G-Protein-Coupled Receptor MrgD Is a Receptor for Angiotensin-(1-7) Involving Adenylyl Cyclase, cAMP, and Phosphokinase A

Hypertension

Volumn 68, Issue 1, 2016, Pages 185-194

  Tetzner, Anja ^a,b   Gebolys, Kinga ^a   Meinert, Christian ^a,c   Klein, Sabine ^d   Uhlich, Anja ^a   Trebicka, Jonel ^d   Villacañas, Óscar ^e   Walther, Thomas ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF BONN   (Germany)

^e Intelligent Pharma SL ^*  (Spain)

Author keywords

angiotensin; G protein coupled receptor; mesangial cells; mice; renin angiotensin system

Indexed keywords

1 (4 DIMETHYLAMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDRO 1H IMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; ADENYLATE CYCLASE; ANGIOTENSIN[1-7]; CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; G ROTEIN COUPLED RECEPTOR MRGD; HEPTAPEPTIDE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; ANGIOTENSIN I; ANGIOTENSIN I (1-7); CYCLIC AMP DEPENDENT PROTEIN KINASE; PEPTIDE FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL EXPANSION; CELL STIMULATION; CONCENTRATION CAMP; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; FEMALE; GENETIC TRANSFECTION; HEK293 CELL LINE; HEMODYNAMICS; HUMAN; HUMAN CELL; MALE; MESANGIUM CELL; MOUSE; NONHUMAN; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SECOND MESSENGER; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; HYPERTENSION; KNOCKOUT MOUSE; METABOLISM; SENSITIVITY AND SPECIFICITY; WESTERN BLOTTING;

ADENYLYL CYCLASES; ANGIOTENSIN I; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; HEK293 CELLS; HUMANS; HYPERTENSION; MALE; MESANGIAL CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; PHOSPHOTRANSFERASES; RECEPTORS, G-PROTEIN-COUPLED; RENIN-ANGIOTENSIN SYSTEM; SENSITIVITY AND SPECIFICITY;

EID: 84969930657     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.116.07572     Document Type: Article

References (34)

