Abstract
We examined the spatial expression pattern of medaka fish (Oryzias latipes) soluble guanylate cyclase alpha(1) and beta(1) subunit genes, OlGCS-alpha(1) and OlGCS-beta(1), and characterized the 5'-flanking region required for expression of both genes by introducing various promoter-luciferase fusion-gene constructs into COS-1 cells and medaka fish embryos. The OlGCS-alpha(1) and OlGCS-beta(1) gene transcripts were detected in whole brain and kidney in 7-day and 9-day embryos. Primer-extension analysis demonstrated that there were no differences among various adult organs (brain, eye, kidney, ovary and testis) in the transcription start site of the OlGCS-alpha(1) and OlGCS-beta(1) genes. Neither gene contained the functional TATA box within its 5'-flanking region, and the basal promoter activity was found between nucleotides +33 and +42 in the OlGCS-alpha(1) gene and between nucleotides +146 and +155 in the OlGCS-beta(1) gene. In the assay of medaka fish embryos, the 5'-flanking region of the OlGCS-beta(1) gene exhibited lower promoter activity than that of the OlGCS-alpha(1) gene. In the experiments on dual-luciferase fusion-gene constructs, the 5'-flanking region of the OlGCS-alpha(1) gene connected to the 5'-flanking region of the OlGCS-beta(1) gene was introduced into medaka fish embryos, and the 5'-flanking regions of both subunit genes were shown to mutually influence each other's promoter activity.
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- Azam M., Gupta G., Chen W., Wellington S., Warburton D., Danziger R. S. Genetic mapping of soluble guanylyl cyclase genes: implications for linkage to blood pressure in the Dahl rat. Hypertension. 1998 Jul;32(1):149–154. doi: 10.1161/01.hyp.32.1.149. [DOI] [PubMed] [Google Scholar]
- Behrends S., Vehse K. The beta(2) subunit of soluble guanylyl cyclase contains a human-specific frameshift and is expressed in gastric carcinoma. Biochem Biophys Res Commun. 2000 Apr 29;271(1):64–69. doi: 10.1006/bbrc.2000.2596. [DOI] [PubMed] [Google Scholar]
- Budworth J., Meillerais S., Charles I., Powell K. Tissue distribution of the human soluble guanylate cyclases. Biochem Biophys Res Commun. 1999 Oct 5;263(3):696–701. doi: 10.1006/bbrc.1999.1444. [DOI] [PubMed] [Google Scholar]
- Buechler W. A., Nakane M., Murad F. Expression of soluble guanylate cyclase activity requires both enzyme subunits. Biochem Biophys Res Commun. 1991 Jan 15;174(1):351–357. doi: 10.1016/0006-291x(91)90527-e. [DOI] [PubMed] [Google Scholar]
- Caccone A., García B. A., Mathiopoulos K. D., Min G. S., Moriyama E. N., Powell J. R. Characterization of the soluble guanylyl cyclase beta-subunit gene in the mosquito Anopheles gambiae. Insect Mol Biol. 1999 Feb;8(1):23–30. doi: 10.1046/j.1365-2583.1999.810023.x. [DOI] [PubMed] [Google Scholar]
- Chiquet M., Mumenthaler U., Wittwer M., Jin W., Koch M. The chick and human collagen alpha1(XII) gene promoter--activity of highly conserved regions around the first exon and in the first intron. Eur J Biochem. 1998 Oct 15;257(2):362–371. doi: 10.1046/j.1432-1327.1998.2570362.x. [DOI] [PubMed] [Google Scholar]
- Garbers D. L., Koesling D., Schultz G. Guanylyl cyclase receptors. Mol Biol Cell. 1994 Jan;5(1):1–5. doi: 10.1091/mbc.5.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gerzer R., Böhme E., Hofmann F., Schultz G. Soluble guanylate cyclase purified from bovine lung contains heme and copper. FEBS Lett. 1981 Sep 14;132(1):71–74. doi: 10.1016/0014-5793(81)80429-2. [DOI] [PubMed] [Google Scholar]
- Giuili G., Roechel N., Scholl U., Mattei M. G., Guellaen G. Colocalization of the genes coding for the alpha 3 and beta 3 subunits of soluble guanylyl cyclase to human chromosome 4 at q31.3-q33. Hum Genet. 1993 Apr;91(3):257–260. doi: 10.1007/BF00218267. [DOI] [PubMed] [Google Scholar]
- Giuili G., Scholl U., Bulle F., Guellaën G. Molecular cloning of the cDNAs coding for the two subunits of soluble guanylyl cyclase from human brain. FEBS Lett. 1992 Jun 8;304(1):83–88. doi: 10.1016/0014-5793(92)80594-7. [DOI] [PubMed] [Google Scholar]
