Expression of the prostaglandin F receptor (FP) gene along the mouse genitourinary tract

Osamu Saito1, Youfei Guan1, Zhonghua Qi1, Linda S. Davis1, Martin Kömhoff2, Yukihiko Sugimoto3, Shuh Narumiya3, Richard M. Breyer1, and Matthew D. Breyer1

1 Division of Nephrology, Department of Medicine, Vanderbilt University Veterans Affairs Medical Center, Nashville, Tennessee 37212; and Departments of 3 Pharmacology, Faculty of Medicine, and 2 Physiological Chemistry and Faculty of Pharmaceutical Sciences, Kyoto University, Kyoto, Japan 606


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

PGF2alpha is one of the major prostanoids produced by the kidney. The cellular effects of PGF2alpha are mediated by a G protein-coupled transmembrane receptor designated the FP receptor. Both in situ hybridization and beta -galactosidase knocked into the endogenous FP locus were used to determine the cellular distribution of the mouse FP receptor. Specific labeling was detected in the kidney, ovary, and uterus. Abundant FP expression in ovarian follicles and uterus is consistent with previous reports of failed parturition in FP-/- mice. In the kidney, coexpression of the mFP mRNA with the thiazide-sensitive cotransporter defined its expression in the distal convoluted tubule (DCT). FP receptor was also present in aquaporin-2-positive cortical collecting ducts (CCD). No FP mRNA was detected in glomeruli, proximal tubules, or thick ascending limbs. Intrarenal expression of the FP receptor in the DCT and CCD suggests an important role for the FP receptor regulating water and solute transport in these segments of the nephron.

dinoprost; nephron; natriuresis; water


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

PROSTANOIDS, including PGE2, PGD2, prostacyclin (PGI2), TxA2, and PGF2alpha , modulate a diverse spectrum of physiological processes, including reproduction, inflammation, microvascular resistance, and epithelial ion transport rates (7, 33). Despite originating from a common precursor, PGH2, the effects of these derivative prostanoids may either oppose each other, as in the case of the prothrombotic action of TxA2 vs. the antithrombotic effects of PGI2 (16), or exert functionally complementary effects such as the smooth muscle constrictor effects of TxA2 and PGF2alpha (48). These cellular and physiological effects are mediated by the selective interaction of each prostanoid with unique G protein-coupled receptors (GPCRs) (8, 33, 46). Genetic disruption of GPCR prostanoid receptors has not only firmly established roles for these receptors as critical mediators of prostanoid action, but it also revealed significant new biology related to the roles of prostaglandins (33, 46). In the case of the FP receptor for PGF2alpha , these studies revealed that the FP receptor is highly expressed in the ovary and its function is essential for normal parturition (47).

The FP receptor is also highly expressed in the kidney (2, 44). Furthermore, PGF2alpha is a major product of cyclooxygenase-mediated arachidonate metabolism in the kidney (14), and renal synthesis of PGF2alpha is regulated by sodium depletion, potassium depletion, and adrenal steroids (35, 40). Infusion of exogenous PGF2alpha modulates renal salt excretion and urine flow (42). Despite this evidence supporting a role for the FP receptor in the kidney, the intrarenal sites of expression or mechanism of these PGF2alpha -activated GPCRs in the kidney remain poorly characterized. The purpose of the present studies was to map the intrarenal distribution of the FP receptor in the kidney.


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Generation of RNA fragments. RNA probes were generated by RT-PCR to amplify a 399-bp fragment spanning the 5'-UTR to Arg100 in the coding region of the mouse FP receptor cDNA from kidney RNA. The sense primer was 5'-AACCACTCAGTGGCTCAGGA-3', and the antisense primer was 5'-GCGGATCCAGTCTTTATC3'. The identity of the amplified product was directly confirmed by sequencing and alignment with the mouse FP receptor (BLAST, NCBI) and ligated into the transcription vector pCR2.1 (Invitrogen). The two distinct clones were isolated, which allowed transcription of either the sense or antisense cDNAs using the T7 promoter. The plasmids were linearized and RNAs transcribed from the flanking T7 promoter in the presence of [alpha -35S]UTP. RNA (5 × 105 cpm/µl) was used for in situ hybridization.