1. Crowley SD, Coffman TM. Recent advances involving the renin-angiotensin system. Exp Cell Res. 2012;318:1049-1056. doi: 10.1016/j. yexcr.2012.02.023.
2. Takeda H, Katagata Y, Hozumi Y, Kondo S. Effects of angiotensin II receptor signaling during skin wound healing. Am J Pathol. 2004;165:1653-1662. doi: 10.1016/S0002-9440(10)63422-0.
3. Vickers C, Hales P, Kaushik V, Dick L, Gavin J, Tang J, Godbout K, Parsons T, Baronas E, Hsieh F, Acton S, Patane M, Nichols A, Tummino P. Hydrolysis of biological peptides by human angiotensin-converting enzyme-related carboxypeptidase. J Biol Chem. 2002;277:14838-14843. doi: 10.1074/jbc.M200581200.
4. Mercure C, Yogi A, Callera GE, Aranha AB, Bader M, Ferreira AJ, Santos RA, Walther T, Touyz RM, Reudelhuber TL. Angiotensin(1-7) blunts hypertensive cardiac remodeling by a direct effect on the heart. Circ Res. 2008;103:1319-1326. doi: 10.1161/CIRCRESAHA.108.184911.
5. Sumners C, Horiuchi M, Widdop RE, McCarthy C, Unger T, Steckelings UM. Protective arms of the renin-angiotensin-system in neurological disease. Clin Exp Pharmacol Physiol. 2013;40:580-588. doi: 10.1111/1440-1681.12137.
6. Santos RAS, Esilva ACS, Maric C, Silva DMR, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SVB, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss H-P, Speth R, Walther T. Angiotensin-(1-7) is an endogenous ligand for the g protein-coupled receptor mas. Proceed Nati Acad Sci USA. 2003;100:8258-8263.
7. Walters PE, Gaspari TA, Widdop RE. Angiotensin-(1-7) acts as a vasodepressor agent via angiotensin II type 2 receptors in conscious rats. Hypertension. 2005;45:960-966. doi: 10.1161/01. HYP.0000160325.59323.b8.
8. Santos RA, Haibara AS, Campagnole-Santos MJ, Simões Esilva AC, Paula RD, Pinheiro SV, Leite MF, Lemos VS, Silva DM, Guerra MT, Khosla MC. Characterization of a new selective antagonist for angiotensin-(1-7), D-pro7-angiotensin-(1-7). Hypertension. 2003;41(3 pt 2):737-743. doi: 10.1161/01.HYP.0000052947.60363.24.
9. Klein N, Gembardt F, Supé S, Kaestle SM, Nickles H, Erfinanda L, Lei X, Yin J, Wang L, Mertens M, Szaszi K, Walther T, Kuebler WM. Angiotensin-(1-7) protects from experimental acute lung injury. Crit Care Med. 2013;41:e334-e343. doi: 10.1097/CCM.0b013e31828a6688.
10. Zhu X, Wang Y, Schwiebs A, Walther T. Chimeric natriuretic peptide ACNP stimulates both natriuretic peptide receptors, the NPRA and NPRB. Mol Cell Endocrinol. 2013;366:117-123. doi: 10.1016/j. mce.2012.11.006.
11. Gembardt F, Grajewski S, Vahl M, Schultheiss HP, Walther T. Angiotensin metabolites can stimulate receptors of the Mas-related genes family. Mol Cell Biochem. 2008;319:115-123. doi: 10.1007/s11010-008-9884-4.
12. Walther T, Balschun D, Voigt JP, Fink H, Zuschratter W, Birchmeier C, Ganten D, Bader M. Sustained long term potentiation and anxiety in mice lacking the Mas protooncogene. J Biol Chem. 1998;273:11867-11873.
13. Zylka MJ, Rice FL, Anderson DJ. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron. 2005;45:17-25. doi: 10.1016/j.neuron.2004.12.015.
14. Iwata M, Cowling RT, Gurantz D, Moore C, Zhang S, Yuan JX, Greenberg BH. Angiotensin-(1-7) binds to specific receptors on cardiac fibroblasts to initiate antifibrotic and antitrophic effects. Am J Physiol Heart Circ Physiol. 2005;289:H2356-H2363. doi: 10.1152/ajpheart.00317.2005.
15. Pérez-Rivero G, Ruiz-Torres MP, Rivas-Elena JV, Jerkic M, Díez-Marques ML, Lopez-Novoa JM, Blasco MA, Rodríguez-Puyol D. Mice deficient in telomerase activity develop hypertension because of an excess of endothelin production. Circulation. 2006;114:309-317. doi: 10.1161/CIRCULATIONAHA.105.611111.
16. Huey R, Morris GM, Olson AJ, Goodsell DS. A semiempirical free energy force field with charge-based desolvation. J Comput Chem. 2007;28:1145-1152. doi: 10.1002/jcc.20634.
17. Horn F, Weare J, Beukers MW, Hörsch S, Bairoch A, Chen W, Edvardsen O, Campagne F, Vriend G. GPCRDB: an information system for G protein-coupled receptors. Nucleic Acids Res. 1998;26:275-279. doi: 10.1093/nar/26.1.275.
