ARTICLE |
Correspondence to: Kuniaki Takata, Lab. of Molecular and Cellular Morphology, Inst. for Molecular and Cellular Regulation, Gunma University, Showa-machi 3-39-15, Maebashi, Gunma 371-8512, Japan
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aquaporins (AQPs) are membrane water channel proteins expressed in various tissues in the body. We surveyed the immunolocalization of AQP3, an isoform of the AQP family, in rat epithelial tissues. AQP3 was localized to many epithelial cells in the urinary, digestive, and respiratory tracts and in the skin. In the urinary tract, AQP3 was present at transitional epithelia. In the digestive tract, abundant AQP3 was found in the stratified epithelia in the upper part, from the oral cavity to the forestomach, and in the simple and stratified epithelia in the lower part, from the distal colon to the anal canal. In the respiratory tract, AQP3 was present in the pseudostratified ciliated epithelia from the nasal cavity to the intrapulmonary bronchi. In the skin, AQP3 was present in the epidermis. Interestingly, AQP3 was present at the basal aspects of the epithelia: in the basolateral membranes in the simple epithelia and in the multilayered epithelia at plasma membranes of the basal to intermediate cells. During development of the skin, AQP3 expression commenced late in fetal life. Because these AQP3-positive epithelia have a common feature, i.e., they are exposed to an environment of possible water loss, we propose that AQP3 could serve as a water channel to provide these epithelial cells with water from the subepithelial side to protect them against dehydration. (J Histochem Cytochem 47:12751286, 1999)
Key Words: water channel protein, aquaporin, AQP3, rat epithelial tissues, immunolocalization
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Rapid water movement across the plasma membranes of cells is mediated by the membrane water channel proteins, aquaporins (AQPs). Ten isoforms of the AQP family have been thus far identified in mammals (AQP0AQP9: for review see
In the kidney collecting duct principal cells, AQP3 is localized at the basolateral plasma membranes (
Although localization of AQP3 has been described sporadically (
![]() |
Materials and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Anti-AQP3 Antibody
Oligopeptides corresponding to the COOH terminal amino acids of rat AQP1 (257269), AQP2 (257271), AQP3 (264279), AQP4 (311323), and AQP5 (251265) were synthesized with a Model 431A peptide synthesizer (Applied Biosystems; Foster, CA). Anti-AQP3 antibody was raised in a rabbit using the AQP3 peptide conjugated to keyhole limpet hemocyanin (Pierce; Rockford, IL).
Animals
Adult male Wistar rats 6 weeks of age, fetal Wistar rats at embryonic Days 15 and 18, and 4-day postnatal rats were used. All animal experiments were in compliance with the NIH Guide for the Care and Use of Laboratory Animals.
Immunoblotting
In adult rats, specimens of kidney inner medulla, mucosal layer of the forestomach, and palmar skin of the hind leg were removed. In the 4-day postnatal rats, specimens of palmar skin of the hind leg were removed. In the fetuses at embryonic Days 15 and 18, specimens of hind legs were removed. These specimens were cut into small pieces and quickly frozen with liquid nitrogen until used. Specimens were homogenized with a glass homogenizer in 10 volumes of ice-cold homogenization buffer consisting of PBS with 2 µg/ml pepstatin A, 2 µg/ml leupeptin, 100 KIE/ml aprotinin, and 2 mM phenylmethylsulfonyl fluoride. Proteins were determined with a BCA Protein Assay Kit (Pierce). Samples were denatured at 37 C for 10 min or at 70 C for 10 min in denaturation buffer composed of 2% SDS, 25 mM Tris-HCl, pH 7.5, 25% glycerol, 0.005% bromophenol blue, 23 mg/ml dithiothreitol, 300 µg/ml DNase I, and 4 mM MgCl2. SDS-PAGE and immunoblotting were carried out by a standard method using [125I]-protein A or [125I]-protein G (NEN; Wilmington, DE) (
Immunofluorescence Microscopy