Tissue preparation. C57BL/6J mice weighing between 20 and 30 g were anesthetized using intraperitoneal ketamine and xylazine (200 mg and 15 mg/kg, respectively). After surgical anesthesia was achieved, mice were killed by cervical dislocation and kidney, stomach, liver, ovary, and uterus were harvested.

For in situ hybridization studies, tissues were fixed in 4% paraformaldehyde. Tissues were imbedded in paraffin and 7-µm sections were cut. Before hybridization, sections were deparaffinized, refixed in paraformaldehyde, treated with proteinase K (20 µg/ml), washed with PBS, refixed in 4% paraformaldehyde, and treated with triethanolamine plus acetic anhydride (0.25% vol/vol). Finally, sections were dehydrated in 100% ethanol.

Anti-sense RNA was hybridized to the sections at 50-55°C for ~18 h as described previously (11). After hybridization, sections were washed at 50°C in 5× SSC + 10 mM beta -mercaptoethanol for 30 min. This was followed by a wash in 50% formamide, 2× SSC, and 100 mM beta -mercaptoethanol for 60 min. After additional washes in 10 mM TRIS, 5 mM EDTA, 500 mM NaCl (TEN), sections were treated with RNase (10 µg/ml), at 37°C for 30 min, followed by another wash in TEN (37°C). Sections were then washed twice in 2× SSC and then twice in 0.1× SSC (50°C). Slides were dehydrated with graded ethanols containing 300 mM ammonium acetate.

For detection of the hybridized probe, slides were dipped in photo emulsion (Ilford K5, Knutsford, UK) diluted 1:1 with 2% glycerol/water and exposed for 7 days at 4°C. After development in Kodak D19, slides were counterstained with hematoxylin and eosin. Photomicrographs were taken using a Zeiss Axioskop using both bright- and darkfield optics.

Preparation of tissue for beta -galactosidase staining and immunohistochemistry. Multiple organs including liver, spleen, stomach, duodenum, lung, and kidneys of the double transgenic mice were harvested at death. After fixation with 4% paraformaldehyde plus 0.25% glutaraldehyde in PBS for 2 h at 4°C, tissue sections were cut with a vibratome into 200-µm slices. To detect beta -galactosidase (beta -gal) activity, these slices were bathed in permeabilization solution (2 mM MgCl2, 0.01% sodium deoxycholate, 0.02% NP-40 in PBS) for 30 min × 2 and then stained with 1 mg/ml 5-bromo-4-chloro-3-indolyl-D-galactopyranoside (X-gal; Sigma, St. Louis, MO) in staining solution (2 mM MgCl2, 5 mM potassium ferricyanide, potassium ferrocyanide, 20 mM Tris, pH 7.4 in PBS) at room temperature in the dark for 48 h (5, 36). Tissues were washed, dehydrated through graded ethanol series, and embedded in paraffin, using standard procedures. Serial 5-µm sections were cut and examined by light microscopy.

Immunostaining. To define the nephron segments that expressed FP receptor mRNA, in situ hybridization was followed by immunostaining of the tissue sections with a rabbit anti-collecting duct antibody or a goat anti-human Tamm-Horsfall antibody, which specifically recognizes medullary and cortical thick ascending limb (mTAL and cTAL) as well as the early portion of the distal tubule. To define the beta -gal-positive nephron segments, sections were co-stained using a goat anti-human Tamm-Horsfall antibody (1:2,500, Organon-Technika) that specifically recognizes mTAL and cTAL as well as the early portion of the distal tubule (28, 49). A commercially available anti-aquaproin-2 (AQP2) antibody was used to specifically identify collecting duct principal cells (AQP21-A, Anti-Rat AQP2 IgG no. 2, Alpha Diagnostic International, San Antonio, TX) (26). To define distal convoluted tubule segments (DCT), an anti-thiazide-sensitive NaCl cotransporter (TSC) antibody was used [generously provided by Dr. M. Knepper (30)]. Staining was localized using a biotinylated anti-IgG secondary antibody applied to beta -gal-stained sections. Biotin was identified using streptavidin coupled to horseradish peroxidase and was visualized with diaminiobenzidine (Vector Vectastain ABC kit). Sections were viewed and imaged with a Zeiss Axioskop and Spot-Cam digital camera (diagnostic instruments).


