Plasma and Kidney Angiotensin Peptides: Importance of the Aminopeptidase A/Angiotensin III Axis

American Journal of Hypertension

Volumn 28, Issue 12, 2015, Pages 1418-1426

  Wysocki, Jan ^a   Ye, Minghao ^a   Batlle, Daniel ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

ACE2; aminopeptidase A; angiotensin (1 7); angiotensin II; angiotensin III; blood pressure; hypertension

Indexed keywords

ANGIOTENSIN; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN I; ANGIOTENSIN III; ANGIOTENSINASE; ANGIOTENSIN[1-10]; ANGIOTENSIN[1-5]; ANGIOTENSIN[1-7]; ANGIOTENSIN[1-8]; ANGIOTENSIN[1-9]; ANGIOTENSIN[2-10]; ANGIOTENSIN[2-7]; ANGIOTENSIN[2-8]; ANGIOTENSIN[3-7]; ANGIOTENSIN[3-8]; GLUTAMYL AMINOPEPTIDASE; MICROSOMAL AMINOPEPTIDASE; UNCLASSIFIED DRUG; ANGIOTENSIN DERIVATIVE; DIPEPTIDYL CARBOXYPEPTIDASE;

ANGIOTENSIN BLOOD LEVEL; ANIMAL EXPERIMENT; ARTICLE; ENZYME ACTIVITY; KIDNEY; KIDNEY PARENCHYMA; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; PEPTIDOMICS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN METABOLISM; QUANTITATIVE ANALYSIS; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; TANDEM MASS SPECTROMETRY; WILD TYPE; ANIMAL; BLOOD; C57BL MOUSE; FEMALE; KNOCKOUT MOUSE; MALE; METABOLISM;

ANGIOTENSINS; ANIMALS; FEMALE; GLUTAMYL AMINOPEPTIDASE; KIDNEY; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDYL-DIPEPTIDASE A; RENIN-ANGIOTENSIN SYSTEM;

EID: 84949980982     PISSN: 08957061     EISSN: 19417225     Source Type: Journal    
DOI: 10.1093/ajh/hpv054     Document Type: Article

References (47)

