Soluble adenylyl cyclase in vascular endothelium: Gene expression control of epithelial sodium channel-α, Na+/K+-ATPase-α/β, and mineralocorticoid receptor

Hypertension

Volumn 63, Issue 4, 2014, Pages 753-761

  Schmitz, Boris ^a,b   Nedele, Johanna ^a   Guske, Katrin ^a   Maase, Martina ^a,c   Lenders, Malte ^a   Schelleckes, Michael ^a   Kusche Vihrog, Kristina ^a,c   Brand, Stefan Martin ^b   Brand, Eva ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b Institute of Sports Medicine   (United States)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

adenylyl cyclase; aldosterone; cyclic AMP response elemen Cbinding protein; vascular stiffness

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENYLATE CYCLASE; ALDOSTERONE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EPITHELIAL SODIUM CHANNEL; ISOPROTEIN; MINERALOCORTICOID RECEPTOR; PROTEIN KINASE C; SMALL INTERFERING RNA;

ANIMAL TISSUE; AORTA; ARTERIAL STIFFNESS; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; KIDNEY COLLECTING TUBULE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PULSE WAVE; TRANSCRIPTION INITIATION; VASCULAR ENDOTHELIUM;

ADENYLYL CYCLASE; ALDOSTERONE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; VASCULAR STIFFNESS;

ADENYLATE CYCLASE; ALDOSTERONE; ANIMALS; AORTA; CELL LINE; CREB-BINDING PROTEIN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENDOTHELIUM, VASCULAR; EPITHELIAL SODIUM CHANNELS; GENE EXPRESSION REGULATION; HUMANS; MICE; MODELS, ANIMAL; PHOSPHORYLATION; RECEPTORS, MINERALOCORTICOID; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SODIUM-POTASSIUM-EXCHANGING ATPASE; VASCULAR STIFFNESS;

EID: 84897063620     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.113.02061     Document Type: Article

References (46)

