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作者：OsamuSaito, YoufeiGuan, ZhonghuaQi, Linda S.Davis, MartinKömhoff, YukihikoSugimoto, ShuhNarumiya, Richard M.Breyer, Matthew D.Breyer作者单位：1 Division of Nephrology, Department of Medicine, VanderbiltUniversity Veterans Affairs Medical Center, Nashville, Tennessee 37212;and Departments of Pharmacology, Faculty of Medicine, and Physiological Chemistry and Faculty of PharmaceuticalSciences, Kyoto University, Kyoto, Japan 606
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【摘要】- ~# k/ L; ]0 E4 v( k5 \
PGF 2 is one of the majorprostanoids produced by the kidney. The cellular effects ofPGF 2 are mediated by a G protein-coupled transmembranereceptor designated the FP receptor. Both in situ hybridization and -galactosidase knocked into the endogenous FP locus were used todetermine the cellular distribution of the mouse FP receptor. Specificlabeling was detected in the kidney, ovary, and uterus. Abundant FPexpression in ovarian follicles and uterus is consistent with previousreports of failed parturition in FP / mice. In the kidney,coexpression of the mFP mRNA with the thiazide-sensitive cotransporterdefined its expression in the distal convoluted tubule (DCT). FPreceptor was also present in aquaporin-2-positive cortical collectingducts (CCD). No FP mRNA was detected in glomeruli, proximal tubules, orthick ascending limbs. Intrarenal expression of the FP receptor in theDCT and CCD suggests an important role for the FP receptor regulating water and solute transport in these segments of the nephron.
- h9 p# K' F' X0 @; R 【关键词】 dinoprost nephron natriuresis water* X. R5 {4 _; H+ T$ D/ E4 s' H
INTRODUCTION
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PROSTANOIDS, including PGE 2, PGD 2, prostacyclin(PGI 2 ), TxA 2, and PGF 2, modulatea diverse spectrum of physiological processes, including reproduction,inflammation, microvascular resistance, and epithelial ion transportrates ( 7, 33 ). Despite originating from a commonprecursor, PGH 2, the effects of these derivativeprostanoids may either oppose each other, as in the case of theprothrombotic action of TxA 2 vs. the antithrombotic effectsof PGI 2 ( 16 ), or exert functionallycomplementary effects such as the smooth muscle constrictor effects ofTxA 2 and PGF 2 ( 48 ). Thesecellular and physiological effects are mediated by the selectiveinteraction of each prostanoid with unique G protein-coupled receptors(GPCRs) ( 8, 33, 46 ). Genetic disruption of GPCR prostanoidreceptors has not only firmly established roles for these receptors ascritical mediators of prostanoid action, but it also revealedsignificant new biology related to the roles of prostaglandins( 33, 46 ). In the case of the FP receptor forPGF 2, these studies revealed that the FP receptor ishighly expressed in the ovary and its function is essential for normalparturition ( 47 ).
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The FP receptor is also highly expressed in the kidney ( 2, 44 ). Furthermore, PGF 2 is a major product ofcyclooxygenase-mediated arachidonate metabolism in the kidney( 14 ), and renal synthesis of PGF 2 isregulated by sodium depletion, potassium depletion, and adrenalsteroids ( 35, 40 ). Infusion of exogenousPGF 2 modulates renal salt excretion and urine flow( 42 ). Despite this evidence supporting a role for the FPreceptor in the kidney, the intrarenal sites of expression or mechanismof these PGF 2 -activated GPCRs in the kidney remainpoorly characterized. The purpose of the present studies was to map theintrarenal distribution of the FP receptor in the kidney.3 B* K' x b' w! j: C
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$ f+ ^2 Q7 e7 C! B# {Generation of RNA fragments. RNA probes were generated by RT-PCR to amplify a 399-bp fragmentspanning the 5'-UTR to Arg 100 in the coding region of themouse FP receptor cDNA from kidney RNA. The sense primer was5'-AACCACTCAGTGGCTCAGGA-3', and the antisense primer was5'-GCGGATCCAGTCTTTATC3'. The identity of the amplified product wasdirectly confirmed by sequencing and alignment with the mouse FPreceptor (BLAST, NCBI) and ligated into the transcription vector pCR2.1(Invitrogen). The two distinct clones were isolated, which allowedtranscription of either the sense or antisense cDNAs using the T7promoter. The plasmids were linearized and RNAs transcribed from theflanking T7 promoter in the presence of [ - 35 S]UTP. RNA(5 × 10 5 cpm/µl) was used for in situ hybridization.
