Identification of the Vasoconstriction-Inhibiting Factor (VIF), a potent endogenous cofactor of angiotensin II acting on the angiotensin II type 2 receptor

Circulation

Volumn 131, Issue 16, 2015, Pages 1426-1434

  Salem, Silvia ^a,b   Jankowski, Vera ^b   Asare, Yaw ^b   Liehn, Elisa ^b   Welker, Pia ^a   Raya Bermudez, Ana ^c   Pineda Martos, Carmen ^c   Rodriguez, Mariano ^c   Muñoz Castañeda, Juan Rafael ^c   Bruck, Heike ^d   Marx, Nikolaus ^b   Machado, Fernanda B ^a   Staudt, Mareike ^b   Heinze, Georg ^e   Zidek, Walter ^a   Jankowski, Joachim ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^c HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

^d UNIVERSITY HOSPITAL ESSEN   (Germany)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Angiotensin; Angiotensin II; AT 2 receptor; Peptides; Vasoconstriction

Indexed keywords

ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; CHROMOGRANIN A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; N(G) NITROARGININE METHYL ESTER; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; VASOCONSTRICTION INHIBITING FACTOR; VASODILATOR AGENT; PEPTIDE; VASOCONSTRICTION-INHIBITING FACTOR, HUMAN;

ADRENAL GLAND; ADULT; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; AORTIC SMOOTH MUSCLE CELL; ARTICLE; BLOOD PRESSURE REGULATION; CAPILLARY ENDOTHELIAL CELL; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; ELEVATED BLOOD PRESSURE; FEMALE; HEART FAILURE; HUMAN; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY FUNCTION; KIDNEY PERFUSION; MALE; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR AFFINITY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SMOOTH MUSCLE FIBER; SYSTOLIC BLOOD PRESSURE; VASOCONSTRICTION; VASODILATATION; AGONISTS; ANIMAL; BLOOD; BOVINE; CELL CULTURE; CHEMISTRY; CHRONIC KIDNEY FAILURE; DRUG EFFECTS; ENDOTHELIUM CELL; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; WISTAR KYOTO RAT; WISTAR RAT;

ADRENAL GLANDS; AMINO ACID SEQUENCE; ANGIOTENSIN II; ANIMALS; CATTLE; CELLS, CULTURED; CHROMOGRANIN A; ENDOTHELIAL CELLS; HEART FAILURE; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MOLECULAR SEQUENCE DATA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, INBRED WKY; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTOR, ANGIOTENSIN, TYPE 2; RENAL INSUFFICIENCY, CHRONIC; RENIN-ANGIOTENSIN SYSTEM; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VASODILATION;

EID: 84929359390     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.013168     Document Type: Article

References (41)

