Circulating ACE2 activity is increased in patients with type 1 diabetes and vascular complications

Journal of Hypertension

Volumn 30, Issue 2, 2012, Pages 375-383

  Soro Paavonen, Aino ^a   Gordin, Daniel ^a   Forsblom, Carol ^a   Rosengard Barlund, Milla ^a   Waden, Johan ^a   Thorn, Lena ^a   Sandholm, Niina ^a   Thomas, Merlin C ^b   Groop, Per Henrik ^a,b  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

albuminuria; angiotensin converting enzyme 2; angiotensin converting enzyme inhibitors; blood pressure; diabetic nephropathy; renin angiotensin system; type 1 diabetes

Indexed keywords

ACETYLSALICYLIC ACID; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN RECEPTOR ANTAGONIST; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR;

ADULT; ANTIHYPERTENSIVE THERAPY; ARTERIAL STIFFNESS; ARTICLE; AUGMENTATION INDEX; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DISEASE DURATION; ENZYME ACTIVITY; ESTIMATED GLOMERULUS FILTRATION RATE; FEMALE; FLUOROMETRY; GLOMERULUS FILTRATION RATE; HUMAN; HYPERTENSION; INSULIN DEPENDENT DIABETES MELLITUS; ISCHEMIC HEART DISEASE; MACROALBUMINURIA; MAJOR CLINICAL STUDY; MALE; MICROALBUMINURIA; PRIORITY JOURNAL; PULSE PRESSURE; PULSE WAVE; SERUM; SYSTOLIC BLOOD PRESSURE;

EID: 84855860581     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0b013e32834f04b6     Document Type: Article

References (45)