From adult rats, specimens of (a) the urinary system: kidney, ureter, urinary bladder, and urethra; (b) body surface: skin from palm, ear, lower lip, anus, abdomen, back, and eyelid; (c) the digestive tract: lower lip, tongue, esophagus, stomach, duodenum, jejunum, ileum, cecum, proximal colon, distal colon, rectum, and anus; and (d) the respiratory tract: nasal cavity wall, trachea, bronchus, and lung, were removed. From rats at postnatal Day 4 and fetuses at embryonic Days 15 and 18, specimens of hind legs and skin from the abdomen were removed. These specimens were cut into small pieces, fixed in 3% formaldehyde in 0.1 M sodium phosphate buffer, pH 7.4, for 3 hr on ice. For preparation of cryostat sections, formaldehyde-fixed specimens were infused with 20% sucrose in PBS overnight, embedded in Tissue-Tek OCT compound (Sakura Finetechnical; Tokyo, Japan), and rapidly frozen with liquid nitrogen. Cryostat sections 36 µm thick were cut, mounted on poly-L-lysine-coated glass slides, immediately immersed in ethanol at -20C for 30 min, and rinsed with PBS. For semithin frozen sections, formaldehyde-fixed specimens were infused with 2.3 M sucrose in 0.1 M sodium phosphate buffer, pH 7.4, overnight (
Immunoelectron Microscopy
Cryostat sections 1016 µm thick from formaldehyde-fixed specimens of the urinary bladder and lower lip were cut, mounted on poly-L-lysine-coated glass slides, immediately immersed in ethanol at -20 C for 30 min, and rinsed with PBS. After incubation with the rabbit anti-AQP3 antibody (1:500 dilution), they were then incubated with Nanogold-conjugated anti-rabbit IgG (1:50 dilution; Nanoprobe, Stony Brook, NY), washed with PBS, and fixed with 1% glutaraldehyde in 0.1 M sodium phosphate buffer, pH 7.4, for 10 min (
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Antibody Specificity
By immunoblotting with anti-AQP3 antibody, two bands were observed in the homogenates of the kidney inner medulla as previously reported (
|
Immunohistochemistry and immunoblotting in the kidney with rabbit anti-AQP3 antibody gave the same results as those in previous studies (
|
Immunoblotting
By immunoblotting with this anti-AQP3 antibody, one sharp band at 26 kD and one broad glycosylated band at 3240 kD were detected in the homogenates of both forestomach and palmar skin, similar to those in the kidney (Figure 1A). These bands disappeared in the presence of COOH terminal peptide of the AQP3 protein (Figure 1B).
Immunofluorescence Microscopy
Urinary Tract.
We examined the renal pelvis, ureter (Figure 3A and Figure 3B), urinary bladder (Figure 3C and Figure 3D), and urethra (Figure 3E and Figure 3F). AQP3 was present in the transitional epithelia covering the lumina. Detailed examination at higher magnification revealed that AQP3 was abundant at the plasma membranes of transitional epithelial cells except for the large superficial cells directly facing the urine. In the distal part of the urethra, transitional epithelium changes to stratified squamous epithelium and finally leads to the epidermis of the skin. The labeling pattern for AQP3 in stratified squamous epithelium was similar to that in the epidermis, as described below. Positive labels for AQP3 were not seen throughout the subepithelial tissues.
|
Body Surface. AQP3 was detected in the epidermis of all the skin examined, i.e., skin from abdomen (Figure 4A and Figure 4B), back, lower lip (Figure 4C and Figure 4D), eyelid, ear, and palm (Figure 4E and Figure 4F). Although the thickness of the epidermis varied from part to part, i.e., thin in the abdomen and back, moderate in the lower lip, eyelid, and ear, and thick in the palm, labeling patterns for AQP3 were basically the same in all parts examined. The label for AQP3 was more intense in the basal and intermediate layers, where it was localized to the plasma membranes of the keratinocytes. The label for AQP3 gradually decreased as the cells differentiated and moved upward to the surface, and completely disappeared in the stratum corneum. Among accessory organs in the skin, AQP3 was also present along the external root sheath of the hair follicle, which is a tubular invagination of the epidermis, and in the sebaceous gland, including Meibomian glands of the eyelids (Figure 4C and Figure 4D).
