Identification of prolyl carboxypeptidase as an alternative enzyme for processing of renal angiotensin II using mass spectrometry

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 10, 2013, Pages

  Grobe, Nadja ^a   Weir, Nathan M ^a   Leiva, Orly ^a   Ong, Frank S ^b   Bernstein, Kenneth E ^b   Schmaier, Alvin H ^c   Morris, Mariana ^a   Elased, Khalid M ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

Angiotensin converting enzyme 2; Angiotensinase C; Mass spectrometry; Prolyl endopeptidase; Renin angiotensin system

Indexed keywords

ANGIOTENSIN II; CARBOXYPEPTIDASE; KIDNEY ENZYME; PROLINE DERIVATIVE;

ANIMAL TISSUE; ARTICLE; CATALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; IMMUNOFLUORESCENCE; IN VITRO STUDY; KIDNEY; MALE; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR IMAGING; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEOMICS; RADIOIMMUNOASSAY; URINE; WESTERN BLOTTING;

ANGIOTENSIN-CONVERTING ENZYME 2; ANGIOTENSINASE C; MASS SPECTROMETRY; PROLYL ENDOPEPTIDASE; RENIN-ANGIOTENSIN SYSTEM;

ANGIOTENSIN I; ANGIOTENSIN II; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; CARBOXYPEPTIDASES; DIPEPTIDES; IMIDAZOLES; KIDNEY; LEUCINE; MALE; MICE; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

MUS;

EID: 84878664282     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00346.2012     Document Type: Article

References (62)