1. Zieman SJ, Melenovsky V, Kass DA. Mechanisms, pathophysiol-ogy, and therapy of arterial stiffness. Arterioscler Thromb Vasc Biol. 2005;25:932-943.
2. Weber T, Ammer M, Rammer M, Adji A, O'Rourke MF, Wassertheurer S, Rosenkranz S, Eber B. Noninvasive determination of carotid-femoral pulse wave velocity depends critically on assessment of travel distance: a comparison with invasive measurement. J Hypertens. 2009;27:1624-1630.
3. Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, Ducimetiere P, Benetos A. Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension. 2001;37:1236-1241.
4. Blacher J, Guerin AP, Pannier B, Marchais SJ, Safar ME, London GM. Impact of aortic stiffness on survival in end-stage renal disease. Circulation. 1999;99:2434-2439.
5. Willum-Hansen T, Staessen JA, Torp-Pedersen C, Rasmussen S, Thijs L, Ibsen H, Jeppesen J. Prognostic value of aortic pulse wave velocity as index of arterial stiffness in the general population. Circulation. 2006;113:664-670.
6. Lacolley P, Challande P, Osborne-Pellegrin M, Regnault V. Genetics and pathophysiology of arterial stiffness. Cardiovasc Res. 2009;81: 637-648.
7. Mullins LJ, Bailey MA, Mullins JJ. Hypertension, kidney, and transgen-ics: a fresh perspective. Physiol Rev. 2006;86:709-746.
8. Izzo JL Jr, Mitchell GF. Aging and arterial structure-function relations. Adv Cardiol. 2007;44:19-34.
9. Brull DJ, Murray LJ, Boreham CA, Ralston SH, Montgomery HE, Gallagher AM, McGuigan FE, Davey Smith G, Savage M, Humphries SE, Young IS. Effect of a COL1A1 Sp1 binding site polymorphism on arterial pulse wave velocity: an index of compliance. Hypertension. 2001;38:444-448.
10. Bunda S, Wang Y, Mitts TF, Liu P, Arab S, Arabkhari M, Hinek A. Aldosterone stimulates elastogenesis in cardiac fbroblasts via mineralo-corticoid receptor-independent action involving the consecutive activation of Galpha13, c-Src, the insulin-like growth factor-I receptor, and phospha-tidylinositol 3-kinase/Akt. J Biol Chem. 2009;284:16633-16647.
11. Kusche-Vihrog K, Callies C, Fels J, Oberleithner H. The epithelial sodium channel (ENaC): mediator of the aldosterone response in the vascular endothelium? Steroids. 2010;75:544-549.
12. Oberleithner H, Riethmüller C, Schillers H, MacGregor GA, de Wardener HE, Hausberg M. Plasma sodium stiffens vascular endo-thelium and reduces nitric oxide release. Proc Natl Acad Sci USA. 2007;104:16281-16286.
13. Blaustein MP, Zhang J, Chen L, Song H, Raina H, Kinsey SP, Izuka M, Iwamoto T, Kotlikoff MI, Lingrel JB, Philipson KD, Wier WG, Hamlyn JM. The pump, the exchanger and endogenous quabain: signaling mechanisms that link salt retention to hypertension. Hypertension. 2009;53:291-298.
14. Mustafa SB, Castro R, Falck AJ, Petershack JA, Henson BM, Mendoza YM, Choudary A, Seidner SR. Protein kinase A and mitogen-activated protein kinase pathways mediate cAMP induction of alpha-epithelial Na+ channels (alpha-ENaC). J Cell Physiol. 2008;215:101-110.
15. Listwak SJ, Gold PW, Whitfeld HJ Jr. The human mineralocorticoid receptor gene promoter: its structure and expression. J Steroid Biochem Mol Biol. 1996;58:495-506.
16. Dagenais A, Denis C, Vives MF, Girouard S, Massé C, Nguyen T, Yamagata T, Grygorczyk C, Kothary R, Berthiaume Y. Modulation of alpha-ENaC and alpha1-Na+-K+-ATPase by cAMP and dexametha-sone in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2001;281:L217-L230.
17. Matlhagela K, Borsick M, Rajkhowa T, Taub M. Identifcation of a prostaglandin-responsive element in the Na, K-ATPase beta 1 promoter that is regulated by cAMP and Ca2+. Evidence for an interactive role of cAMP regulatory element-binding protein and Sp1. J Biol Chem. 2005;280:334-346.
18. Zippin JH, Chen Y, Nahirney P, Kamenetsky M, Wuttke MS, Fischman DA, Levin LR, Buck J. Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J. 2003; 17:82-84.
19. Feng Q, Zhang Y, Li Y, Liu Z, Zuo J, Fang F. Two domains are critical for the nuclear localization of soluble adenylyl cyclase. Biochimie. 2006;88:319-328.
20. Hallows KR, Wang H, Edinger RS, Butterworth MB, Oyster NM, Li H, Buck J, Levin LR, Johnson JP, Pastor-Soler NM. Regulation of epithelial Na+ transport by soluble adenylyl cyclase in kidney collecting duct cells. J Biol Chem. 2009;284:5774-5783.
21. Ahmad M, Medford RM. Evidence for the regulation of Na+, K(+)-ATPase alpha 1 gene expression through the interaction of aldosterone and cAMP-inducible transcriptional factors. Steroids. 1995;60:147-152.
22. Wang G, Kawakami K, Gick G. Regulation of Na, K-ATPase alpha1 sub-unit gene transcription in response to low K(+): role of CRE/ATF-and GC box-binding proteins. J Cell Physiol. 2007;213:167-176.
23. Wang J, Li X, Ke Y, Lu Y, Wang F, Fan N, Sun H, Zhang H, Liu R, Yang J, Ye L, Liu M, Ning G. GPR48 increases mineralocorticoid receptor gene expression. J Am Soc Nephrol. 2012;23:281-293.