1. Hollenberg NK, Price DA, Fisher ND, Lansang MC, Perkins B, Gordon MS, et al. Glomerular hemodynamics and the renin-angiotensin system in patients with type 1 diabetes mellitus. Kidney Int 2003; 63:172-178. (Pubitemid 35463918)
2. Lafayette RA, Mayer G, Park SK, Meyer TW. Angiotensin II receptor blockade limits glomerular injury in rats with reduced renal mass. J Clin Invest 1992; 90:766-771.
3. Eiskjaer H, Sorensen SS, Danielsen H, Pedersen EB. Glomerular and tubular antinatriuretic actions of low-dose angiotensin II infusion in man. J Hypertens 1992; 10:1033-1040.
4. Briones AM, Rodriguez-Criado N, Hernanz R, Garcia-Redondo AB, Rodrigues-Diez RR, Alonso MJ, et al. Atorvastatin prevents angiotensin II-induced vascular remodeling and oxidative stress. Hypertension 2009; 54:142-149.
5. Schjoedt KJ, Hansen HP, Tarnow L, Rossing P, Parving HH. Long-term prevention of diabetic nephropathy: an audit. Diabetologia 2008; 51:956-961.
6. Nakagawa T. Diabetic nephropathy: aldosterone breakthrough in patients on an ACEI. Nat 2010; 6:194-196.
7. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, et al. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 2000; 87:E1-E9.
8. Ferrario CM. Angiotensin-converting enzyme 2 and angiotensin-(1-7): an evolving story in cardiovascular regulation. Hypertension 2006; 47:515-521. (Pubitemid 43843868)
9. Ye M, Wysocki J, William J, Soler MJ, Cokic I, Batlle D. Glomerular localization and expression of angiotensin-converting enzyme 2 and angiotensin-converting enzyme: implications for albuminuria in diabetes. J Am Soc Nephrol 2006; 17:3067-3075. (Pubitemid 44707767)
10. Soler MJ, Wysocki J, Ye M, Lloveras J, Kanwar Y, Batlle D. ACE2 inhibition worsens glomerular injury in association with increased ACE expression in streptozotocin-induced diabetic mice. Kidney Int 2007; 72:614-623. (Pubitemid 47312795)
11. Oudit GY, Herzenberg AM, Kassiri Z, Wong D, Reich H, Khokha R, et al. Loss of angiotensin-converting enzyme-2 leads to the late development of angiotensin II-dependent glomerulosclerosis. Am J Pathol 2006; 168:1808-1820. (Pubitemid 43825302)
12. Tikellis C, Bialkowski K, Pete J, Sheehy K, Su Q, Johnston C, et al. ACE2 deficiency modifies renoprotection afforded by ACE inhibition in experimental diabetes. Diabetes 2008; 57:1018-1025.
13. Thorn LM, Forsblom C, Fagerudd J, Thomas MC, Pettersson-Fernholm K, Saraheimo M, et al. Metabolic syndrome in type 1 diabetes: association with diabetic nephropathy and glycemic control (the FinnDiane study). Diabetes Care 2005; 28:2019-2024. (Pubitemid 41060978)
14. Saraheimo M, Forsblom C, Pettersson-Fernholm K, Flyvbjerg A, Groop PH, Frystyk J. Increased levels of alpha-defensin (S1, S2 and S3) in type 1 diabetic patients with nephropathy. Nephrol Dial Transplant 2008; 23:914-918. (Pubitemid 351767570)
15. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18:499-502.
16. Levey AS, Coresh J, Greene T, Stevens LA, Zhang YL, Hendriksen S, et al. Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med 2006; 145:247-254. (Pubitemid 46768608)
17. O'Rourke MF, Kelly RP. Wave reflection in the systemic circulation and its implications in ventricular function. J Hypertens 1993; 11:327-337. (Pubitemid 23139773)
18. Epelman S, Tang WH, Chen SY, Van Lente F, Francis GS, Sen S. Detection of soluble angiotensin-converting enzyme 2 in heart failure: insights into the endogenous counter-regulatory pathway of the reninangiotensin-aldosterone system. J Am Coll Cardiol 2008; 52:750-754.
19. Pendergrass KD, Pirro NT, Westwood BM, Ferrario CM, Brosnihan KB, Chappell MC. Sex differences in circulating and renal angiotensins of hypertensive mRen(2). Lewis but not normotensive Lewis rats. Am J Physiol Heart Circ Physiol 2008; 295:H10-H20.
20. Yanes LL, Sartori-Valinotti JC, Iliescu R, Romero DG, Racusen LC, Zhang H, et al. Testosterone-dependent hypertension and upregulation of intrarenal angiotensinogen in Dahl salt-sensitive rats. Am J Physiol Renal Physiol 2009; 296:F771-F779.
21. Reich HN, Oudit GY, Penninger JM, Scholey JW, Herzenberg AM. Decreased glomerular and tubular expression of ACE2 in patients with type 2 diabetes and kidney disease. Kidney Int 2008; 74:1610-1616.
22. Ferrario CM, Jessup J, Chappell MC, Averill DB, Brosnihan KB, Tallant EA, et al. Effect of angiotensin-converting enzyme inhibition and angiotensin II receptor blockers on cardiac angiotensin-converting enzyme 2. Circulation 2005; 111:2605-2610. (Pubitemid 40740859)
23. Ferrario CM, Jessup J, Gallagher PE, Averill DB, Brosnihan KB, Ann Tallant E, et al. Effects of renin-angiotensin system blockade on renal angiotensin-(1-7) forming enzymes and receptors. Kidney Int 2005; 68:2189-2196. (Pubitemid 43117793)