1. Abate N, Chandalia M, Cabo-Chan AV, Moe OW, Sakhaee K. The metabolic syndrome and uric acid nephrolithiasis: novel features of renal manifestation of insulin resistance. Kidney Int 65: 386-392, 2004.
2. Adams GN, LaRusch GA, Stavrou E, Zhou Y, Nieman MT, Jacobs GH, Cui Y, Lu Y, Jain MK, Mahdi F, Shariat-Madar Z, Okada Y, D'Alecy LG, Schmaier AH. Murine prolylcarboxypeptidase depletion induces vascular dysfunction with hypertension and faster arterial throm-bosis. Blood 117: 3929-3937, 2011.
3. Alghamri MS, Weir NM, Anstadt MP, Elased KM, Gurley SB, Morris M. Enhanced angiotensin II-induced cardiac and aortic remodeling in ACE2 knockout mice. J Cardiovasc Pharmacol Ther 18: 138-151, 2013.
4. Allred AJ, Diz DI, Ferrario CM, Chappell MC. Pathways for angio-tensin-(1-7) metabolism in pulmonary and renal tissues. Am J Physiol Renal Physiol 279: F841-F850, 2000.
5. Bakker AV, Jung S, Spencer RW, Vinick FJ, Faraci WS. Slow tight-binding inhibition of prolyl endopeptidase by benzyloxycarbonyl-prolyl-prolinal. Biochem J 271: 559-562, 1990.
6. Bindom SM, Hans CP, Xia H, Boulares AH, Lazartigues E. Angio-tensin I-converting enzyme type 2 (ACE2) gene therapy improves glyce-mic control in diabetic mice. Diabetes 59: 2540-2548, 2010.
7. +exchange and ammonium secretion. Am J Physiol Renal Physiol 294: F1315-F1322, 2008.
8. 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 417: 822-828, 2002.
9. Danilczyk U, Penninger JM. Angiotensin-converting enzyme II in the heart and the kidney. Circ Res 98: 463-471, 2006.
10. 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 carboxypepti-dase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 87: E1-E9, 2000.
11. Elased KM, Cool DR, Morris M. Novel mass spectrometric methods for evaluation of plasma angiotensin converting enzyme 1 and renin activity. Hypertension 46: 953-959, 2005.
12. Elased KM, Cunha TS, Gurley SB, Coffman TM, Morris M. New mass spectrometric assay for angiotensin-converting enzyme 2 activity. Hypertension 47: 1010-1017, 2006.
13. Feng Y, Xia H, Cai Y, Halabi CM, Becker LK, Santos RA, Speth RC, Sigmund CD, Lazartigues E. Brain-selective overexpression of human angiotensin-converting enzyme type 2 attenuates neurogenic hypertension. Circ Res 106: 373-382, 2010.
14. Giani JF, Munoz MC, Pons RA, Cao G, Toblli JE, Turyn D, Dominici FP. Angiotensin-(1-7) reduces proteinuria and diminishes structural dam-age in renal tissue of stroke-prone spontaneously hypertensive rats. Am J Physiol Renal Physiol 300: F272-F282, 2011.
15. Greis KD. Mass spectrometry for enzyme assays and inhibitor screening: an emerging application in pharmaceutical research. Mass Spectrom Rev 26: 324-339, 2007.
16. Grobe N, Elased KM, Cool DR, Morris M. Mass spectrometry for the molecular imaging of angiotensin metabolism in kidney. Am J Physiol Endocrinol Metab 302: E1016-E1024, 2012.
17. 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 116: 2218-2225, 2006.
18. Gurley SB, Clare SE, Snow KP, Hu A, Meyer TW, Coffman TM. Impact of genetic background on nephropathy in diabetic mice. Am J Physiol Renal Physiol 290: F214-F222, 2006.
19. Gurley SB, Coffman TM. Angiotensin-converting enzyme 2 gene tar-geting studies in mice: mixed messages. Exp Physiol 93: 538-542, 2008.
20. Guy JL, Jackson RM, Acharya KR, Sturrock ED, Hooper NM, Turner AJ. Angiotensin-converting enzyme-2 (ACE2): comparative modeling of the active site, specificity requirements, and chloride depen-dence. Biochemistry 42: 13185-13192, 2003.
21. Gwathmey TM, Pendergrass KD, Reid SD, Rose JC, Diz DI, Chappell MC. Angiotensin-(1-7)-angiotensin-converting enzyme 2 attenuates reac-tive oxygen species formation to angiotensin II within the cell nucleus. Hypertension 55: 166-171, 2010.
22. Huentelman MJ, Grobe JL, Vazquez J, Stewart JM, Mecca AP, Katovich MJ, Ferrario CM, Raizada MK. Protection from angiotensin II-induced cardiac hypertrophy and fibrosis by systemic lentiviral delivery of ACE2 in rats. Exp Physiol 90: 783-790, 2005.
23. Kawahara A, Enari M, Talanian RV, Wong WW, Nagata S. Fas-induced DNA fragmentation and proteolysis of nuclear proteins. Genes Cells 3: 297-306, 1998.
24. Liu C, Lv XH, Li HX, Cao X, Zhang F, Wang L, Yu M, Yang JK. Angiotensin-(1-7) suppresses oxidative stress and improves glucose up-take via Mas receptor in adipocytes. Acta Diabetol 49: 291-299, 2012.
25. Liu CX, Hu Q, Wang Y, Zhang W, Ma ZY, Feng JB, Wang R, Wang XP, Dong B, Gao F, Zhang MX, Zhang Y. Angiotensin-converting enzyme (ACE) 2 overexpression ameliorates glomerular injury in a rat model of diabetic nephropathy: a comparison with ACE inhibition. Mol Med 17: 59-69, 2011.
26. Luther JM, Brown NJ. The renin-angiotensin-aldosterone system and glucose homeostasis. Trends Pharmacol Sci 32: 734-739, 2011.
27. Maalouf NM, Cameron MA, Moe OW, Adams-Huet B, Sakhaee K. Low urine pH: a novel feature of the metabolic syndrome. Clin J Am Soc Nephrol 2: 883-888, 2007.
28. Maalouf NM, Cameron MA, Moe OW, Sakhaee K. Metabolic basis for low urine pH in type 2 diabetes. Clin J Am Soc Nephrol 5: 1277-1281, 2010.