- Harteneck C., Koesling D., Söling A., Schultz G., Böhme E. Expression of soluble guanylyl cyclase. Catalytic activity requires two enzyme subunits. FEBS Lett. 1990 Oct 15;272(1-2):221–223. doi: 10.1016/0014-5793(90)80489-6. [DOI] [PubMed] [Google Scholar]
- Harteneck C., Wedel B., Koesling D., Malkewitz J., Böhme E., Schultz G. Molecular cloning and expression of a new alpha-subunit of soluble guanylyl cyclase. Interchangeability of the alpha-subunits of the enzyme. FEBS Lett. 1991 Nov 4;292(1-2):217–222. doi: 10.1016/0014-5793(91)80871-y. [DOI] [PubMed] [Google Scholar]
- Ito E., Toki T., Ishihara H., Ohtani H., Gu L., Yokoyama M., Engel J. D., Yamamoto M. Erythroid transcription factor GATA-1 is abundantly transcribed in mouse testis. Nature. 1993 Apr 1;362(6419):466–468. doi: 10.1038/362466a0. [DOI] [PubMed] [Google Scholar]
- Koesling D., Harteneck C., Humbert P., Bosserhoff A., Frank R., Schultz G., Böhme E. The primary structure of the larger subunit of soluble guanylyl cyclase from bovine lung. Homology between the two subunits of the enzyme. FEBS Lett. 1990 Jun 18;266(1-2):128–132. doi: 10.1016/0014-5793(90)81523-q. [DOI] [PubMed] [Google Scholar]
- Koesling D., Herz J., Gausepohl H., Niroomand F., Hinsch K. D., Mülsch A., Böhme E., Schultz G., Frank R. The primary structure of the 70 kDa subunit of bovine soluble guanylate cyclase. FEBS Lett. 1988 Oct 24;239(1):29–34. doi: 10.1016/0014-5793(88)80539-8. [DOI] [PubMed] [Google Scholar]
- Koglin M., Behrends S. Cloning and functional expression of the rat alpha(2) subunit of soluble guanylyl cyclase. Biochim Biophys Acta. 2000 Dec 1;1494(3):286–289. doi: 10.1016/s0167-4781(00)00211-6. [DOI] [PubMed] [Google Scholar]
- Koglin M., Vehse K., Budaeus L., Scholz H., Behrends S. Nitric oxide activates the beta 2 subunit of soluble guanylyl cyclase in the absence of a second subunit. J Biol Chem. 2001 Jun 13;276(33):30737–30743. doi: 10.1074/jbc.M102549200. [DOI] [PubMed] [Google Scholar]
- Kuo W. N., Kanadia R. N., Mcnabb M. Soluble guanylate cyclase in Saccharomyces cerevisiae. Biochem Mol Biol Int. 1998 Jun;45(1):125–131. doi: 10.1080/15216549800202492. [DOI] [PubMed] [Google Scholar]
- Kurtz A., Götz K. H., Hamann M., Wagner C. Stimulation of renin secretion by nitric oxide is mediated by phosphodiesterase 3. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4743–4747. doi: 10.1073/pnas.95.8.4743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leprini A., Gherzi R., Vecchi E., Borsi L., Zardi L., Siri A. Rat tenascin-R gene: structure, chromosome location and transcriptional activity of promoter and exon 1. Cytogenet Cell Genet. 1998;83(1-2):115–123. doi: 10.1159/000015146. [DOI] [PubMed] [Google Scholar]
- Lin C. S., Chow S., Lau A., Tu R., Lue T. F. Identification and regulation of human PDE5A gene promoter. Biochem Biophys Res Commun. 2001 Jan 26;280(3):684–692. doi: 10.1006/bbrc.2000.4220. [DOI] [PubMed] [Google Scholar]
- Liu H., Force T., Bloch K. D. Nerve growth factor decreases soluble guanylate cyclase in rat pheochromocytoma PC12 cells. J Biol Chem. 1997 Feb 28;272(9):6038–6043. doi: 10.1074/jbc.272.9.6038. [DOI] [PubMed] [Google Scholar]
- Lucas K. A., Pitari G. M., Kazerounian S., Ruiz-Stewart I., Park J., Schulz S., Chepenik K. P., Waldman S. A. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev. 2000 Sep;52(3):375–414. [PubMed] [Google Scholar]
- Mikami T., Kusakabe T., Suzuki N. Molecular cloning of cDNAs and expression of mRNAs encoding alpha and beta subunits of soluble guanylyl cyclase from medaka fish Oryzias latipes. Eur J Biochem. 1998 Apr 1;253(1):42–48. doi: 10.1046/j.1432-1327.1998.2530042.x. [DOI] [PubMed] [Google Scholar]
- Mikami T., Kusakabe T., Suzuki N. Tandem organization of medaka fish soluble guanylyl cyclase alpha1 and beta1 subunit genes. Implications for coordinated transcription of two subunit genes. J Biol Chem. 1999 Jun 25;274(26):18567–18573. doi: 10.1074/jbc.274.26.18567. [DOI] [PubMed] [Google Scholar]
- Nakane M., Arai K., Saheki S., Kuno T., Buechler W., Murad F. Molecular cloning and expression of cDNAs coding for soluble guanylate cyclase from rat lung. J Biol Chem. 1990 Oct 5;265(28):16841–16845. [PubMed] [Google Scholar]