24. Gallagher PE, Ferrario CM, Tallant EA. MAP kinase/phosphatase pathway mediates the regulation of ACE2 by angiotensin peptides. Am J Physiol Cell Physiol 2008; 295:C1169-C1174. (Pubitemid 352790330)
25. Rice GI, Jones AL, Grant PJ, Carter AM, Turner AJ, Hooper NM. Circulating activities of angiotensin-converting enzyme, its homolog, angiotensin- converting enzyme 2, and neprilysin in a family study. Hypertension 2006; 48:914-920. (Pubitemid 44611005)
26. Lew RA, Warner FJ, Hanchapola I, Yarski MA, Manohar J, Burrell LM, et al. Angiotensin-converting enzyme 2 catalytic activity in human plasma is masked by an endogenous inhibitor. Exp Physiol 2008; 93:685-693. (Pubitemid 351595050)
27. Tikellis C, Johnston CI, Forbes JM, Burns WC, Burrell LM, Risvanis J, et al. Characterization of renal angiotensin-converting enzyme 2 in diabetic nephropathy. Hypertension 2003; 41:392-397. (Pubitemid 36314606)
28. Ye M, Wysocki J, Naaz P, Salabat MR, LaPointe MS, Batlle D. Increased ACE 2 and decreased ACE protein in renal tubules from diabetic mice: a renoprotective combination? Hypertension 2004; 43: 1120-1125. (Pubitemid 38579924)
29. Fraga-Silva RA, Sorg BS, Wankhede M, Dedeugd C, Jun JY, Baker MB, et al. ACE2 activation promotes antithrombotic activity. Mol Med 2010; 16:210-215.
30. Thomas MC, Pickering RJ, Tsorotes D, Koitka A, Sheehy K, Bernardi S, et al. Genetic Ace2 deficiency accentuates vascular inflammation and atherosclerosis in the ApoE knockout mouse. Circ Res 2010; 107:888-897.
31. Dilauro M, Zimpelmann J, Robertson SJ, Genest D, Burns KD. Effect of ACE2 and angiotensin-(1-7) in a mouse model of early chronic kidney disease. Am J Physiol Renal Physiol 2010; 298:F1523-F1532.
32. Wysocki J, Ye M, Soler MJ, Gurley SB, Xiao HD, Bernstein KE, et al. ACE and ACE2 activity in diabetic mice. Diabetes 2006; 55:2132-2139. (Pubitemid 44509989)
33. Lely AT, Hamming I, van Goor H, Navis GJ. Renal ACE2 expression in human kidney disease. J Pathol 2004; 204:587-593. (Pubitemid 39585958)
34. Konoshita T, Wakahara S, Mizuno S, Motomura M, Aoyama C, Makino Y, et al. Tissue gene expression of renin-angiotensin system in human type 2 diabetic nephropathy. Diabetes Care 2006; 29:848-852. (Pubitemid 44115305)
35. Mizuiri S, Hemmi H, Arita M, Ohashi Y, Tanaka Y, Miyagi M, et al. Expression of ACE and ACE2 in individuals with diabetic kidney disease and healthy controls. Am J Kidney Dis 2008; 51:613-623. (Pubitemid 351400834)
36. Lambert DW, Yarski M, Warner FJ, Thornhill P, Parkin ET, Smith AI, et al. Tumor necrosis factor-alpha convertase (ADAM17) mediates regulated ectodomain shedding of the severe-acute respiratory syndrome-coronavirus (SARS-CoV) receptor, angiotensin-converting enzyme-2 (ACE2). J Biol Chem 2005; 280:30113-30119. (Pubitemid 41216188)
37. Lautrette A, Li S, Alili R, Sunnarborg SW, Burtin M, Lee DC, et al. Angiotensin II and EGF receptor cross-talk in chronic kidney diseases: a new therapeutic approach. Nat Med 2005; 11:867-874. (Pubitemid 41161119)
38. Melenhorst WB, Visser L, Timmer A, van den Heuvel MC, Stegeman CA, van Goor H. ADAM17 upregulation in human renal disease: a role in modulating TGF-alpha availability? Am J Physiol Renal Physiol 2009; 297:F781-F790.
39. Fedak PW, Moravec CS, McCarthy PM, Altamentova SM, Wong AP, Skrtic M, et al. Altered expression of disintegrin metalloproteinases and their inhibitor in human dilated cardiomyopathy. Circulation 2006; 113:238-245.
40. Epelman S, Shrestha K, Troughton RW, Francis GS, Sen S, Klein AL, et al. Soluble angiotensin-converting enzyme 2 in human heart failure: relation with myocardial function and clinical outcomes. J Card Fail 2009; 15:565-571.
41. Goulter AB, Goddard MJ, Allen JC, Clark KL. ACE2 gene expression is up-regulated in the human failing heart. BMC Med 2004; 2:19.
42. Tolonen N, Forsblom C, Thorn L, Waden J, Rosengard-Barlund M, Saraheimo M, et al. Relationship between lipid profiles and kidney function in patients with type 1 diabetes. Diabetologia 2008; 51:12-20. (Pubitemid 50002203)
43. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem 2000; 275:33238-33243.
44. Oudit GY, Liu GC, Zhong J, Basu R, Chow FL, Zhou J, et al. Human recombinant ACE2 reduces the progression of diabetic nephropathy. Diabetes 2010; 59:529-538.
45. Zhong J, Basu R,Guo D,ChowFL, Byrns S, Schuster M, et al.Angiotensinconverting enzyme 2 suppresses pathological hypertrophy, myocardial fibrosis, and cardiac dysfunction. Circulation 2010; 122:717-728.