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Intrarenal distribution of the FP receptor. Autoradiograms of the kidney, with an anti-sense FP receptor riboprobe (Fig. 1), showed intense labeling of subpopulations of epithelial tubules in the renal cortex. No specific labeling was obtained with a sense mRNA probe (data not shown). There was light and diffuse labeling of the outer medulla. There was no detectable labeling of the papilla. A similar pattern of FP mRNA expression was obtained by mapping beta -gal activity in heterozygous FP +/- mice (Fig. 1B).


View larger version (77K):
[in this window]
[in a new window]
 
Fig. 1.   Expression of FP receptor mRNA in kidney. A: ×10 darkfield photomicrograph of an in situ hybridization using the mouse FP receptor mRNA as a riboprobe. The white grains indicate areas of message expression that predominate in the cortex. B: ×50 photomicrograph of a kidney from an FP +/- mouse. The blue reaction product identifies structures in which beta -galactosidase activity is present in cells, marking active transcription of the lacZ gene knocked into the endogenous FP receptor locus in mice.

Segmental expression of the mFP receptor was most abundant in tubules that colabeled with antibodies to the TSC- and AQP2 antibody (collecting duct specific)-positive tubules. There was no evidence for hybridization of the FP antisense fragment to either proximal straight tubules or thick ascending limb (Fig. 2). No labeling of papillary or inner medullary structures was observed.


View larger version (131K):
[in this window]
[in a new window]
 
Fig. 2.   Localization of FP receptor mRNA in kidney by beta -galactosidase staining and in situ hybridization. Coimmunostaining using segment-specific antibodies was performed. For in situ hybridization, panels show tangential illumination combined with brightfield illumination of a mouse kidney section where the white grains depict sites of FP receptor riboprobe hybridization. Segments expressing beta -galactosidase driven by the endogenous FP promoter are identified by the blue reaction product. Thiazide-sensitive cotransporter (TSC) immunoreactivity, characteristic for the distal convoluted tubule (DCT), colocalizes with either white grains or beta -galactosidase, indicating expression of FP receptor mRNA in DCT. Tamm-Horsfall (TH) immunoreactivity, restricted to the thick ascending limb (TAL), does not colocalize with FP receptor mRNA and TH-positive TAL, whereas the FP receptor is expressed in TH-negative tubules. Aquaporin-2 (AQP2) specifically labels the collecting duct and colocalizes with FP receptor mRNA expressed in AQP-positive tubules.

Extrarenal tissues. Abundant beta -gal expression was detected in stromal surrounding the ureteral smooth muscle (Fig. 3). Epididymus possesses endogenous beta -gal activity in control animals, complicating the interpretation of this tissues. However, this endogenous activity was not present in any other organs from wild-type animals examined including the distal vas deferens and luminal cells of the testis where low levels of beta -gal activity were detected. In the female genital tract, beta -gal expression was detected in ovary corpora luteal cells and the smooth muscle cells lining the fallopian tubule and uterus. Patches of intense beta -gal labeling in tissues obtained from FP +/- mice were associated with dermal hair follicles. Liver failed to show any beta -gal staining in hepatocytes, however, labeling of vascular tissue was detected.


View larger version (124K):
[in this window]
[in a new window]
 
Fig. 3.   beta -Galactosidase expression in FP-lacZ knocked into tissues: ureter, testis, uterus, ovary, skin, and liver.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The kidney is a site of robust prostaglandin synthesis and expresses abundant prostanoid receptors (8, 10, 46). Renal expression of the FP, EP1, EP3, and TP receptor mRNAs is particularly high (13, 25, 46). Furthermore, many of the signaling pathways activated by this subset of receptors are similar (12, 33), allowing for the possibility that these receptors subserve functionally redundant roles. In this regard, it is of note that striking similarities between the renal effects of PGE2 and PGF2alpha exist. Similar to PGE2, intrarenal infusion of PGF2alpha is associated with natriuresis and diuresis, without altering glomerular filtration rate or renal hemodynamics (50). Furthermore, basolateral addition of either PGF2alpha or PGE2 can antagonize ADH-stimulated water absorption in microperfused collecting ducts (43). Nonetheless, because PGF2alpha potently activates both prostaglandin FP and EP3 receptors (1, 31), it is difficult to attribute these renal affects specifically to activation of the FP receptor. Furthermore, we are unaware of any published studies examining the renal effects of FP receptor-selective agonists. For these reasons, it is important that the present studies now demonstrate segmental expression of FP receptor mRNA along the mouse nephron.