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5 x6 M1 i+ _* \8 D# x3 W9 ITissue preparation. C57BL/6J mice weighing between 20 and 30 g were anesthetized usingintraperitoneal ketamine and xylazine (200 mg and 15 mg/kg, respectively). After surgical anesthesia was achieved, mice were killedby cervical dislocation and kidney, stomach, liver, ovary, and uteruswere harvested.! A7 }, A3 O3 \2 K/ I
8 [3 o" ^3 o/ w. ^( ]+ \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, refixedin paraformaldehyde, treated with proteinase K (20 µg/ml), washedwith PBS, refixed in 4% paraformaldehyde, and treated with triethanolamine plus acetic anhydride (0.25% vol/vol). Finally, sections were dehydrated in 100% ethanol.
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) l+ @, f5 |3 W3 w K1 h) wAnti-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 -mercaptoethanol for 30 min. This was followed by a wash in 50%formamide, 2× SSC, and 100 mM -mercaptoethanol for 60 min. Afteradditional washes in 10 mM TRIS, 5 mM EDTA, 500 mM NaCl (TEN), sectionswere treated with RNase (10 µg/ml), at 37°C for 30 min, followed byanother 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.
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& `( ]8 t( d/ N7 TFor detection of the hybridized probe, slides were dipped in photoemulsion (Ilford K5, Knutsford, UK) diluted 1:1 with 2% glycerol/waterand exposed for 7 days at 4°C. After development in Kodak D19, slideswere counterstained with hematoxylin and eosin. Photomicrographs weretaken using a Zeiss Axioskop using both bright- and darkfield optics.
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, ~( H- S+ ~* w+ KPreparation of tissue for -galactosidase staining andimmunohistochemistry. Multiple organs including liver, spleen, stomach, duodenum, lung, andkidneys of the double transgenic mice were harvested at death. Afterfixation with 4% paraformaldehyde plus 0.25% glutaraldehyde in PBSfor 2 h at 4°C, tissue sections were cut with a vibratome into200-µm slices. To detect -galactosidase ( -gal) activity, theseslices were bathed in permeabilization solution (2 mMMgCl 2, 0.01% sodium deoxycholate, 0.02% NP-40 in PBS) for30 min × 2 and then stained with 1 mg/ml5-bromo-4-chloro-3-indolyl- D -galactopyranoside (X-gal;Sigma, St. Louis, MO) in staining solution (2 mM MgCl 2, 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.- q1 K1 q' M3 p7 g: K0 a1 p
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Immunostaining. To define the nephron segments that expressed FP receptor mRNA, in situhybridization was followed by immunostaining of the tissue sectionswith a rabbit anti-collecting duct antibody or a goat anti-humanTamm-Horsfall antibody, which specifically recognizes medullary andcortical thick ascending limb (mTAL and cTAL) as well as the earlyportion of the distal tubule. To define the -gal-positive nephronsegments, sections were co-stained using a goat anti-humanTamm-Horsfall antibody (1:2,500, Organon-Technika) that specificallyrecognizes mTAL and cTAL as well as the early portion of the distaltubule ( 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), ananti-thiazide-sensitive NaCl cotransporter (TSC) antibody was used[generously provided by Dr. M. Knepper ( 30 )]. Stainingwas localized using a biotinylated anti-IgG secondary antibody appliedto -gal-stained sections. Biotin was identified using streptavidincoupled to horseradish peroxidase and was visualized withdiaminiobenzidine (Vector Vectastain ABC kit). Sections were viewed andimaged with a Zeiss Axioskop and Spot-Cam digital camera (diagnostic instruments).3 s- p! V: j' Q! J A) _
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' A: W D+ ?- k: V/ F8 w% R/ ^1 C& MIntrarenal distribution of the FP receptor. Autoradiograms of the kidney, with an anti-sense FP receptor riboprobe(Fig. 1 ), showed intense labeling ofsubpopulations of epithelial tubules in the renal cortex. Nospecific labeling was obtained with a sense mRNA probe (data notshown). There was light and diffuse labeling of the outer medulla.There was no detectable labeling of the papilla. A similar pattern ofFP mRNA expression was obtained by mapping -gal activity inheterozygous FP / mice (Fig. 1 B ).! W4 i) T+ w' J
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Fig. 1. Expression of FP receptor mRNA in kidney. A :×10 darkfield photomicrograph of an in situ hybridization using themouse FP receptor mRNA as a riboprobe. The white grains indicate areasof message expression that predominate in the cortex. B :×50 photomicrograph of a kidney from an FP / mouse. The bluereaction product identifies structures in which -galactosidaseactivity is present in cells, marking active transcription of the lacZgene knocked into the endogenous FP receptor locus inmice. [* `5 ?. v, S R1 j- Z& K! O
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Segmental expression of the mFP receptor was most abundant intubules that colabeled with antibodies to the TSC- and AQP2 antibody(collecting duct specific)-positive tubules. There was no evidence forhybridization of the FP antisense fragment to either proximalstraight tubules or thick ascending limb (Fig. 2 ). No labeling of papillary or innermedullary structures was observed.
