same
picture are marked very strongly, and other are remarkably weaker. It is possible if these protein transporters
are functionally recycled in temporo-spatial conception.
Discussion
The transport proteins GLUT4, SGLT1, TGN38
a
b
Fig. 3. Immunofluorescence localization of TGN38 in the renal cortical tubules,
mainly in the proximal S1 tubules
Fluorescence micrograph (a) and corresponding Nomarski differential interference contrast image (b). Fluorescence
micrograph is shown using rabbit anti-TGN38 as a primary antibody with Alexa 546 as a secondary antibody. Arrows and
arrowheads indicate positive for TGN38 proximal and distal tubules of nephroni, respectively. TGN38 is marked with
different intensity and localized heterogeneously. CM – corpusculum renis Malpighii, negative for TGN38. Bar: 200 µm.
Medicina (Kaunas) 2004; 40(7)
Transport proteins in rats’ renal corpuscle and tubules
Fig. 4. Immunofluorescence localization of AQP2
in the tubules of nephroni, mainly in the proximal
tubules and in the thin part of the Henle’s loop.
Some collecting tubules are also marked. AQP2
lacks in the renale corpuscles
Fluorescence micrograph is shown by using rabbit antiAQP2 as a primary antibody with Alexa 546 as a secondary
antibody. Arrows, arrowheads and double arrowheads
indicate positive for AQP2 proximal tubules, thin part of
Henles’s loop and collecting tubules, respectively. CM –
corpusculum renis Malpighii, negative for AQP2. Bar:
200 µm.
Fig. 5. Control fluorescence micrograph using the
normal serum instead of primary antibodies and
one of secondary antibodies – Alexa 546
Fluorescence micrograph is shown by using normal serum
instead of a primary antibody with Alexa 546 as a secondary
antibody. All structures stained non-specifically in red color.
Nuclei are stained dark blue with DAPI (arrows).
Bar: 100 µm.
and AQP2 are the main transepithelial transporters of
glucose (GLUT4, SGLT1, TGN38) and water (AQP2)
in kidney (2, 4, 9, 14, 21).
The glucose is reabsorbed mainly in the proximal
tubules epithelium (principal) cells of nephroni. The
sugar is reabsorbed in the convoluted part of proximal
tubules by a low-affinity, and in the straight parts by a
Medicina (Kaunas) 2004; 40(7)
653
high-affinity (7). The water is reabsorbed mainly in
the proximal tubules of nephroni and in the thin part
of Henle’s loop, also in the other tubules of nephron
and in the renal collecting tubules (21).
In our research an intensive GLUT4 expression in
proximal tubules and in convoluted segment of distal
tubules, connected with JGA, has been observed.
GLUT4 transporters remove glucose from the plasma
membrane and recycle back to the intracellular storage
compartments (22). This mechanism of localization
for the GLUT4 responds rapidly and efficiently (23).
GLUT4 translocation is remarkably inhibited and regulated by inosital phosphatase (24). GLUT4 expression and glucose uptake are decreased in diabetic animals (25). The glucose transporter GLUT4 is insulinresponsive (4) and therefore localized in convoluted
segment of distal tubules, connected with endocrine
JGA.
SGLT1, an isoform of Na(+)-dependent glucose
transporters, is localized at the apical plasma membrane of the proximal tubules (6, 7) and of the thin
segment of Henle’s loop (1, 8). Our data suggest, that
intensive SGLT1 expression was marked in all renal
tubules, and also in the glomerulus corpusculi renis.
In our work the hemato-renal barrier cells (endothelial
cells of capillary wall) are colored together with ultrafiltration cells (podocytes of the visceral layer of
capsula glomeruli), covering the capillary network.
Its differentiation by used methods of immunohistochemistry is not possible. In comparing the distribution
of diffuse glucose transport (by GLUT4) and active
Na(+)-dependent transport (by SGLT1) the important
role of Na(+)-dependent glucose transporters (SGLTfamily) in renal sugar metabolism was accented
(SGLT1 expressed in all parts of nephroni and in glomerulus corpusculi renis).