The present studies used both in situ hybridization and a beta -gal reporter knocked into the endogenous FP locus (47) to map the distribution of the FP receptor. FP receptor expression determined using these two different techniques was mutually supportive. In the kidney, the most intense labeling was detected over a subpopulation of cells in the cortex. The mouse FP receptor mRNA was most abundant in distal nephron segments colabeling with antibodies to the TSC1 and the vasopressin-stimulated water channel AQP2. In mice, TSC1 is expressed only in the DCT, where it mediates NaCl absorption (15). FP receptor activation could inhibit salt absorption in this nephron segment, thereby contributing to the natriuretic effects of PGF2alpha . The DCT is also a major site of calcium absorption (32, 38), so it is also conceivable that PGF2alpha plays a role in modulating Ca2+ absorption by the kidney. Similarly, the detection of the FP receptor in AQP2-immunoreactive cells demonstrates its expression in the collecting duct (20, 21), representing another site where its activation could contribute to PGF2alpha -induced natriuresis and diuresis.

Although the presence of low levels of FP mRNA in the thick ascending limb cannot be excluded, it seems clear that the expression of FP transcripts in the thick ascending limb is markedly less than in either the DCT or cortical collecting duct (CCD). Interestingly, there appears to be a gradient for the intensity of FP gene expression along the distal tubule, with greater levels of expression in the DCT/connecting tubule, > CCD >>MCD. This is in contrast to EP3 mRNA, which is more abundant in medullary CD than CCD and expressed in mTAL as well (9, 11, 45). Finally, the EP1 receptor is most abundant in the papillary collecting duct (25, 45). This axial heterogeneity of the prostanoid receptors is consistent with a major role for PGF2alpha action in the renal cortex as opposed to the medulla, where PGE2 action may predominate.

The cellular effects of the FP receptor in distal renal epithelia remain uncharacterized. In fibroblasts, smooth muscle cells, or cells transfected with the FP receptor, PGF2alpha activates a signaling pathway coupled to increased cell calcium and phosphatidylinositol hydrolysis (3, 23, 24). A similar signaling pathway is activated by the EP1 receptor in the collecting duct, and this signaling pathway contributes the capacity of PGE2 to inhibit vasopressin-stimulated water flow and sodium absorption (19, 25, 27). Activation of a Ca2+-coupled signaling pathway by the FP receptor in the collecting duct could therefore contribute to natriuresis and diuresis caused by PGF2alpha infusion. Other studies in transfected cells show that the FP receptor can activate a beta -catenin-coupled signaling pathway (18), however, the significance of this pathway in differentiated renal epithelial is uncharacterized. Alternatively, of the known prostanoid receptors, the FP receptor protein sequence is most closely related to the EP3 receptor (37) that preferentially couples to Gi and inhibits vasopressin-stimulated cAMP generation and water flow via this pertussis toxin-sensitive mechanism (25, 27, 41). Additional studies will be required to determine which, if any of these pathways, is activated by the FP receptor in these nephron segments.

As previously reported, beta -gal expression was abundant in ovarian corpus luteum where FP activation appears to play a critical role in parturition, initiating the perinatal decline in progesterone secretion (47). The expression of beta -gal in corpora luteal cells provides additional validation for concordance of beta -gal expression with FP mRNA expression since abundant expression FP mRNA has been demonstrated in corpora lutea of mice by both techniques (44, 47). FP receptor is also expressed in uterine smooth muscle (6), consistent with the present studies demonstrating beta -gal in this tissue. Robust beta -gal activity was also detected along the male genital tract, particularly in the epithelia lining the lumen of the epididymis and vas deferens. Because the epididymis possesses endogenous beta -gal activity (17, 22) detected in the wild type (not shown), the significance of staining in this segment of the male genital tract remains uncertain. In contrast, we did not detect beta -gal activity in wild-type testis, so FP recetor could be expressed in this tissue and its activation contributes to previous reports that in vivo administration of PGF2alpha to mice causes atrophy of epididymal epithelium (39).