1. Kobori H, Nangaku M, Navar LG, Nishiyama A. The intrarenal reninangiotensin system: from physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev 2007; 59(3):251-287.
2. Ferrario CM, Ahmad S, Nagata S, Simington SW, Varagic J, Kon N, Dell'italia LJ. An evolving story of angiotensin-II-forming pathways in rodents and humans. Clin Sci (Lond) 2014; 126:461-469.
3. Raij L. The pathophysiologic basis for blocking the renin-angiotensin system in hypertensive patients with renal disease. Am J Hypertens 2005; 18:95S-99S.
4. Crowley SD, Gurley SB, Herrera MJ, Ruiz P, Griffiths R, Kumar AP, Kim HS, Smithies O, Le TH, Coffman TM. Angiotensin II causes hypertension and cardiac hypertrophy through its receptors in the kidney. Proc Natl Acad Sci USA 2006; 103(47):17985-17990.
5. Baylis C, Brenner BM. Modulation by prostaglandin synthesis inhibitors of the action of exogenous angiotensin II on glomerular ultrafiltration in the rat. Circ Res 1978; 43:889-898.
6. Schiffrin EL, Touyz RM. Inflammation and vascular hypertrophy induced by angiotensin II: role of NADPH oxidase-derived reactive oxygen species independently of blood pressure elevation? Arterioscler Thromb Vasc Biol 2003; 23(5):707-709.
7. Ruiz-Ortega M, Egido J. Angiotensin II modulates cell growth-related events and synthesis of matrix proteins in renal interstitial fibroblasts. Kidney Int 1997; 52:1497-1510.
8. Navar LG, Kobori H, Prieto MC, Gonzalez-Villalobos RA. Intratubular renin-angiotensin system in hypertension. Hypertension 2011; 57:355-362.
9. Park S, Bivona BJ, Ford SM Jr, Xu S, Kobori H, de Garavilla L, Harrison-Bernard LM. Direct evidence for intrarenal chymase-dependent angiotensin II formation on the diabetic renal microvasculature. Hypertension 2013; 61:465-471.
10. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, Oliveira-dos-Santos AJ, da Costa J, Zhang L, Pei Y, Scholey J, Ferrario CM, Manoukian AS, Chappell MC, Backx PH, Yagil Y, Penninger JM. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 2002; 417:822-828.
11. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart RE, Acton S. A novel angiotensin-converting enzyme-related carboxypeptidase(ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 2000; 87:E1-E9.
12. 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.
13. Ferrario CM, Varagic J. The ANG-(1-7)/ACE2/mas axis in the regulation of nephron function. Am J Physiol Renal Physiol 2010; 298:F1297-F1305.
14. Batlle D, Wysocki J, Soler MJ, Ranganath K. Angiotensin-converting enzyme 2: enhancing the degradation of angiotensin II as a potential therapy for diabetic nephropathy. Kidney Int 2012; 81:520-528.
15. Wysocki J, Ye M, Rodriguez E, González-Pacheco FR, Barrios C, Evora K, Schuster M, Loibner H, Brosnihan KB, Ferrario CM, Penninger JM, Batlle D. Targeting the degradation of angiotensin II with recombinant angiotensin-converting enzyme 2: prevention of angiotensin II-dependent hypertension. Hypertension 2010; 55:90-98.
16. Ferreira AJ, Murça TM, Fraga-Silva RA, Castro CH, Raizada MK, Santos RA. New cardiovascular and pulmonary therapeutic strategies based on the Angiotensin-converting enzyme 2/angiotensin-(1-7)/mas receptor axis. Int J Hypertens 2012; 2012:147825.
17. Ye M, Wysocki J, Gonzalez-Pacheco FR, Salem M, Evora K, Garcia-Halpin L, Poglitsch M, Schuster M, Batlle D. Murine recombinant angiotensin-converting enzyme 2: effect on angiotensin II-dependent hypertension and distinctive angiotensin-converting enzyme 2 inhibitor characteristics on rodent and human angiotensin-converting enzyme 2. Hypertension 2012; 60:730-740.
18. Velez JC, Bland AM, Arthur JM, Raymond JR, Janech MG. Characterization of renin-angiotensin system enzyme activities in cultured mouse podocytes. Am J Physiol Renal Physiol 2007; 293:F398-F407.
19. Padia SH, Kemp BA, Howell NL, Fournie-Zaluski MC, Roques BP, Carey RM. Conversion of renal angiotensin II to angiotensin III is critical for AT2 receptor-mediated natriuresis in rats. Hypertension 2008; 51:460-465.
20. Grobe N, Weir NM, Leiva O, Ong FS, Bernstein KE, Schmaier AH, Morris M, Elased KM. Identification of prolyl carboxypeptidase as an alternative enzyme for processing of renal angiotensin II using mass spectrometry. Am J Physiol Cell Physiol 2013; 304(10):C945-953.
21. Volland H, Pradelles P, Ronco P, Azizi M, Simon D, Creminon C, Grassi J. A solid-phase immobilized epitope immunoassay (SPIE-IA) permitting very sensitive and specific measurement of angiotensin II in plasma. J Immunol Methods 1999; 228(1-2):37-47.
22. Allred AJ, Diz DI, Ferrario CM, Chappell MC. Pathways for angiotensin-( 1-7) metabolism in pulmonary and renal tissues. Am J Physiol Renal Physiol 2000; 279:F841-F850.