18. Pérodin J, Deraët M, Auger-Messier M, Boucard AA, Rihakova L, Beaulieu ME, Lavigne P, Parent JL, Guillemette G, Leduc R, Escher E. Residues 293 and 294 are ligand contact points of the human angiotensin type 1 receptor. Biochemistry. 2002;41:14348-14356.
19. Prokop JW, Santos RA, Milsted A. Differential mechanisms of activation of the Ang peptide receptors AT1, AT2, and MAS: using in silico techniques to differentiate the three receptors. PLoS One. 2013;8:e65307. doi: 10.1371/journal.pone.0065307.
20. O'Boyle NM, Banck M, James CA, Morley C, Vandermeersch T, Hutchison GR. Open Babel: An open chemical toolbox. J Cheminform. 2011;3:33. doi: 10.1186/1758-2946-3-33.
21. Tallant EA, Clark MA. Molecular mechanisms of inhibition of vascular growth by angiotensin-(1-7). Hypertension. 2003;42:574-579. doi: 10.1161/01.HYP.0000090322.55782.30.
22. Liu GC, Oudit GY, Fang F, Zhou J, Scholey JW. Angiotensin-(1-7)- induced activation of ERK1/2 is cAMP/protein kinase A-dependent in glomerular mesangial cells. Am J Physiol Renal Physiol. 2012;302:F784-F790. doi: 10.1152/ajprenal.00455.2011.
23. Mordwinkin NM, Meeks CJ, Jadhav SS, Espinoza T, Roda N, Di Zerega GS, Louie SG, Rodgers KE. Angiotensin-(1-7) administration reduces oxidative stress in diabetic bone marrow. Endocrinology. 2012;153:2189-2197. doi: 10.1210/en.2011-2031.
24. Peiró C, Vallejo S, Gembardt F, Azcutia V, Heringer-Walther S, Rodríguez-Mañas L, Schultheiss HP, Sánchez-Ferrer CF, Walther T. Endothelial dysfunction through genetic deletion or inhibition of the G protein-coupled receptor Mas: a new target to improve endothelial function. J Hypertens. 2007;25:2421-2425. doi: 10.1097/HJH.0b013e3282f0143c.
25. Uno M, Nishimura S, Fukuchi K, Kaneta Y, Oda Y, Komori H, Takeda S, Haga T, Agatsuma T, Nara F. Identification of physiologically active substances as novel ligands for MRGPRD. J Biomed Biotechnol. 2012;2012:816159. doi: 10.1155/2012/816159.
26. Higuchi S, Ohtsu H, Suzuki H, Shirai H, Frank GD, Eguchi S. Angiotensin II signal transduction through the AT1 receptor: novel insights into mechanisms and pathophysiology. Clin Sci (Lond). 2007;112:417-428. doi: 10.1042/CS20060342.
27. Mayr B, Montminy M. Transcriptional regulation by the phosphorylation dependent factor CREB. Nat Rev Mol Cell Biol. 2001;2:599-609. doi: 10.1038/35085068.
28. Verano-Braga T, Schwämmle V, Sylvester M, Passos-Silva DG, Peluso AA, Etelvino GM, Santos RA, Roepstorff P. Time-resolved quantitative phosphoproteomics: new insights into Angiotensin-(1-7) signaling networks in human endothelial cells. J Proteome Res. 2012;11:3370-3381. doi: 10.1021/pr3001755.
29. Meinert C, Gembardt F, Böhme I, Tetzner A, Wieland T, Greenberg B, Walther T. Identification of intracellular proteins and signaling pathways in human endothelial cells regulated by angiotensin-(1-7). J Proteomics. 2016;130:129-139. doi: 10.1016/j.jprot.2015.09.020.
30. Lautner RQ, Villela DC, Fraga-Silva RA, et al. Discovery and characterization of alamandine: a novel component of the renin-angiotensin system. Circ Res. 2013;112:1104-1111. doi: 10.1161/CIRCRESAHA.113.301077.
31. Han Y, Sun HJ, Li P, Gao Q, Zhou YB, Zhang F, Gao XY, Zhu GQ. Angiotensin-(1-7) in paraventricular nucleus modulates sympathetic activity and cardiac sympathetic afferent reflex in renovascular hypertensive rats. PLoS One. 2012;7:e48966. doi: 10.1371/journal.pone.0048966.
32. Heringer-Walther S, Eckert K, Schumacher SM, Uharek L, Wulf-Goldenberg A, Gembardt F, Fichtner I, Schultheiss HP, Rodgers K, Walther T. Angiotensin-(1-7) stimulates hematopoietic progenitor cells in vitro and in vivo. Haematologica. 2009;94:857-860. doi: 10.3324/haematol.2008.000034.
33. Boer AK, Drayer AL, Vellenga E. cAMP/PKA-mediated regulation of erythropoiesis. Leuk Lymphoma. 2003;44:1893-1901. doi: 10.1080/1042819031000116715.
34. Ohshima K, Mogi M, Nakaoka H, Iwanami J, Min LJ, Kanno H, Tsukuda K, Chisaka T, Bai HY, Wang XL, Ogimoto A, Higaki J, Horiuchi M. Possible role of angiotensin-converting enzyme 2 and activation of angiotensin II type 2 receptor by angiotensin-(1-7) in improvement of vascular remodeling by angiotensin II type 1 receptor blockade. Hypertension. 2014;63:e53-e59. doi: 10.1161/HYPERTENSIONAHA.113.02426.