beta -Gal expression was not apparent in hepatocytes, despite reported effects of PGF2alpha on hepatic glucose output (34), consistent with the possibility of an unrelated receptor or pharmacological target for PGF2alpha in mediating these effects. Interestingly, intense expression of beta -gal activity was observed in hepatic vasculature, where it could mediate the capacity of PGF2alpha to induce nitric oxide-dependent vasodilatation (4). Finally, the present studies also identified a restricted pattern of FP receptor in skin, particularly in the dermal papillae. This site of expression may be important in mediating the stimulatory effect of latanaprost, an FP-selective agonist, on hair growth (29).

In summary, the present studies demonstrate high levels of expression of mRNA for the FP receptor in kidney distal tubules, including the DCT and CCD. The intrarenal distribution of FP receptor mRNA corresponds with the known effects of PGF2alpha on salt and water transport in the kidney. The FP receptor is expressed along both male and female genitourinary tracts.


    ACKNOWLEDGEMENTS

This work was funded in part by an American Heart Association fellowship award (to O. Saito), an American Diabetes Association award (to Y. F. Guan), and VA Merit Award and National Institutes of Health Grant DK-37097 (to M. D. Breyer).


    FOOTNOTES

Present address of M. Kömhoff: Dept. of Pediatrics, Philips-Univ. Marburg, Deutschhausstrasse 12, D35053 Marburg, Germany.

Address for reprint requests and other correspondence: M. D. Breyer, Division of Nephrology and Dept. of Medicine, Vanderbilt Univ., F427-ACRE Bldg., Dept. of Veterans Affairs Medical Center, Nashville, TN 37212 (E-mail: Matthew.Breyer{at}vanderbilt.edu).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

First published March 11, 2003;10.1152/ajprenal.00441.2002

Received 30 December 2002; accepted in final form 9 February 2003.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

1.   Abramovitz, M, Adam M, Boie Y, Carriere M, Denis D, Godbout C, Lamontagne S, Rochette C, Sawyer N, Tremblay NM, Belley M, Gallant M, Dufresne C, Gareau Y, Ruel R, Juteau H, Labelle M, Ouimet N, and Metters KM. The utilization of recombinant prostanoid receptors to determine the affinities and selectivities of prostaglandins and related analogs. Biochim Biophys Acta 1483: 285-293, 2000[ISI][Medline].

2.   Abramovitz, M, Adam M, Boie Y, Grygorczyk R, Rushmore TH, Nguyen T, Funk CD, Bastien L, Sawyer N, Rochette C, Slipetz DM, and Metters KM. Human prostanoid receptors: cloning and characterization. Adv Prostaglandin Thromboxane Leukot Res 23: 499-504, 1995[ISI][Medline].

3.   Abramovitz, M, Boie Y, Nguyen T, Rushmore TH, Bayne MA, Metters KM, Slipetz DM, and Grygorczyk R. Cloning and expression of a cDNA for the human prostanoid FP receptor. J Biol Chem 269: 2632-2636, 1994[Abstract/Free Full Text].

4.   Astin, M, and Stjernschantz J. Mechanism of prostaglandin E2-, F2alpha - and latanoprost acid-induced relaxation of submental veins. Eur J Pharmacol 340: 195-201, 1997[ISI][Medline].

5.   Ave, P, Colucci-Guyon E, Babinet C, and Huerre MR. An improved method to detect beta -galactosidase activity in transgenic mice: a post-staining procedure on paraffin embedded tissue sections. Transgenic Res 6: 37-40, 1997[ISI][Medline].

6.   Baguma-Nibasheka, M, Wentworth RA, Green LR, Jenkins SL, and Nathanielsz PW. Differences in the in vitro sensitivity of ovine myometrium and mesometrium to oxytocin and prostaglandins E2 and F2alpha . Biol Reprod 58: 73-78, 1998[Abstract].

7.   Breyer, MD, and Breyer RM. Prostaglandin E receptors and the kidney. Am J Physiol Renal Physiol 279: F12-F23, 2000[Abstract/Free Full Text].

8.   Breyer, MD, and Breyer RM. G protein-coupled prostanoid receptors and the kidney. Annu Rev Physiol 63: 579-605, 2001[ISI][Medline].