|
Digestive Tract. We examined the oral surface of the lower lip, tongue, esophagus, stomach, duodenum, jejunum, ileum, cecum, proximal colon, distal colon, rectum, and anus. AQP3 was found in the epithelia in the upper part of the digestive tract, from the lower lip to forestomach (nonglandular portion), where the surface was covered with the cornified stratified epithelia (Figure 5A and Figure 5B). Abundant AQP3 was localized at plasma membranes of the epithelial cells in the basal and intermediate layers. Labeling gradually decreased towards the surface, and the keratinized cells were negative for AQP3, a pattern similar to that seen in the epidermis. At the junction of the forestomach and fundic stomach (glandular portion), cornified stratified epithelium abruptly changes to simple columnar epithelium. The labels for AQP3 decreased at this junction. In the fundic stomach, AQP3 was restricted to the surface mucous cells. The label for AQP3 gradually decreased according to the depth of the gastric pit. Cells deep in the pit and cells in the gastric gland opening to the pit had no label for AQP3 (Figure 5A and Figure 5B). Along the small intestine, AQP3 was hardly detected in the duodenum and jejunum. In the ileum, weak labeling for AQP3 was detected at the basolateral membranes of absorptive epithelial cells located in the villus tip (Figure 5C5F). Along the large intestine, AQP3 was detected in the distal colon (Figure 5G5J) and rectum, whereas it was not detected in the cecum or proximal colon. In the distal colon and rectum, AQP3 was localized at the basolateral membranes of epithelial cells directly facing the lumen and at the neck of the crypts (Figure 5I and Figure 5J). In the crypt, label for AQP3 gradually decreased according to the depth. Cells deep in the crypt had no label for AQP3. At the junction of the rectal and anal epithelia, simple columnar epithelium changes to cornified stratified epithelium, which is a continuation to the epidermis. In these stratified portion, the labeling pattern for AQP3 was basically the same as in the epithelia of upper gastrointestinal tract, such as esophagus. No label for AQP3 was seen throughout the subepithelial tissues along the digestive tract.
|
Respiratory Tract. We examined the nasal cavity wall, trachea, primary bronchus, and lung. AQP3 was present in the pseudostratified ciliated epithelia of the nasal cavity wall (Figure 6A and Figure 6B), trachea (Figure 6C and Figure 6D), primary bronchus, and a part of intrapulmonary bronchi (Figure 6E and Figure 6F). AQP3 was localized at the plasma membranes of basal cells and at the basolateral membranes of some ciliated cells but not in mucous cells. The epithelium of the nasal cavity wall had more AQP3-positive ciliated cells than the tracheal and bronchial epithelia (Figure 6A and Figure 6B). Interestingly, at the proximal portion of the intrapulmonary bronchi, AQP3 disappeared in the junction between the pseudostratified ciliated epithelium and the simple columnar epithelium, where basal cells disappeared (Figure 6E and Figure 6F). Most of the intrapulmonary bronchi, bronchioles, and alveoli were negative for AQP3.
|
Immunoelectron Microscopy
We examined the ultrastructural localization of AQP3 with Nanogold probes in the transitional epithelium of the urinary bladder and the epidermis of the cutaneous surface of the lower lip. Label for AQP3 was present along plasma membranes of both transitional epithelial cells and epidermal keratinocytes (Figure 7A and Figure 7C ). No positive label for AQP3 was seen in the cytoplasmic organelles. Immunohistochemical controls gave no positive staining, showing the specificity of the stain (Figure 7B).
|
Developmental Changes of AQP3 Expression in the Skin
By immunoblotting of the hind leg, AQP3 was not detected at embryonic Day 15. AQP3 was found in the hind leg at embryonic Day 18 as well as in the hind leg palmar skin at postnatal Day 4 (Figure 8). Next, we examined the immunolocalization of AQP3 in the hind leg and abdominal skin. No label for AQP3 was detected at embryonic Day 15 (Figure 9A and Figure 9B), whereas at embryonic Day 18 AQP3 was present at the epidermis (Figure 9C and Figure 9D). In the skin at postnatal Day 4, AQP3 was localized to the epidermal basal and intermediate cell layers but not in the stratum corneum, similar to that in the adult rat (Figure 9E and Figure 9F).