24. Edgell CJ, McDonald CC, Graham JB. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci USA. 1983;80:3734-3737.
25. Hohage H, Stachon A, Feidt C, Hirsch JR, Schlatter E. Regulation of organic cation transport in IHKE-1 and LLC-PK1 cells. Fluorometric studies with 4-(4-dimethylaminostyryl)-N-methylpyridinium. J Pharmacol Exp Ther. 1998;286:305-310.
26. Jessen H, Røigaard H, Riahi-Esfahani S, Jacobsen C. A comparative study on the uptake of alpha-aminoisobutyric acid by normal and immortalized human embryonic kidney cells from proximal tubule. Biochim Biophys Acta. 1994;1190:279-288.
27. Tveito G, Hansteen IL, Dalen H, Haugen A. Immortalization of normal human kidney epithelial cells by nickel(II). Cancer Res. 1989;49:1829-1835.
28. Kusche-Vihrog K, Urbanova K, Blanqué A, Wilhelmi M, Schillers H, Kliche K, Pavenstädt H, Brand E, Oberleithner H. C-reactive protein makes human endothelium stiff and tight. Hypertension. 2011;57:231-237.
29. Schreiber E, Matthias P, Müller MM, Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 1989;17:6419.
30. Schmitz B, Salomon A, Rötrige A, Ritter M, Ringelstein EB, Fischer JW, Paul M, Brand E, Brand SM. Interindividual transcriptional regulation of the human biglycan gene involves three common molecular haplotypes. Arterioscler Thromb Vasc Biol. 2013;33:871-880.
31. Zippin JH, Farrell J, Huron D, Kamenetsky M, Hess KC, Fischman DA, Levin LR, Buck J. Bicarbonate-responsive "soluble" adeny-lyl cyclase defines a nuclear cAMP microdomain. J Cell Biol. 2004;164:527-534.
32. Boerma M, Fu Q, Wang J, Loose DS, Bartolozzi A, Ellis JL, McGonigle S, Paradise E, Sweetnam P, Fink LM, Vozenin-Brotons MC, Hauer-Jensen M. Comparative gene expression profling in three primary human cell lines after treatment with a novel inhibitor of Rho kinase or atorvastatin. Blood Coagul Fibrinolysis. 2008;19:709-718.
33. Mick VE, Itani OA, Loftus RW, Husted RF, Schmidt TJ, Thomas CP. The alpha-subunit of the epithelial sodium channel is an aldosterone-induced transcript in mammalian collecting ducts, and this transcriptional response is mediated via distinct cis-elements in the 5'-fanking region of the gene. Mol Endocrinol. 2001;15:575-588.
34. Kobayashi M, Kawakami K. ATF-1CREB heterodimer is involved in constitutive expression of the housekeeping Na, K-ATPase alpha 1 subunit gene. Nucleic Acids Res. 1995;23:2848-2855.
35. Messeguer X, Escudero R, Farré D, Núñez O, Martínez J, Albà MM. PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics. 2002;18:333-334.
36. Staub O, Gautschi I, Ishikawa T, Breitschopf K, Ciechanover A, Schild L, Rotin D. Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J. 1997;16:6325-6336.
37. Zippin JH, Chadwick PA, Levin LR, Buck J, Magro CM. Soluble adenylyl cyclase defnes a nuclear cAMP microdomain in keratinocyte hyperprolif-erative skin diseases. J Invest Dermatol. 2010;130:1279-1287.
38. Xu WM, Chen J, Chen H, Diao RY, Fok KL, Dong JD, Sun TT, Chen WY, Yu MK, Zhang, XH, Tsang LL, Lau A, Shi QX, Shi QH, Huang PB, Chan HC. Defective CFTR-dependent CREB activation results in impaired spermatogenesis and azoospermia. PLoS One. 2011;6:e19120.
39. Flacke JP, Flacke H, Appukuttan A, Palisaar RJ, Noldus J, Robinson BD, Reusch HP, Zippin JH, Ladilov Y. Type 10 soluble adenylyl cyclase is overexpressed in prostate carcinoma and controls proliferation of prostate cancer cells. J Biol Chem. 2013;288:3126-3135.
40. Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS, Levin LR, Williams CJ, Buck J, Moss SB. The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell. 2005;9:249-259.
41. Johannessen M, Moens U. Multisite phosphorylation of the cAMP response element-binding protein (CREB) by a diversity of protein kinases. Front Biosci. 2007;12:1814-1832.
42. Dash PK, Karl KA, Colicos MA, Prywes R, Kandel ER. cAMP response element-binding protein is activated by Ca2+/calmodulin-as well as cAMP-dependent protein kinase. Proc Natl Acad Sci USA. 1991;88:5061-5065.
43. Pilz RB, Casteel DE. Regulation of gene expression by cyclic GMP. Circ Res. 2003;93:1034-1046.
44. Sauzeau V, Rolli-Derkinderen M, Marionneau C, Loirand G, Pacaud P. RhoA expression is controlled by nitric oxide through cGMP-dependent protein kinase activation. J Biol Chem. 2003;278:9472-9480.
45. Taddei S, Ghiadoni L. Phosphodiesterase 5 inhibition to treat essential hypertension: is this the beginning of the story? Hypertension. 2006;48:546-548.
46. Verhovez A, Williams TA, Morello F, Monticone S, Brizzi MF, Dentelli P, Fallo F, Fabris B, Amenta F, Gomez-Sanchez C, Veglio F, Mulatero P. Aldosterone does not modify gene expression in human ECs. Horm Metab Res. 2012;44:234-238.