9.   Breyer, MD, Davis L, Jacobson HR, and Breyer RM. Differential localization of prostaglandin E receptor subtypes in human kidney. Am J Physiol Renal Fluid Electrolyte Physiol 270: F912-F918, 1996[Abstract/Free Full Text].

10.   Breyer, MD, and Harris RC. Cyclooxygenase 2 and the kidney. Curr Opin Nephrol Hypertens 10: 89-98, 2001[ISI][Medline].

11.   Breyer, MD, Jacobson HR, Davis LS, and Breyer RM. In situ hybridization and localization of mRNA for the rabbit prostaglandin EP3 receptor. Kidney Int 44: 1372-1378, 1993[ISI][Medline].

12.   Breyer, RM, Bagdassarian CK, Myers SA, and Breyer MD. Prostanoid receptors: subtypes and signaling. Annu Rev Pharmacol Toxicol 41: 661-690, 2001[ISI][Medline].

13.   Breyer, RM, Emeson RB, Breyer MD, Abromson RM, Davis LS, and Ferrenbach SM. Alternative splicing generates multiple isoforms of a rabbit prostaglandin E2 receptor. J Biol Chem 298: 6163-6169, 1994.

14.   Campbell, WB, Holland OB, Adams BV, and Gomez-Sanchez CE. Urinary excretion of prostaglandin E2, prostaglandin F2alpha , and thromboxane B2 in normotensive and hypertensive subjects on varying sodium intakes. Hypertension 4: 735-741, 1982[ISI][Medline].

15.   Campean, V, Kricke J, Ellison D, Luft FC, and Bachmann S. Localization of thiazide-sensitive Na+-Cl- cotransport and associated gene products in mouse DCT. Am J Physiol Renal Physiol 281: F1028-F1035, 2001[Abstract/Free Full Text].

16.   Cheng, Y, Austin SC, Rocca B, Koller BH, Coffman TM, Grosser T, Lawson JA, and FitzGerald GA. Role of prostacyclin in the cardiovascular response to thromboxane A2. Science 296: 539-541, 2002[Abstract/Free Full Text].

17.   Cossu, G, and Boitani C. Lactosaminoglycans synthesized by mouse male germ cells are fucosylated by an epididymal fucosyltransferase. Dev Biol 102: 402-408, 1984[ISI][Medline].

18.   Fujino, H, and Regan JW. Fp prostanoid receptor activation of a t-cell factor/beta -catenin signaling pathway. J Biol Chem 276: 12489-12492, 2001[Abstract/Free Full Text].

19.   Funk, C, Furchi L, FitzGerald G, Grygorczyk R, Rochette C, Bayne MA, Abramovitz M, Adam M, and Metters KM. Cloning and expression of a cDNA for the human prostaglandin E receptor EP1 subtype. J Biol Chem 268: 26767-26772, 1993[Abstract/Free Full Text].

20.   Fushimi, K, Sasaki S, Yamamoto T, Hayashi M, Furukawa T, Uchida S, Kuwahara M, Ishibashi K, Kawasaki M, Kihara I, and Marumo F. Functional characterization and cell immunolocalization of AQP-CD water channel in kidney collecting duct. Am J Physiol Renal Fluid Electrolyte Physiol 267: F573-F582, 1994[Abstract/Free Full Text].

21.   Fushimi, K, Uchida S, Hara Y, Hirata Y, Marumo F, and Sasaki S. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361: 549-552, 1993[ISI][Medline].

22.   Gossrau, R. Histochemical demonstration of beta -glucuronidase, alpha -mannosidase and alpha -galactosidase using 1-naphthyl glycosides (author's transl). Histochemie 36: 367-381, 1973[ISI][Medline].

23.   Griffin, BW, Magnino PE, Pang IH, and Sharif NA. Pharmacological characterization of an FP prostaglandin receptor on rat vascular smooth muscle cells (A7r5) coupled to phosphoinositide turnover and intracellular calcium mobilization. J Pharmacol Exp Ther 286: 411-418, 1998[Abstract/Free Full Text].