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We showed in this work that the water channel protein AQP3 was present in the epithelia covering the body surface and its continuities invaginated into the body, i.e., the urinary tract, digestive tract, and respiratory tract. AQP3 is expressed in the principal cells of the renal collecting ducts and is localized at the basolateral membrane (
On the body surface, AQP3 was present in the stratified epithelium covering the body surface, i.e., the epidermis of the skin. The epidermis, like the transitional epithelium of the urinary tract, serves as a barrier against water loss. The outermost layer of the epidermis is composed of keratinized stratum corneum (
Moreover, we examined AQP3 distribution throughout the digestive tract from the oral cavity to the anal canal. AQP3 was present at the epithelium of the upper part (from the lower lip to the forestomach) and the lower part (from the distal colon to the anal canal). AQP3 was present in the stratified squamous epithelia of the oral cavity, esophagus, and forestomach, whose ability to absorb water from the luminal contents is minimal. Much more AQP3 was present in the large intestine than in the small intestine, whereas 8090% of total water absorption throughout the digestive tract is carried out in the small intestine (
What, therefore, is the role of AQP3 in these epithelia? We suggest that AQP3 in these epithelia could provide a route of water entry to water-deprived cells to maintain intracellular osmolality and cell volume. The epithelia of the body surface and its invaginated continuities appear to exist in an environment of potential water loss for mammals that live on land. The mammalian integument is directly exposed to the air and is subject to possible loss of water through evaporation after birth. AQP3 was present in these covering epithelia. Upper digestive epithelia (from the oral cavity to the forestomach), lower digestive epithelia (from the distal colon to the anal canal), and upper respiratory epithelia, in all of which AQP3 is present, may be exposed to an environment similar to that of the body surface, i.e., potential water loss from the epithelial cells. In addition, AQP3 was present in the epithelia of the urinary tract directly facing the hypertonic urine, where the epithelial cells would encounter possible osmotic water loss due to the difference in tonicity between the luminal urine and the intracellular fluid. The above-mentioned epithelia in an environment of potential water loss have barrier properties on their surfaces, i.e., the stratum corneum in the cornified stratified epithelium and the unique apical membranes of the superficial epithelial cells in the transitional epithelium. AQP3 present in the basal (or abluminal) aspects of these epithelia may provide an additional protective system against water loss. Although AQP3 in the epithelia of the digestive tract may function in absorption of water in case of low osmolality in the lumen, the principal role of AQP3 at their plasma membranes may provide a route of water entry into epithelial cells from the subepithelial side to maintain intracellular osmolality and cell volume if cells undergo water loss.
In a simple epithelium sealed by tight junctions, AQP3 localized at the basolateral membranes may function directly in the entry of water into the cell. In the stratified epithelia, uppermost epithelial cells may be highest risk for dehydration, whereas AQP3 is localized in the intermediate and basal cells. Because epithelial cells are connected by gap junctions (
To provide insight into the roles of AQP3, including the above possibility in the epithelial cells, we examined the ontogenic changes of AQP3 expression in rat skin. The fetus has a low risk for osmotic change because it is surrounded by the amniotic fluid. After delivery, the body surface of the neonate is abruptly exposed to the air, and the risk for dehydration through the body surface arises. AQP3 was expressed in the epidermis of the body surfaces on embryonic Day 18 and postnatal Day 4, whereas it was not on embryonic Day 15.
In summary, we showed the comprehensive and detailed immunolocalization of AQP3 in rat epithelial tissues. Developmentally, expression of AQP3 in the epidermis begins in the late stage of fetal development. These observations suggest that AQP3 in these epithelia may play a role in providing water to water-deprived cells to maintain intracellular osmolality and cell volume. Further examination of the relationship between AQP3 expression and osmolality is needed to establish the functional role of AQP3 in the epithelia.
![]() |
Footnotes |
---|
Presented at the Fifth Joint Meeting of the Japan Society of Histochemistry and Cytochemistry and the Histochemical Society, July 2326, 1998, University of CaliforniaSan Diego, La Jolla, California.
![]() |
Acknowledgments |
---|
Supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports, and Culture of Japan. T. Matsuzaki is a JSPS Research Fellow.
We thank S. Matsuzaki for assistance.
Received for publication May 20, 1999; accepted May 20, 1999.