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1 W+ X5 w& A2 ^) E& YFig. 2. Localization of FP receptor mRNA in kidney by -galactosidase staining and in situ hybridization. Coimmunostainingusing segment-specific antibodies was performed. For in situhybridization, panels show tangential illumination combined withbrightfield illumination of a mouse kidney section where the whitegrains depict sites of FP receptor riboprobe hybridization. Segmentsexpressing -galactosidase driven by the endogenous FP promoter areidentified by the blue reaction product. Thiazide-sensitivecotransporter (TSC) immunoreactivity, characteristic for the distalconvoluted tubule (DCT), colocalizes with either white grains or -galactosidase, indicating expression of FP receptor mRNA in DCT.Tamm-Horsfall (TH) immunoreactivity, restricted to the thick ascendinglimb (TAL), does not colocalize with FP receptor mRNA and TH-positiveTAL, whereas the FP receptor is expressed in TH-negative tubules.Aquaporin-2 (AQP2) specifically labels the collecting duct andcolocalizes with FP receptor mRNA expressed in AQP-positivetubules.: X% s2 A7 k. ?: l: R6 E8 ~
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Extrarenal tissues. Abundant -gal expression was detected in stromal surrounding theureteral smooth muscle (Fig. 3 ).Epididymus possesses endogenous -gal activity in control animals,complicating the interpretation of this tissues. However, thisendogenous activity was not present in any other organs from wild-typeanimals examined including the distal vas deferens and luminal cells ofthe testis where low levels of -gal activity were detected. In thefemale genital tract, -gal expression was detected in ovary corporaluteal cells and the smooth muscle cells lining the fallopian tubuleand uterus. Patches of intense -gal labeling in tissues obtainedfrom FP / mice were associated with dermal hair follicles.Liver failed to show any -gal staining in hepatocytes, however,labeling of vascular tissue was detected.
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Fig. 3. -Galactosidase expression in FP-lacZ knocked intotissues: ureter, testis, uterus, ovary, skin, and liver.
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The kidney is a site of robust prostaglandin synthesis andexpresses abundant prostanoid receptors ( 8, 10, 46 ). Renal expression of the FP, EP 1, EP 3, and TP receptormRNAs is particularly high ( 13, 25, 46 ). Furthermore, manyof the signaling pathways activated by this subset of receptors aresimilar ( 12, 33 ), allowing for the possibility that thesereceptors subserve functionally redundant roles. In this regard, it isof note that striking similarities between the renal effects ofPGE 2 and PGF 2 exist. Similar toPGE 2, intrarenal infusion of PGF 2 isassociated with natriuresis and diuresis, without altering glomerularfiltration rate or renal hemodynamics ( 50 ). Furthermore,basolateral addition of either PGF 2 or PGE 2 can antagonize ADH-stimulated water absorption in microperfusedcollecting ducts ( 43 ). Nonetheless, because PGF 2 potently activates both prostaglandin FP andEP 3 receptors ( 1, 31 ), it is difficult toattribute these renal affects specifically to activation of the FPreceptor. Furthermore, we are unaware of any published studiesexamining the renal effects of FP receptor-selective agonists. Forthese reasons, it is important that the present studies now demonstratesegmental expression of FP receptor mRNA along the mouse nephron.
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- @& a8 x0 C! `+ ^The present studies used both in situ hybridization and a -galreporter 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 thekidney, the most intense labeling was detected over a subpopulation ofcells in the cortex. The mouse FP receptor mRNA was most abundant indistal nephron segments colabeling with antibodies to the TSC1 and thevasopressin-stimulated water channel AQP2. In mice, TSC1 is expressedonly in the DCT, where it mediates NaCl absorption ( 15 ).FP receptor activation could inhibit salt absorption in this nephronsegment, thereby contributing to the natriuretic effects ofPGF 2. The DCT is also a major site of calcium absorption( 32, 38 ), so it is also conceivable thatPGF 2 plays a role in modulating Ca 2 absorption by the kidney. Similarly, the detection of the FP receptorin AQP2-immunoreactive cells demonstrates its expression in thecollecting duct ( 20, 21 ), representing another site whereits activation could contribute to PGF 2 -inducednatriuresis and diuresis.