24.   Griffin, BW, Williams GW, Crider JY, and Sharif NA. FP prostaglandin receptors mediating inositol phosphates generation and calcium mobilization in Swiss 3T3 cells: a pharmacological study. J Pharmacol Exp Ther 281: 845-854, 1997[Abstract/Free Full Text].

25.   Guan, Y, Zhang Y, Breyer RM, Fowler B, Davis L, Hebert RL, and Breyer MD. Prostaglandin E2 inhibits renal collecting duct Na+ absorption by activating the EP1 receptor. J Clin Invest 102: 194-201, 1998[Abstract/Free Full Text].

26.   Hayashi, M, Sasaki S, Tsuganezawa H, Monkawa T, Kitajima W, Konishi K, Fushimi K, Marumo F, and Saruta T. Role of vasopressin V2 receptor in acute regulation of aquaporin-2. Kidney Blood Press Res 19: 32-37, 1996[ISI][Medline].

27.   Hebert, RL, Jacobson HR, Fredin D, and Breyer MD. Evidence that separate PGE2 receptors modulate water and sodium transport in rabbit cortical collecting duct. Am J Physiol Renal Fluid Electrolyte Physiol 265: F643-F650, 1993[Abstract/Free Full Text].

28.   Hoyer, JR, Sisson SP, and Vernier RL. Tamm-Horsfall glycoprotein: ultrastructural immunoperoxidase localization in rat kidney. Lab Invest 41: 168-173, 1979[ISI][Medline].

29.   Johnstone, MA, and Albert DM. Prostaglandin-induced hair growth. Surv Ophthalmol 47, Suppl1: S185-S202, 2002[ISI][Medline].

30.   Kim, GH, Masilamani S, Turner R, Mitchell C, Wade JB, and Knepper MA. The thiazide-sensitive Na-Cl cotransporter is an aldosterone-induced protein. Proc Natl Acad Sci USA 95: 14552-14557, 1998[Abstract/Free Full Text].

31.   Kiriyama, M, Ushikubi F, Kobayashi T, Hirata M, Sugimoto Y, and Narumiya S. Ligand binding specificities of the eight types and subtypes of the mouse prostanoid receptors expressed in Chinese hamster ovary cells. Br J Pharmacol 122: 217-224, 1997[Abstract].

32.   Loffing, J, Loffing-Cueni D, Valderrabano V, Klausli L, Hebert SC, Rossier BC, Hoenderop JG, Bindels RJ, and Kaissling B. Distribution of transcellular calcium and sodium transport pathways along mouse distal nephron. Am J Physiol Renal Physiol 281: F1021-F1027, 2001[Abstract/Free Full Text].

33.   Narumiya, S, Sugimoto Y, and Ushikubi F. Prostanoid receptors: structures, properties, and functions. Physiol Rev 79: 1193-1226, 1999[Abstract/Free Full Text].

34.   Puschel, GP, Miura H, Neuschafer-Rube F, and Jungermann K. Inhibition by the protein kinase C activator 4beta -phorbol 12-myristate 13-acetate of the prostaglandin F2alpha -mediated and noradrenaline-mediated but not glucagon-mediated activation of glycogenolysis in rat liver. Eur J Biochem 217: 305-311, 1993[Abstract].

35.   Rathaus, M, Bernheim J, Katz D, Green J, and Podjarny E. Effect of sodium and chloride depletion on urinary prostaglandin F2alpha excretion in potassium loaded rats. Prostaglandins Leukot Essent Fatty Acids 46: 277-282, 1992[ISI][Medline].

36.   Robert, B, St John PL, and Abrahamson DR. Direct visualization of renal vascular morphogenesis in Flk1 heterozygous mutant mice. Am J Physiol Renal Physiol 275: F164-F172, 1998[Abstract/Free Full Text].

37.   Sakamoto, K, Ezashi T, Miwa K, Okuda-Ashitaka E, Houtani T, Sugimoto T, Ito S, and Hayaishi O. Molecular cloning and expression of a cDNA of the bovine prostaglandin F2alpha receptor. Adv Prostaglandin Thromboxane Leukot Res 23: 259-261, 1995[ISI][Medline].

38.   Shimizu, T, Yoshitomi K, Nakamura M, and Imai M. Effects of PTH, calcitonin, and cAMP on calcium transport in rabbit distal nephron segments. Am J Physiol Renal Fluid Electrolyte Physiol 259: F408-F414, 1990[Abstract/Free Full Text].

