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1,25 Dihydroxyvitamin D Amplifies Type a Natriuretic Peptide Receptor Expression and Activity in Target Cells

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1,25 Dihydroxyvitamin D Amplifies Type a Natriuretic Peptide Receptor Expression and Activity in Target Cells Articles 1,25 Dihydroxyvitamin D Amplifies Type A Natriuretic Peptide Receptor Expression and Activity in Target Cells Songcang Chen, Xi-Ping Ni, Michael H. Humphreys, and David G. Gardner Diabetes Center and Department of Medicine, University of California at San Francisco, San Francisco, California 1,25 dihydroxyvitamin D (VD) has been shown to exert a number of beneficial effects on cardiovascular function, including reduction in BP and inhibition of cardiac hypertrophy. In an effort to identify a possible mechanistic link between VD and these salutary effects, the role of VD in controlling the activity and expression of the type A natriuretic peptide receptor (NPR-A), a receptor that signals reductions in BP and suppression of cellular growth in the myocardium and vascular wall, was investigated. VD, as well as the nonhypercalcemic analogue RO-25-6760, increased NPR-A–dependent cyclic guanosine monophosphate production and NPR-A gene expression in cultured rat aortic smooth muscle cells. The increase in NPR-A expression was associated with an increase in NPR-A gene promoter activity that was critically dependent on the presence of a functional VD receptor response element located approximately 495 bp upstream from the transcription start site of the gene. This element was associated with the VD receptor/retinoid X receptor complex in vitro. Mutation of this element resulted in complete elimination of the VD-dependent induction of the NPR-A gene promoter but did not affect osmotic stimulation of the promoter. Treatment of rats with RO-25-6760 for 7 d increased the atrial natriuretic peptide–dependent excretion of sodium and cyclic guanosine monophosphate without affecting mean arterial BP or plasma calcium levels. This was associated with a twofold increase in NPR-A mRNA levels in the inner medulla. Amplification of NPR-A activity represents a plausible mechanism to account for at least some of the beneficial effects that VD exerts on cardiovascular function. J Am Soc Nephrol 16: 329–339, 2005. doi: 10.1681/ASN.2004090797 he natriuretic peptides constitute a family of closely receptor. Blockade of NPR-C has been shown to increase levels related vasoactive hormones that play an important of endogenous natriuretic peptides in circulating plasma (7). T role in the regulation of cardiovascular, renal, and en- Vitamin D is a seco-steroid that bears a number of important docrine homeostasis (1). Atrial natriuretic peptide (ANP) and similarities to hormonal ligands that act through nuclear mech- brain natriuretic peptide (BNP) are produced predominantly in anisms to control gene expression. Its most polar metabolite, the heart, whereas C-type natriuretic peptide (CNP) is pro- 1,25 dihydroxyvitamin D (VD), binds specifically and with high duced in endothelial cells of the vasculature (2), reproductive affinity to a member of the nuclear receptor gene family termed tissues (3), growth plate of long bones (4), and the central the vitamin D receptor (VDR). The liganded VDR, when com- nervous system (5). The natriuretic peptides exert their biologic plexed with its heterodimeric partner, the retinoid X receptor effects through association with specific membrane-bound re- (RXR), associates with specific regulatory elements on DNA ceptors. Natriuretic peptide receptor types A and B (NPR-A called vitamin D response elements (VDRE). One such VDRE, and NPR-B, respectively) each have a large extracellular ligand- DR3, is a direct repeat of the sequence AGGTCA separated by binding domain connected to the intracellular signaling do- a three-nucleotide spacer (AGGTCANNNAGGTCA). DR3 dis- main through a single membrane-spanning segment. The intra- plays selectivity in preferentially binding to the VDR-RXR het- cellular domain harbors a noncatalytic, kinase-like region erodimer versus other nuclear receptor dimeric complexes (8). linked to a particulate guanylyl cyclase at the carboxy terminus A number of studies have identified VD as a potentially of the molecule (1). NPR-A serves as the cognate receptor for important regulator of BP and cardiovascular homeostasis. The both ANP and BNP, whereas NPR-B binds selectively to CNP. mechanism underlying the inverse relationship between VD Most of the important physiologic activities of these peptides levels and BP is not completely understood; however, the re- seem to be mediated through activation of these guanylyl cy- cent studies of Li et al. (9) suggest that the renin-angiotensin clase–linked receptors. A third receptor subtype, NPR-C, is system may be involved. Using genetically engineered VDR thought to function largely, albeit not entirely (6), as a clearance knockout mice, they showed that these animals were hyperten- sive relative to their VDR ϩ/ϩ littermates and that this in- Received September 27, 2004. Accepted October 20, 2004. crease in BP was accompanied by apparent activation of the plasma renin-angiotensin system (RAS). Published online ahead of