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' s R4 e. {0 o- {, g) d5 jAlthough the presence of low levels of FP mRNA in the thick ascendinglimb cannot be excluded, it seems clear that the expression of FPtranscripts in the thick ascending limb is markedly less than in eitherthe DCT or cortical collecting duct (CCD). Interestingly, there appearsto be a gradient for the intensity of FP gene expression along thedistal tubule, with greater levels of expression in MCD. This is in contrast to EP 3 mRNA,which is more abundant in medullary CD than CCD and expressed in mTALas well ( 9, 11, 45 ). Finally, the EP 1 receptoris most abundant in the papillary collecting duct ( 25, 45 ). This axial heterogeneity of the prostanoid receptors is consistent with a major role for PGF 2 action in therenal cortex as opposed to the medulla, where PGE 2 actionmay predominate., g6 F7 r0 x7 B/ V% B
/ w' r' r" @; k" y5 i. dThe cellular effects of the FP receptor in distal renal epitheliaremain uncharacterized. In fibroblasts, smooth muscle cells, or cellstransfected with the FP receptor, PGF 2 activates asignaling pathway coupled to increased cell calcium andphosphatidylinositol hydrolysis ( 3, 23, 24 ). A similarsignaling pathway is activated by the EP 1 receptor in thecollecting duct, and this signaling pathway contributes the capacity ofPGE 2 to inhibit vasopressin-stimulated water flow andsodium absorption ( 19, 25, 27 ). Activation of aCa 2 -coupled signaling pathway by the FP receptor in thecollecting duct could therefore contribute to natriuresis and diuresiscaused by PGF 2 infusion. Other studies in transfectedcells show that the FP receptor can activate a -catenin-coupledsignaling pathway ( 18 ), however, the significance of thispathway in differentiated renal epithelial is uncharacterized.Alternatively, of the known prostanoid receptors, the FP receptorprotein sequence is most closely related to the EP3 receptor( 37 ) that preferentially couples to Gi and inhibitsvasopressin-stimulated cAMP generation and water flow via thispertussis toxin-sensitive mechanism ( 25, 27, 41 ).Additional studies will be required to determine which, if any of thesepathways, is activated by the FP receptor in these nephron segments.
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As previously reported, -gal expression was abundant in ovariancorpus luteum where FP activation appears to play a critical role inparturition, initiating the perinatal decline in progesterone secretion( 47 ). The expression of -gal in corpora luteal cells provides additional validation for concordance of -gal expression with FP mRNA expression since abundant expression FP mRNA has beendemonstrated in corpora lutea of mice by both techniques ( 44, 47 ). FP receptor is also expressed in uterine smooth muscle ( 6 ), consistent with the present studiesdemonstrating -gal in this tissue. Robust -gal activity was alsodetected along the male genital tract, particularly in the epithelialining the lumen of the epididymis and vas deferens. Because theepididymis possesses endogenous -gal activity ( 17, 22 )detected in the wild type (not shown), the significance of staining inthis segment of the male genital tract remains uncertain. In contrast,we did not detect -gal activity in wild-type testis, so FP recetorcould be expressed in this tissue and its activation contributes to previous reports that in vivo administration of PGF 2 tomice causes atrophy of epididymal epithelium ( 39 ).% ?4 m8 K0 `0 V3 }' G
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-Gal expression was not apparent in hepatocytes, despite reportedeffects of PGF 2 on hepatic glucose output( 34 ), consistent with the possibility of an unrelatedreceptor or pharmacological target for PGF 2 in mediatingthese effects. Interestingly, intense expression of -gal activitywas observed in hepatic vasculature, where it could mediate thecapacity of PGF 2 to induce nitric oxide-dependentvasodilatation ( 4 ). Finally, the present studies alsoidentified a restricted pattern of FP receptor in skin, particularly inthe dermal papillae. This site of expression may be important inmediating the stimulatory effect of latanaprost, an FP-selective agonist, on hair growth ( 29 ).
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In summary, the present studies demonstrate high levels of expressionof mRNA for the FP receptor in kidney distal tubules, including the DCTand CCD. The intrarenal distribution of FP receptor mRNA correspondswith the known effects of PGF 2 on salt and watertransport in the kidney. The FP receptor is expressed along both maleand female genitourinary tracts.% ^ Y, U& l4 q, W, b& v# m$ c, Y
( o9 M* r9 o O B5 r, eACKNOWLEDGEMENTS
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# p! M4 X# X. }2 _This work was funded in part by an American Heart Associationfellowship award (to O. Saito), an American Diabetes Association award(to Y. F. Guan), and VA Merit Award and National Institutes ofHealth Grant DK-37097 (to M. D. Breyer).- [, j/ ^- \& u8 b; i7 }1 P
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