39.   Singh, SK, and Dominic CJ. Prostaglandin F2alpha -induced changes in the sex organs of the male laboratory mouse. Exp Clin Endocrinol 88: 309-315, 1986[ISI][Medline].

40.   Siragy, HM, and Carey RM. The subtype 2 angiotensin receptor regulates renal prostaglandin F2alpha formation in conscious rats. Am J Physiol Regul Integr Comp Physiol 273: R1103-R1107, 1997[Abstract/Free Full Text].

41.   Sonnenburg, WK, Zhu J, and Smith WL. A prostglandin E receptor coupled to a pertussis toxin-sensitive guanine nucleotide regulatory protein in rabbit cortical collecting tubule cells. J Biol Chem 265: 8479-8483, 1990[Abstract/Free Full Text].

42.   Stier, CT, Jr, Roberts LJ, II, and Wong PY. Renal response to 9alpha , 11beta -prostaglandin F2 in the rat. J Pharmacol Exp Ther 243: 487-491, 1987[Abstract].

43.   Stokes, JB. Modulation of vasopressin-induced water permeability of the cortical collecting tubule by endogenous and exogenous prostaglandins. Miner Electrolyte Metab 11: 240-248, 1985[ISI][Medline].

44.   Sugimoto, Y, Hasumoto K, Namba T, Irie A, Katsuyama M, Negishi M, Kakizuka A, Naumiya S, and Ichikawa A. Cloning and expression of a cDNA for mouse prostaglandin F receptor. J Biol Chem 269: 1356-1360, 1994[Abstract/Free Full Text].

45.   Sugimoto, Y, Namba T, Shigemoto R, Negishi M, Ichikawa A, and Narumiya S. Distinct cellular localization of mRNAs for three subtypes of prostaglandin E receptor in kidney. Am J Physiol Renal Fluid Electrolyte Physiol 266: F823-F828, 1994[Abstract/Free Full Text].

46.   Sugimoto, Y, Narumiya S, and Ichikawa A. Distribution and function of prostanoid receptors: studies from knockout mice. Prog Lipid Res 39: 289-314, 2000[ISI][Medline].

47.   Sugimoto, Y, Yamasaki A, Segi E, Tsuboi K, Aze Y, Nishimura T, Oida H, Yoshida N, Tanaka T, Katsuyama M, Hasumoto K, Murata T, Hirata M, Ushikubi F, Negishi M, Ichikawa A, and Narumiya S. Failure of parturition in mice lacking the prostaglandin F receptor. Science 277: 681-683, 1997[Abstract/Free Full Text].

48.   Tosun, M, Paul RJ, and Rapoport RM. Intracellular Ca2+ elevation and contraction due to prostaglandin F2alpha in rat aorta. Eur J Pharmacol 340: 203-208, 1997[ISI][Medline].

49.   Zhu, X, Cheng J, Gao J, Lepor H, Zhang ZT, Pak J, and Wu XR. Isolation of mouse THP gene promoter and demonstration of its kidney- specific activity in transgenic mice. Am J Physiol Renal Physiol 282: F608-F617, 2002[Abstract/Free Full Text].

50.   Zook, TE, and Strandhoy JW. Mechanisms of the natriuretic and diuretic effects of prostaglandin F2alpha . J Pharmacol Exp Ther 217: 674-680, 1981[Abstract].


Am J Physiol Renal Fluid Electrolyte Physiol 284(6):F1164-F1170




This Article
Abstract
Full Text (PDF)
All Versions of this Article:
284/6/F1164    most recent
00441.2002v1
Alert me when this article is cited
Alert me if a correction is posted
Citation Map
Services
Email this article to a friend
Similar articles in this journal
Similar articles in ISI Web of Science
Similar articles in PubMed
Alert me to new issues of the journal
Download to citation manager
Search for citing articles in:
ISI Web of Science (2)
Google Scholar
Articles by Saito, O.
Articles by Breyer, M. D.
Articles citing this Article
PubMed
PubMed Citation
Articles by Saito, O.
Articles by Breyer, M. D.


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Visit Other APS Journals Online
Copyright © 2003 by the American Physiological Society.