1. Roscioni SS, Heerspink HJ, de Zeeuw D. The effect of RAAS blockade on the progression of diabetic nephropathy. Nat Rev Nephrol. 2014;10:77-87. doi: 10.1038/nrneph.2013.251.
2. Sayer G, Bhat G. The renin-angiotensin-aldosterone system and heart failure. Cardiol Clin. 2014;32:21-32, vii. doi: 10.1016/j.ccl.2013.09.002.
3. Weiss JW, Thorp ML, O'Hare AM. Renin-angiotensin system blockade in older adults with chronic kidney disease: a review of the literature. Curr Opin Nephrol Hypertens. 2010;19:413-419. doi: 10.1097/MNH.0b013e32833b8d6b.
4. George J, Struthers AD, Lang CC. Modulation of the renin-angiotensinaldosterone system in heart failure. Curr Atheroscler Rep. 2014;16:403. doi: 10.1007/s11883-014-0403-7.
5. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 2007;292:C82-C97. doi: 10.1152/ajpcell.00287.2006.
6. Dahlöf B, Devereux RB, Kjeldsen SE, Julius S, Beevers G, de Faire U, Fyhrquist F, Ibsen H, Kristiansson K, Lederballe-Pedersen O, Lindholm LH, Nieminen MS, Omvik P, Oparil S, Wedel H; LIFE Study Group. Cardiovascular morbidity and mortality in the Losartan Intervention For Endpoint Reduction in Hypertension Study (LIFE): a randomised trial against atenolol. Lancet. 2002;359:995-1003. doi: 10.1016/ S0140-6736(02)08089-3.
7. Li J, Culman J, Hörtnagl H, Zhao Y, Gerova N, Timm M, Blume A, Zimmermann M, Seidel K, Dirnagl U, Unger T. Angiotensin AT2 receptor protects against cerebral ischemia-induced neuronal injury. FASEB J. 2005;19:617-619. doi: 10.1096/fj.04-2960fje.
8. Santos RA, Ferreira AJ, Simões E Silva AC. Recent advances in the angiotensin-converting enzyme 2-angiotensin(1-7)-Mas axis. Exp Physiol. 2008;93:519-527. doi: 10.1113/expphysiol.2008.042002.
9. Sampaio WO, Henrique de Castro C, Santos RA, Schiffrin EL, Touyz RM. Angiotensin-(1-7) counterregulates angiotensin II signaling in human endothelial cells. Hypertension. 2007;50:1093-1098. doi: 10.1161/HYPERTENSIONAHA.106.084848.
10. Jankowski V, Tölle M, Santos RA, Günthner T, Krause E, Beyermann M, Welker P, Bader M, Pinheiro SV, Sampaio WO, Lautner R, Kretschmer A, van der Giet M, Zidek W, Jankowski J. Angioprotectin: an angiotensin II-like peptide causing vasodilatory effects. FASEB J. 2011;25:2987-2995. doi: 10.1096/fj.11-185470.
11. Bogaert YE, Linas S. The role of obesity in the pathogenesis of hypertension. Nat Clin Pract Nephrol. 2009;5:101-111. doi: 10.1038/ncpneph1022.
12. Beevers G, Lip GY, O'Brien E. ABC of hypertension: the pathophysiology of hypertension. BMJ. 2001;322:912-916.
13. Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson Å, Kampf C, Sjöstedt E, Asplund A, Olsson I, Edlund K, Lundberg E, Navani S, Szigyarto CA, Odeberg J, Djureinovic D, Takanen JO, Hober S, Alm T, Edqvist PH, Berling H, Tegel H, Mulder J, Rockberg J, Nilsson P, Schwenk JM, Hamsten M, von Feilitzen K, Forsberg M, Persson L, Johansson F, Zwahlen M, von Heijne G, Nielsen J, Pontén F. Proteomics: tissue-based map of the human proteome. Science. 2015;347:1260419. doi: 10.1126/science.1260419.
14. Franco C, Soares R, Pires E, Koci K, Almeida AM, Santos R, Coelho AV. Understanding regeneration through proteomics. Proteomics. 2013;13:686-709. doi: 10.1002/pmic.201200397.
15. Aunis D, Miras-Portugal MT, Mandel P. Bovine adrenal medullary dopamine-beta-hydroxylase: studies on the structure. Biochim Biophys Acta. 1974;365:259-273.
16. Pintor J, Rotllán P, Torres M, Miras-Portugal MT. Characterization and quantification of diadenosine hexaphosphate in chromaffin cells: granular storage and secretagogue-induced release. Anal Biochem. 1992;200:296-300.
17. Jankowski J, Stephan N, Knobloch M, Fischer S, Schmaltz D, Zidek W, Schlüter H. Mass-spectrometry-linked screening of protein fractions for enzymatic activities: a tool for functional genomics. Anal Biochem. 2001;290:324-329. doi: 10.1006/abio.2001.5001.
18. Gobom J, Schuerenberg M, Mueller M, Theiss D, Lehrach H, Nordhoff E. Alpha-cyano-4-hydroxycinnamic acid affinity sample preparation: a protocol for MALDI-MS peptide analysis in proteomics. Anal Chem. 2001;73:434-438.
19. van der Giet M, Khattab M, Börgel J, Schlüter H, Zidek W. Differential effects of diadenosine phosphates on purinoceptors in the rat isolated perfused kidney. Br J Pharmacol. 1997;120:1453-1460. doi: 10.1038/sj.bjp.0701074.
20. UniProt. http://www.uniprot.org/uniprot/P01019. Accessed April 7, 2015.
21. Jankowski V, Vanholder R, van der Giet M, Tölle M, Karadogan S, Gobom J, Furkert J, Oksche A, Krause E, Tran TN, Tepel M, Schuchardt M, Schlüter H, Wiedon A, Beyermann M, Bader M, Todiras M, Zidek W, Jankowski J. Mass-spectrometric identification of a novel angiotensin peptide in human plasma. Arterioscler Thromb Vasc Biol. 2007;27:297-302. doi: 10.1161/01.ATV.0000253889.09765.5f.