- Nakane M., Saheki S., Kuno T., Ishii K., Murad F. Molecular cloning of a cDNA coding for 70 kilodalton subunit of soluble guanylate cyclase from rat lung. Biochem Biophys Res Commun. 1988 Dec 30;157(3):1139–1147. doi: 10.1016/s0006-291x(88)80992-6. [DOI] [PubMed] [Google Scholar]
- Nighorn A., Gibson N. J., Rivers D. M., Hildebrand J. G., Morton D. B. The nitric oxide-cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta. J Neurosci. 1998 Sep 15;18(18):7244–7255. doi: 10.1523/JNEUROSCI.18-18-07244.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Papapetropoulos A., Abou-Mohamed G., Marczin N., Murad F., Caldwell R. W., Catravas J. D. Downregulation of nitrovasodilator-induced cyclic GMP accumulation in cells exposed to endotoxin or interleukin-1 beta. Br J Pharmacol. 1996 Jul;118(6):1359–1366. doi: 10.1111/j.1476-5381.1996.tb15545.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Papapetropoulos A., Marczin N., Mora G., Milici A., Murad F., Catravas J. D. Regulation of vascular smooth muscle soluble guanylate cyclase activity, mRNA, and protein levels by cAMP-elevating agents. Hypertension. 1995 Oct;26(4):696–704. doi: 10.1161/01.hyp.26.4.696. [DOI] [PubMed] [Google Scholar]
- Ruetten H., Zabel U., Linz W., Schmidt H. H. Downregulation of soluble guanylyl cyclase in young and aging spontaneously hypertensive rats. Circ Res. 1999 Sep 17;85(6):534–541. doi: 10.1161/01.res.85.6.534. [DOI] [PubMed] [Google Scholar]
- Schmidt H. H., Walter U. NO at work. Cell. 1994 Sep 23;78(6):919–925. doi: 10.1016/0092-8674(94)90267-4. [DOI] [PubMed] [Google Scholar]
- Shah S., Hyde D. R. Two Drosophila genes that encode the alph and beta subunits of the brain soluble guanylyl cyclase. J Biol Chem. 1995 Jun 23;270(25):15368–15376. doi: 10.1074/jbc.270.25.15368. [DOI] [PubMed] [Google Scholar]
- Sharina I. G., Krumenacker J. S., Martin E., Murad F. Genomic organization of alpha1 and beta1 subunits of the mammalian soluble guanylyl cyclase genes. Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):10878–10883. doi: 10.1073/pnas.190331697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smale S. T. Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes. Biochim Biophys Acta. 1997 Mar 20;1351(1-2):73–88. doi: 10.1016/s0167-4781(96)00206-0. [DOI] [PubMed] [Google Scholar]
- Star R. A. Intrarenal localization of nitric oxide synthase isoforms and soluble guanylyl cyclase. Clin Exp Pharmacol Physiol. 1997 Aug;24(8):607–610. doi: 10.1111/j.1440-1681.1997.tb02100.x. [DOI] [PubMed] [Google Scholar]
- Wang Y., Goligorsky M. S., Lin M., Wilcox J. N., Marsden P. A. A novel, testis-specific mRNA transcript encoding an NH2-terminal truncated nitric-oxide synthase. J Biol Chem. 1997 Apr 25;272(17):11392–11401. [PubMed] [Google Scholar]
- Wilcox C. S., Welch W. J., Murad F., Gross S. S., Taylor G., Levi R., Schmidt H. H. Nitric oxide synthase in macula densa regulates glomerular capillary pressure. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11993–11997. doi: 10.1073/pnas.89.24.11993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamagami S., Suzuki K., Suzuki N. Expression and exon/intron organization of two medaka fish homologs of the mammalian guanylyl cyclase A. J Biochem. 2001 Jul;130(1):39–50. doi: 10.1093/oxfordjournals.jbchem.a002960. [DOI] [PubMed] [Google Scholar]
- Yu S., Avery L., Baude E., Garbers D. L. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3384–3387. doi: 10.1073/pnas.94.7.3384. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yuen P. S., Potter L. R., Garbers D. L. A new form of guanylyl cyclase is preferentially expressed in rat kidney. Biochemistry. 1990 Dec 11;29(49):10872–10878. doi: 10.1021/bi00501a002. [DOI] [PubMed] [Google Scholar]
- Zabel U., Häusler C., Weeger M., Schmidt H. H. Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione s-transferase affinity tag. J Biol Chem. 1999 Jun 25;274(26):18149–18152. doi: 10.1074/jbc.274.26.18149. [DOI] [PubMed] [Google Scholar]
- Zabel U., Weeger M., La M., Schmidt H. H. Human soluble guanylate cyclase: functional expression and revised isoenzyme family. Biochem J. 1998 Oct 1;335(Pt 1):51–57. doi: 10.1042/bj3350051. [DOI] [PMC free article] [PubMed] [Google Scholar]