![]() |
Literature Cited |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aszterbaum M, Menon GK, Feingold KR, Williams ML (1992) Ontogeny of the epidermal barrier to water loss in the rat: correlation of function with stratum corneum structure and lipid content. Pediatr Res 31:308-317[Abstract]
Brown D, Katsura T, Kawashima M, Verkman AS, Sabolic I (1995) Cellular distribution of the aquaporins: a family of water channel proteins. Histochem Cell Biol 104:1-9[Medline]
Bruzzone R, White TW, Paul DL (1996) Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27[Abstract]
Chang A, Hammond TG, Sun TT, Zeidel ML (1994) Permeability properties of the mammalian bladder apical membrane. Am J Physiol 267:C1483-1492
Ebling FJG (1992) Functions of the skin. In Champion RH, Burton JL, Ebling FJG, eds. Textbook of Dermatology. Oxford, Blackwell Scientific, 125-155
Ecelbarger CA, Terris J, Frindt G, Echevarria M, Marples D, Nielsen S, Knepper MA (1995) Aquaporin-3 water channel localization and regulation in rat kidney. Am J Physiol 269:F663-672
Echevarria M, Windhager EE, Tate SS, Frindt G (1994) Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc Natl Acad Sci USA 91:10997-11001
Ezaki O, Kasuga M, Akanuma Y, Takata K, Hirano H, FujitaYamaguchi Y, Kasahara M (1986) Recycling of the glucose transporter, the insulin receptor, and insulin in rat adipocytes. Effect of acidtropic agents. J Biol Chem 261:3295-3305
Frigeri A, Gropper MA, Turck CW, Verkman AS (1995a) Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. Proc Natl Acad Sci USA 92:4328-4331[Abstract]
Frigeri A, Gropper MA, Umenishi F, Kawashima M, Brown D, Verkman AS (1995b) Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci 108:2993-3002
Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S (1993) Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361:549-552[Medline]
Gorin MB, Yancey SB, Cline J, Revel J-P, Horwitz J (1984) The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell 39:49-59[Medline]
Hasegawa H, Ma T, Skach W, Matthay MA, Verkman AS (1994) Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues. J Biol Chem 269:5497-5500
Hamann S, Zeuthen T, Cour ML, Nagelhus EA, Ottersen OP, Agre P, Nielsen S (1998) Aquaporins in complex tissues: distribution of aquaporins 1-5 in human and rat eye. Am J Physiol 274:C1332-1345
Hicks RM (1965) The fine structure of the transitional epithelium of rat ureter. J Cell Biol 26:25-48
Hicks RM (1966) The permeability of rat transitional epithelium. Keratinization and the barrier to water. J Cell Biol 28:21-31
Ishibashi K, Kuwahara M, Gu Y, Kageyama Y, Tohsaka A, Suzuki F, Marumo F, Sasaki S (1997a) Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J Biol Chem 272:20782-20786
Ishibashi K, Kuwahara M, Gu Y, Tanaka Y, Marumo F, Sasaki S (1998) Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem Biophys Res Commun 244:268-274[Medline]
Ishibashi K, Kuwahara M, Kageyama Y, Tohsaka A, Marumo F, Sasaki S (1997b) Cloning and functional expression of a second new aquaporin abundantly expressed in testis. Biochem Biophys Res Commun 237:714-718[Medline]
Ishibashi K, Sasaki S, Fushimi K, Uchida S, Kuwahara M, Saito H, Furukawa T, Nakajima K, Yamaguchi Y, Gojobori T, Marumo F (1994) Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc Natl Acad Sci USA 91:6269-6273[Abstract]
Ishibashi K, Sasaki S, Fushimi K, Yamamoto T, Kuwahara M, Marumo F (1997c) Immunolocalization and effect of dehydration on AQP3, a basolateral water channel of kidney collecting ducts. Am J Physiol 272:F235-241
Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P (1994) Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci USA 91:13052-13056
King LS, Agre P (1996) Pathophysiology of the aquaporin water channels. Annu Rev Physiol 58:619-648[Medline]
Knepper MA, Wade JB, Terris J, Ecelbarger CA, Marples D, Mandon B, Chou C-L, Kishore BK, Nielsen S (1996) Renal aquaporins. Kidney Int 49:1712-1717[Medline]
Koyama Y, Yamamoto T, Kondo D, Funaki H, Yaoita E, Kawasaki K, Sato N, Hatakeyama K, Kihara I (1997) Molecular cloning of a new aquaporin from rat pancreas and liver. J Biol Chem 272:30329-30333