22. Helle KB. Vasostatins: vascular targets. Adv Exp Med Biol. 2000;482:225-238. doi: 10.1007/0-306-46837-9-18.
23. Sahu BS, Sonawane PJ, Mahapatra NR. Chromogranin A: a novel susceptibility gene for essential hypertension. Cell Mol Life Sci. 2010;67:861-874. doi: 10.1007/s00018-009-0208-y.
24. Roatta S, Passatore M, Novello M, Colombo B, Dondossola E, Mohammed M, Losano G, Corti A, Helle KB. The chromogranin A-derived N-terminal peptide vasostatin-I: in vivo effects on cardiovascular variables in the rabbit. Regul Pept. 2011;168:10-20. doi: 10.1016/j.regpep.2011.02.015.
25. Tota B, Quintieri AM, Di Felice V, Cerra MC. New biological aspects of chromogranin A-derived peptides: focus on vasostatins. Comp Biochem Physiol A Mol Integr Physiol. 2007;147:11-18. doi: 10.1016/j.cbpa.2006.05.016.
26. Cerra MC, De Iuri L, Angelone T, Corti A, Tota B. Recombinant N-terminal fragments of chromogranin-A modulate cardiac function of the Langendorff-perfused rat heart. Basic Res Cardiol. 2006;101:43-52. doi: 10.1007/s00395-005-0547-2.
27. Schillaci G, De Vuono S, Pucci G. An endogenous brake on the sympathetic nervous system: the emerging role of catestatin in hypertension. J Cardiovasc Med (Hagerstown). 2011;12:609-612. doi: 10.2459/JCM.0b013e328348d925.
28. Corti A. Chromogranin A and the tumor microenvironment. Cell Mol Neurobiol. 2010;30:1163-1170. doi: 10.1007/s10571-010-9587-8.
29. Wei Z, Biswas N, Wang L, Courel M, Zhang K, Soler-Jover A, Taupenot L, O'Connor DT. A common genetic variant in the 3'-UTR of vacuolar H+-ATPase ATP6V0A1 creates a micro-RNA motif to alter chromogranin A processing and hypertension risk. Circ Cardiovasc Genet. 2011;4:381-389. doi: 10.1161/CIRCGENETICS.111.959767.
30. Savoia C, Tabet F, Yao G, Schiffrin EL, Touyz RM. Negative regulation of RhoA/Rho kinase by angiotensin II type 2 receptor in vascular smooth muscle cells: role in angiotensin II-induced vasodilation in stroke-prone spontaneously hypertensive rats. J Hypertens. 2005;23:1037-1045.
31. Lemarié CA, Schiffrin EL. The angiotensin II type 2 receptor in cardiovascular disease. J Renin Angiotensin Aldosterone Syst. 2010;11:19-31. doi: 10.1177/1470320309347785.
32. Dandapat A, Hu CP, Chen J, Liu Y, Khan JA, Remeo F, Carey RM, Hermonat PL, Mehta JL. Over-expression of angiotensin II type 2 receptor (agtr2) decreases collagen accumulation in atherosclerotic plaque. Biochem Biophys Res Commun. 2008;366:871-877. doi: 10.1016/j.bbrc.2007.11.061.
33. Abadir PM, Periasamy A, Carey RM, Siragy HM. Angiotensin II type 2 receptor-bradykinin B2 receptor functional heterodimerization. Hypertension. 2006;48:316-322. doi: 10.1161/01.HYP.0000228997.88162.a8.
34. Kumar D, Menon V, Ford WR, Clanachan AS, Jugdutt BI. Effect of angiotensin II type 2 receptor blockade on mitogen activated protein kinases during myocardial ischemia-reperfusion. Mol Cell Biochem. 2004;258:211-218.
35. Wenzel S, Taimor G, Piper HM, Schlüter KD. Redox-sensitive intermediates mediate angiotensin II-induced p38 MAP kinase activation, AP-1 binding activity, and TGF-beta expression in adult ventricular cardiomyocytes. FASEB J. 2001;15:2291-2293. doi: 10.1096/fj.00-0827fje.
36. Metz-Boutigue MH, Kieffer AE, Goumon Y, Aunis D. Innate immunity: involvement of new neuropeptides. Trends Microbiol. 2003;11:585-592.
37. Tasiemski A, Hammad H, Vandenbulcke F, Breton C, Bilfinger TJ, Pestel J, Salzet M. Presence of chromogranin-derived antimicrobial peptides in plasma during coronary artery bypass surgery and evidence of an immune origin of these peptides. Blood. 2002;100:553-559.
38. Ceconi C, Ferrari R, Bachetti T, Opasich C, Volterrani M, Colombo B, Parrinello G, Corti A. Chromogranin A in heart failure: a novel neurohumoral factor and a predictor for mortality. Eur Heart J. 2002;23:967-974. doi: 10.1053/euhj.2001.2977.
39. Hsiao RJ, Mezger MS, O'Connor DT. Chromogranin A in uremia: progressive retention of immunoreactive fragments. Kidney Int. 1990;37:955-964.
40. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SV, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss HP, Speth R, Walther T. Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci U S A. 2003;100:8258-8263. doi: 10.1073/pnas.1432869100.
41. Lautner RQ, Villela DC, Fraga-Silva RA, Silva N, Verano-Braga T, Costa-Fraga F, Jankowski J, Jankowski V, Sousa F, Alzamora A, Soares E, Barbosa C, Kjeldsen F, Oliveira A, Braga J, Savergnini S, Maia G, Peluso AB, Passos-Silva D, Ferreira A, Alves F, Martins A, Raizada M, Paula R, Motta-Santos D, Klempin F, Kemplin F, Pimenta A, Alenina N, Sinisterra R, Bader M, Campagnole-Santos MJ, Santos RA. Discovery and characterization of alamandine: a novel component of the reninangiotensin system. Circ Res. 2013;112:1104-1111. doi: 10.1161/CIRCRESAHA.113.301077.