In our experiments TGN38 was expressed in all
renal tubules, highly in the S1 proximal tubules as it
elevates the glucose reabsorption. TGN38 was located
mainly in proximal convolute tubules epithelium (in
principal cells) and was a bit weaker in distal tubules.
Other parts (straight segments of proximal tubules,
thin and thick segments of Henle’s loop) of nephroni
are marked heterogeneously with different intensity.
It may be interpreted in recycling of TGN38 with apical and/or lateral surface of cell membrane and the
trans-Golgi network as well as other intracellular
compartments (26–28).
Second part of our studies dealt with water channel
proteins – aquaporins (AGPs) – serving in the water
permeation across cellular membrane. At least 10 isoforms of aquaporins have been identified, from which
654
Piret Hussar, Toivo Suuroja, Ülo Hussar, Tiit Haviko
AQP1 to 4 playing major roles in nephron water transport. Major renal aquaporin AQP2 has been reported
to be present in small vesicles in the cytoplasm, serving
as the pool of the AQP2 storage and responsible for
the ADH-induced translocation to the plasma membrane. Once AQP2 is at the plasma membrane of the
renal tubule cells, it serves in the reabsorption of water
from primary urine. Therefore, in our experiments
AQP2 was used. Our data suggest that the most intensive AQP2 expression in the proximal tubules and in
the thin part of Henle’s loop has been detected. In
some cases aquaporin expression in the collecting tubules has been observed. AQP2 expression lacks in
the distal tubules of nephroni, in contrary to glucose
transporter proteins (GLUT4, SGLT1) expression at
the distal tubules, connected with renal juxtaglomerular apparatus (JGA). Accordingly, the endocrine
regulation of water reabsorption is realized by the
para-juxtaglomerular system in the renal tubules. The
AQP2, water channel protein, is mainly located in the
apical plasma membrane of all renal tubules epithelial
cells and in the basolateral surface of the inner medullary-collecting duct (21). After intraperitoneal administration of oxytocin a remarked redistribution (translocation) of AQP2 in the intracellular compartments
was noted (21). Oxytocin may be one of the factors,
which accounts of vasopressin-independent AQP2
targeting in the ren. AQP2 is ADN-responsive (10)
and therefore is expressed by vasopressin, etc.
The molecular mechanisms of receiving the signal
on the renal tubular epithelial cells receptors for stimulation the expression of the transport proteins GLUT4,
SGLT1, TGN38 and AQP2 have been unknown.
GLUT4 as well as TGN38 and AQP2 of some kind
of tubules nephroni (proximal, distal tubules, etc.) are
marked heterogeneously (with different intensity).
Some ductuli at the same picture are marked strongly,
and others are remarkably weaker. Such kind of picture
is possible if these protein transporters are functionally
recycled in temporo-spatial conception.
The localization and activity of transepithelial
transport proteins in different parts of nephron is also
greatly heterogeneous. Probably, it is dependent on
the weak determination of urinary organs (renal tubu-
les among them). These peculiarities of biology of
the urinary system are required to provide the especially fine filter for elimination.
Conclusion
The comparable fluorescence immunohistochemistry was performed in male Wistar rats to observe
the localization of transepithelial transport proteins
for glucose and water ultrafiltration and reabsorption
in renal corpuscle and tubules.
An intensive GLUT4 expression in proximal tubules and in convoluted segment of distal tubules, connected with JGA, has been observed. The intensive
SGLT1 expression was marked in all renal tubules,
and also in the glomerulus of renal corpuscle. Na(+)dependent glucose transport in ren is more extensive
compared to facilitated-diffusion glucose transport.
TGN38 was expressed mainly in the S1 of proximal
tubules and was a bit weaker in distal tubules to elevate
the glucose reabsorption. The most intensive AQP2
expression in the proximal tubules and in the thin part
of loop of Henle has been detected. In some cases
aquaporin expression in the collecting tubules has been
observed.