23. Campbell DJ, Kladis A. Simultaneous radioimmunoassay of six angiotensin peptides in arterial and venous plasma of man. J Hypertens 1990; 8(2):165-172.
24. Poglitsch M, Domenig O, Schwager C, Stranner S, Peball B, Janzek E, Wagner B, Jungwirth H, Loibner H, Schuster M. Recombinant Expression and Characterization of Human and Murine ACE2: Species-Specific Activation of the Alternative Renin-Angiotensin-System. Int J Hypertens 2012; 2012:428950.
25. Gurley SB, Allred A, Le TH, Griffiths R, Mao L, Philip N, Haystead TA, Donoghue M, Breitbart RE, Acton SL, Rockman HA, Coffman TM. Altered blood pressure responses and normal cardiac phenotype in ACE2-null mice. J Clin Invest 2006; 116(8):2218-2225.
26. Wysocki J, Ortiz-Melo DI, Mattocks NK, Xu K, Prescott J, Evora K, Ye M, Sparks MA, Haque SK, Batlle D, Gurley SB. ACE2 deficiency increases NADPH-mediated oxidative stress in the kidney. Physiol Rep 2014; 2(3):e00264.
27. Wysocki J, Garcia-Halpin L, Ye M, Maier C, Sowers K, Burns KD, Batlle D. Regulation of urinary ACE2 in diabetic mice. Am J Physiol Renal Physiol 2013; 305:F600-F611.
28. Haber PK, Ye M, Wysocki J, Maier C, Haque SK, Batlle D. Angiotensinconverting enzyme 2-independent action of presumed angiotensinconverting enzyme 2 activators: studies in vivo, ex vivo, and in vitro. Hypertension 2014; 63:774-782.
29. Wysocki J, Ye M, Soler MJ, Gurley SB, Xiao HD, Bernstein KE, Coffman TM, Chen S, Batlle D. ACE and ACE2 activity in diabetic mice. Diabetes 2006; 55:2132-2139.
30. Velez JC. The importance of the intrarenal renin-angiotensin system. Nat Clin Pract Nephrol 2009; 5:89-100.
31. Navar LG, Harrison-Bernard LM, Nishiyama A, Kobori H. Regulation of intrarenal angiotensin II in hypertension. Hypertension 2002; 39:316-322.
32. Yun JC, Donahue JJ, Bartter FC, Kelly GD. Effect of pentobarbital anesthesia and laparotomy on plasma renin activity in the dog. Can J Physiol Pharmacol 1979; 57(4):412-416.
33. Velez JC, Ryan KJ, Harbeson CE, Bland AM, Budisavljevic MN, Arthur JM, Fitzgibbon WR, Raymond JR, Janech MG. Angiotensin I is largely converted to angiotensin (1-7) and angiotensin (2-10) by isolated rat glomeruli. Hypertension 2009; 53:790-797.
34. Hildebrand D, Merkel P, Eggers LF, Schlüter H. Proteolytic processing of angiotensin-I in human blood plasma. PLoS One 2013; 8:e64027.
35. Rice GI, Thomas DA, Grant PJ, Turner AJ, Hooper NM. Evaluation of angiotensin-converting enzyme (ACE), its homologue ACE2 and neprilysin in angiotensin peptide metabolism. Biochem J 2004; 383(Pt 1):45-51.
36. 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.
37. Kugler P. Aminopeptidase A is angiotensinase A. II. Biochemical studies on aminopeptidase A and M in rat kidney homogenate. Histochemistry 1982; 74:247-261.
38. Janssen BJ, De Celle T, Debets JJ, Brouns AE, Callahan MF, Smith TL. Effects of anesthetics on systemic hemodynamics in mice. Am J Physiol Heart Circ Physiol 2004; 287(4):H1618-H1624.
39. Schenk HD, Radke J, Ensink FB, Drobnik L, Kettler D, Sonntag H, Hellige G, Bretschneider HJ. Interactions between renal and general hemodynamics in fentanyl, droperidol, ketamine, thiopental and in peridural anesthesia-animal studies. Anaesthesiol Reanim 1995; 20(3):60-70.
40. Kitagawa H, Yamazaki T, Akiyama T, Mori H, Sunagawa K. Effects of ketamine on in vivo cardiac sympathetic nerve endings. J Cardiovasc Pharmacol 2001; 38(Suppl 1):S39-S42.
41. Xu Q, Ming Z, Dart AM, Du XJ. Optimizing dosage of ketamine and xylazine in murine echocardiography. Clin Exp Pharmacol Physiol 2007; 34(5-6):499-507.
42. Navar LG, Imig JD, Zou L, Wang CT. Intrarenal production of angiotensin II. Semin Neurol 1997; 17(5):412-422.
43. Campbell DJ, Lawrence AC, Towrie A, Kladis A, Valentijn AJ. Differential regulation of angiotensin peptide levels in plasma and kidney of the rat. Hypertension 1991; 18:763-773.
44. van Kats JP, Schalekamp MA, Verdouw PD, Duncker DJ, Danser AH. Intrarenal angiotensin II: interstitial and cellular levels and site of production. Kidney Int 2001; 60:2311-2317.
45. Siragy HM, Howell NL, Ragsdale NV, Carey RM. Renal interstitial fluid angiotensin. Modulation by anesthesia, epinephrine, sodium depletion, and renin inhibition. Hypertension 1995; 25:1021-1024.
46. Padia SH, Kemp BA, Howell NL, Gildea JJ, Keller SR, Carey RM. Intrarenal angiotensin III infusion induces natriuresis and angiotensin type 2 receptor translocation in Wistar-Kyoto but not in spontaneously hypertensive rats. Hypertension 2009; 53:338-343.
47. 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