print. Publication date available at www.jasn.org. The data are equally supportive for an important regulatory Address correspondence to: Dr. David G. Gardner, 1109 HSW, Diabetes Center, role for VD in the heart. Rats made vitamin D–deficient display University of California at San Francisco, 3rd and Parnassus Avenue, San Francisco, CA 94143-0540. Phone: 415-476-2729; Fax: 415-564-5813; E-mail: elevations not only in BP but also in ventricular hypertrophy [email protected] (10). The former seems to be related, at least in part, to the Copyright © 2005 by the American Society of Nephrology ISSN: 1046-6673/1602-0329 330 Journal of the American Society of Nephrology J Am Soc Nephrol 16: 329–339, 2005 attendant hypocalcemia because calcium supplementation cor- of the sample and standard using a commercial antibody and rects the hypertension; however, the cardiac hypertrophy per- [125I]cGMP as tracer. sists. Subsequent studies from the same group indicated that a major component of the hypertrophy seen in vitamin D–defi- RNA Isolation and Northern Blot Analysis cient animals reflects expansion of the interstitial compartment RASM cells were plated in 10-cm dishes, cultured, and treated with in the heart (predominantly cardiac fibroblasts) with increased VD or the nonhypercalcemic vitamin D analogue RO-25-6760 (20,21) at production of extracellular matrix proteins (11). VD has been different concentrations, as indicated in the individual figure legends. shown to reduce endothelin-stimulated ANP and BNP gene Total RNA was extracted from cells using the RNeasy minikit accord- expression (markers of myocyte hypertrophy) and transcrip- ing to instructions provided by the manufacturer. Total RNA was tion in cultured neonatal rat atrial (12) and ventricular (13) denatured and separated on a gel that contained 2.2% formaldehyde, transferred to nitrocellulose filters, and hybridized to radiolabeled myocytes and to suppress the hypertrophic response to endo- cDNA as described previously (22). A 1.2-kb EcoRI fragment of the rat thelin, a well known hypertrophic agonist in the cultured ven- NPR-A cDNA was isolated from vector sequence, radiolabeled using tricular myocyte model (13). It is interesting that this suppres- the Primer-it RMT kit (Stratagene), and separated from free nucleotide sive activity seems to require structural features of the VDR using NucTrap push columns (Stratagene). The membranes were pre- that are more typically associated with the activation function hybridized for 30 min at 68°C and hybridized with 32P-labeled NPR-A of this receptor (14,15). cDNA (107 cpm/2 ml of hybridization solution) for1hat68°C in Like the liganded VDR, activated NPR-A has been shown to hybridization solution provided by Stratagene. All membranes were be both antihypertrophic and antihypertensive (16,17) in a subsequently stripped and rehybridized with a radiolabeled 1150-bp number of different model systems. In the present study, we BamHI/EcoRI fragment of 18S rDNA to permit normalization among explored the possibility that VD might exert beneficial effects samples for differences in RNA loading and/or transfer to the filter. on the cardiovascular system through NPR-A. Our findings Hybridization signal was detected by autoradiography and quantified using the NIH Image program. support this hypothesis in demonstrating that VD increases both the activity of the NPR-A protein and the expression of the NPR-A gene in cultured rat aortic smooth muscle (RASM) cells. Plasmid Constructions Ϫ1575 rat NPR-A LUC was generated by cloning 1575 bp of NPR-A 5Ј flanking sequence into BamH1/NarI sites of pFOXLUC vector as Materials and Methods described previously (23). Six of the deletion mutants were generated Materials through the use of convenient restriction sites. In each case, the 3Ј ␣ 32 [ - P]dCTP and the cyclic guanosine monophosphate (cGMP) RIA linkage used the NarI site of the pFOXLUC vector. The 5Ј linkage used kit were purchased from Perkin-Elmer Life Sciences (Boston, MA). unique restriction sites (NdeI for Ϫ1290LUC, BclI for Ϫ716LUC, HindIII ANP was obtained from Phoenix Pharmaceuticals, Inc. (Mountain for Ϫ387LUC, SstII for Ϫ273LUC, and DraII for Ϫ77LUC) for placement View, CA). RNeasy minikit was from Qiagen Inc. (Santa Clara, CA). in the polylinker of the parent vector. The shortest construct, Ϫ9LUC Primer-it RMT kit, hybridization solution, and NucTrap push columns was generated using an upstream sense oligonucleotide (5Ј-GGGGAT were purchased from Stratagene (La Jolla, CA). RO-25-6760 was pro- CCTTCTGGCACACTCCTG-3Ј) that incorporated a BamHI site at its 5Ј vided by M. Uskokovic (Roche Pharmaceuticals). Other reagents were terminus and a downstream antisense oligonucleotide (5Ј-TAGAG- obtained through standard commercial suppliers. GATAGAATGGCGCCGG-3Ј) derived from 3Ј linker sequence of pFOXLUC containing the NarI site. A PCR product of appropriate size Culture of Vascular Smooth Muscle Cells was restricted with BamHI/NarI and cloned into compatible sites of pFOXLUC. All of the deletion constructs were sequenced to confirm the Neonatal RASM cells, originally isolated by P. Lynch at the Univer- predicted structure. sity of Southern California, were obtained at passage 20 from H.
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