GLUT4 as well as TGN38 and AQP2 of some kind
of tubules nephroni (proximal, distal tubules, etc.) are
marked heterogeneously (with different intensity).
Probably, it is possible if these protein transporters
are functionally recycled in temporo-spatial conception.
The localization and activity of transepithelial
transport proteins in different part of nephroni is also
greatly heterogeneous. Probably, it is dependent on
the weak determination of urinary organs.
Acknowledgements
We wish to thank Prof. K. Takata and the whole
Laboratory of Molecular and Cellular Morphology,
Institute for Molecular and Cellular Regulation of
Gunma University, Japan where Piret Hussar had a
great luck to work with a perfect team. This work was
supported in part by Grants-in-Aids for Scientific
Research from the Ministry of Education, Science,
Sports and Culture of Japan.
Baltymø perneðimas þiurkiø inkstø kûneliuose ir vamzdeliuose
Piret Hussar, Toivo Suuroja1, Ülo Hussar, Tiit Haviko2
Tartu universiteto Anatomijos katedra, 1Estijos þemës ûkio universiteto Morfologijos katedra
2
Tartu universiteto Traumatologijos ir ortopedijos klinika, Estija
Raktaþodþiai: inksto kûnelis, nefrono vamzdeliai, baltymø transepitelinis perneðimas.
Medicina (Kaunas) 2004; 40(7)
Transport proteins in rats’ renal corpuscle and tubules
655
Santrauka. Darbo tikslas. Nustatyti baltymø transepiteliniø neðikliø lokalizacijà gliukozës ir vandens
reabsorbijos metu inkstø kûneliuose ir vamzdeliuose.
Tyrimo medþiaga ir metodai. Inkstuose atlikta imunohistochemija sveikoms vyriðkos lyties Wistar veislës
þiurkëms. Naudoti: lengvinanti gliukozës difuzijà neðiklis GLUT4, nuo Na(+)– priklausantis gliukozës koneðiklis SGLTI, neðiklis TGN38 ir vandens neðiklis akvaporinas-2 (AQP2).
Rezultatai. Intensyvi GLUT4 ekspresija uþfiksuota inkstø proksimaliniuose vamzdeliuose ir distaliniø
vamzdeliø vingiuotuose segmentuose. Intensyvi SGLTI ekspresija buvo ryðki visuose inkstø vamzdeliuose,
taip pat inkstø kamuolëliø kûneliuose. TGN38 ekspresija daugiau pasireiðkia proksimaliniø S1 segmento
vamzdeliuose, silpniau – distaliniuose vamzdeliuose. Didþiausio intensyvumo AQP2 ekspresija nustatyta
proksimaliniuose vamzdeliuose ir iðplonëjusio vamzdelio (Henlës kilpos) kylanèiojoje dalyje. Kai kuriais
atvejais AQP2 ekspresija buvo pastebëta surenkamuose inkstø vamzdeliuose. Tie patys nefrono vamzdeliai
pasiþymi ir heterogeniðkumu. Pasiskirstymas baltymø transepiteliniø neðikliø skirtingose nefrono dalyse taip
pat yra þymiai heterogeniðkas, nes silpnai determinuotas ðlapimo iðskyrimo sistemoje.
Iðvados. Lyginamasis baltymø neðikliø pasiskirstymas þiurkiø inkstø kûneliuose ir vamzdeliuose buvo
nustatomas fluorescencine imunohistochemine metodika. Gauti duomenys rodo, kad gliukozës ir vandens
transepitelinis baltymø perneðimas heterogeniðkas visose inksto dalyse ir tai atitinka baltymø neðikliø recirkuliacijà.
Adresas susiraðinëjimui: Ü. Hussar, Department of Anatomy, University of Tartu, Architekti 28, 50407 Tartu, Estonia
El. paðtas: ulo.hussar@ut.ee
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Received 10 December 2003, accepted 22 April 2004
Straipsnis gautas 2003 12 10, priimtas 2004 04 22
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