Ma T, Frigeri A, Hasegawa H, Verkman AS (1994) Cloning of a water channel homolog expressed in brain meningeal cells and kidney collecting duct that functions as a stilbene-sensitive glycerol transporter. J Biol Chem 269:21845-21849
Ma T, Frigeri A, Skach W, Verkman AS (1993) Cloning of a novel rat kidney cDNA homologous to CHIP28 and WCH-CD water channels. Biochem Biophys Res Commun 197:654-659[Medline]
Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1998) Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J Biol Chem 273:4296-4299
Ma T, Yang B, Verkman AS (1997) Cloning of a novel water and urea-permeable aquaporin from mouse expressed strongly in colon, placenta, liver, and heart. Biochem Biophys Res Commun 240:324-328[Medline]
Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K (1999) Aquaporin-5 (AQP5), a water channel protein, in the rat salivary and lacrimal glands: immunolocalization and effect of secretory stimulation. Cell Tissue Res 295:513-521[Medline]
Murata F, Tsuyama S, Ihida K, Kashio N, Kawano M, Li ZZ (1992) Sulfated glycoconjugates demonstrated in combination with high iron diamine thiocarbohydrazide-silver proteinate and silver acetate physical development. J Electron Microsc 41:14-20[Medline]
Nielsen S, Chou C-L, Marples D, Christensen EI, Kishore BK, Knepper MA (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92:1013-1017[Abstract]
Nielsen S, King LS, Christensen BM, Agre P (1997) Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am J Physiol 273:C1549-1561[Medline]
Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P (1993) CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J Cell Biol 120:371-383[Abstract]
Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci USA 88:11110-11114[Abstract]
Raina S, Preston GM, Guggino WB, Agre P (1995) Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues. J Biol Chem 270:1908-1912
Sabolic I, Valenti G, Verbavatz J-M, van Hoek AN, Verkman AS, Ausiello DA, Brown D (1992) Localization of the CHIP28 water channel in rat kidney. Am J Physiol 263:C1225-1233
Sawada H, Esaki M (1994) Use of nanogold followed by silver enhancement and gold toning for preembedding immunolocalization in osmium-fixed, Epon-embedded tissues. J Electron Microsc 43:361-366[Medline]
Schnermann J, Chou C-L, Ma T, Traynor T, Knepper MA, Verkman AS (1998) Defective proximal tubular fluid reabsorption in transgenic aquaporin-1 null mice. Proc Natl Acad Sci USA 95:9660-9664
Selub SE (1995) Digestion and absorption. In Haubrich WS, Schaffner F, eds. Gastroenterology. Philadelphia, WB Saunders, 941-995
Shin B-C, Suzuki T, Matsuzaki T, Tanaka S, Kuraoka A, Shibata Y, Takata K (1996) Immunolocalization of GLUT1 and connexin 26 in the rat placenta. Cell Tissue Res 285:83-89[Medline]
Staehelin LA, Chlapowski FJ, Bonneville MA (1972) Lumenal plasma membrane of the urinary bladder. I. Three-dimensional reconstruction from freeze-etch images. J Cell Biol 53:73-91
Takata K, Kasahara T, Kasahara M, Ezaki O, Hirano H (1990) Erythrocyte/HepG2-type glucose transporter is concentrated in cells of blood-tissue barriers. Biochem Biophys Res Commun 173:67-73[Medline]
Takata K, Kasahara T, Kasahara M, Ezaki O, Hirano H (1991) Localization of Na+-dependent active type and erythrocyte/HepG2-type glucose transporters in rat kidney: immunofluorescence and immunogold study. J Histochem Cytochem 39:287-298[Abstract]
Takata K, Singer SJ (1988) Phosphotyrosine-modified proteins are concentrated at the membranes of epithelial and endothelial cells during tissue development in chick embryos. J Cell Biol 106:1757-1764[Abstract]
Umenishi F, Verkman AS, Gropper MA (1996) Quantitative analysis of aquaporin mRNA expression in rat tissues by RNase protection assay. DNA Cell Biol 15:475-480[Medline]
Yamamoto T, Sasaki S (1998) Aquaporins in the kidney: emerging new aspects. Kidney Int 54:1041-1051[Medline]
Yamamoto T, Sasaki S, Fushimi K, Ishibashi K, Yaoita E, Kawasaki K, Marumo F, Kihara I (1995) Vasopressin increases AQP-CD water channel in apical membrane of collecting duct cells in Brattleboro rats. Am J Physiol 268:C1546-1551