29. Maes M, Monteleone P, Bencivenga R, Goossens F, Maj M, van WD, Bosmans E, Scharpe S. Lower serum activity of prolyl endopeptidase in anorexia and bulimia nervosa. Psychoneuroendocrinology 26: 17-26, 2001.
30. Monteiro MB, Senador D, Zhang WF, Morris M, Elased KM. Balance of ACE and ACE2 in diabetes: decreased renal ACE2 activity in hyper-tensive db/db diabetic mice. Hypertension 52: E91, 2008.
31. Nadarajah R, Milagres R, Dilauro M, Gutsol A, Xiao F, Zimpelmann J, Kennedy C, Wysocki J, Batlle D, Burns KD. Podocyte-specific overexpression of human angiotensin-converting enzyme 2 attenuates diabetic nephropathy in mice. Kidney Int 82: 292-303, 2012.
32. Odya CE, Marinkovic DV, Hammon KJ, Stewart TA, Erdos EG. Purification and properties of prolylcarboxypeptidase (angiotensinase C) from human kidney. J Biol Chem 253: 5927-5931, 1978.
33. Oudit GY, Liu GC, Zhong J, Basu R, Chow FL, Zhou J, Loibner H, Janzek E, Schuster M, Penninger JM, Herzenberg AM, Kassiri Z, Scholey JW. Human recombinant ACE2 reduces the progression of diabetic nephropathy. Diabetes 59: 529-538, 2010.
34. Patel VB, Bodiga S, Fan D, Das SK, Wang Z, Wang W, Basu R, Zhong J, Kassiri Z, Oudit GY. Cardioprotective effects mediated by angiotensin II type 1 receptor blockade and enhancing angiotensin 1-7 in experimental heart failure in angiotensin-converting enzyme 2-null mice. Hypertension 59: 1195-1203, 2012.
35. Rioli V, Kato A, Portaro FC, Cury GK, te Kaat K, Vincent B, Checler F, Camargo AC, Glucksman MJ, Roberts JL, Hirose S, Ferro ES. Neuropeptide specificity and inhibition of recombinant isoforms of the endopeptidase 342416 family: comparison with the related recombinant endopeptidase 342415. Biochem Biophys Res Commun 250: 5-11, 1998.
36. Rodriguez-Iturbe B, Pons H, Herrera-Acosta J, Johnson RJ. Role of immunocompetent cells in nonimmune renal diseases. Kidney Int 59: 1626-1640, 2001.
37. Schadock I, Todiras M, Vilianovich L, Qadri F, Heuser A, Siems WE, Santos RA, Bader M. Contribution of central angiotensin II to the hypertensive phenotype of prolylcarboxypeptidase knockout mice. Hyper-tension 58: E36, 2011.
38. Senanayake P, Moriguchi A, Kumagai H, Ganten D, Ferrario CM, Brosnihan KB. Increased expression of angiotensin peptides in the brain of transgenic hypertensive rats. Peptides 15: 919-926, 1994.
39. Skeggs LT Jr, Kahn JR, Shumway NP. The preparation and function of the hypertensin-converting enzyme. J Exp Med 103: 295-299, 1956.
40. Tan F, Morris PW, Skidgel RA, Erdös EG. Sequencing and cloning of human prolylcarboxypeptidase (angiotensinase C). Similarity to both ser-ine carboxypeptidase and prolylendopeptidase families. J Biol Chem 268: 16631-16638, 1993.
41. Taylor EN, Curhan GC. Body size and 24-hour urine composition. Am J Kidney Dis 48: 905-915, 2006.
42. Tikellis C, Bialkowski K, Pete J, Sheehy K, Su Q, Johnston C, Cooper ME, Thomas MC. ACE2 deficiency modifies renoprotection afforded by ACE inhibition in experimental diabetes. Diabetes 57: 1018-1025, 2008.
43. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ. A human homolog of angiotensin-converting enzyme. Cloning and func-tional expression as a captopril-insensitive carboxypeptidase. J Biol Chem 275: 33238-33243, 2000.
44. Velez JC. Prolyl carboxypeptidase: a forgotten kidney angiotensinase. Focus on "Identification of prolyl carboxypeptidase as an alternative enzyme for processing of renal angiotensin II using mass spectrometry." Am J Physiol Cell Physiol (April 3, 2013). doi:10.1152/ajpcell.00081.2013.
45. Velez JC, Ierardi JL, Bland AM, Morinelli TA, Arthur JM, Raymond JR, Janech MG. Enzymatic processing of angiotensin peptides by human glomerular endothelial cells. Am J Physiol Renal Physiol 302: F1583-F1594, 2012.
46. Verma A, Shan ZY, Lei B, Yuan LH, Liu X, Nakagawa T, Grant MB, Lewin AS, Hauswirth WW, Raizada MK, Li QH. ACE2 and ANG-(1-7) confer protection against development of diabetic retinopathy. Mol Ther 20: 28-36, 2012.
47. 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 en-zyme-related carboxypeptidase. J Biol Chem 277: 14838-14843, 2002.
48. Wallingford N, Perroud B, Gao Q, Coppola A, Gyengesi E, Liu ZW, Gao XB, Diament A, Haus KA, Shariat-Madar Z, Mahdi F, Wardlaw SL, Schmaier AH, Warden CH, Diano S. Prolylcarboxypeptidase reg-ulates food intake by inactivating α-MSH in rodents. J Clin Invest 119: 2291-2303, 2009.
49. Ward PE, Bausback HH, Odya CE. Kinin and angiotensin metabolism by purified renal post-proline cleaving enzyme. Biochem Pharmacol 36: 3187-3193, 1987.
50. Warden CH, Fisler JS, Espinal G, Graham J, Havel PJ, Perroud B. Maternal influence of prolyl endopeptidase on fat mass of adult progeny. Int J Obes (Lond) 33: 1013-1022, 2009.
51. Weir NM, Salem E, Grobe N, Yan ZY, Morris M, Elased KM. Renal angiotensin converting enzyme 2 protects kidney function during chronic ANG II infusion in mice. Hypertension 58: E79, 2011.
52. Welches WR, Brosnihan KB, Ferrario CM. A comparison of the properties and enzymatic activities of three angiotensin processing en-zymes: angiotensin converting enzyme, prolyl endopeptidase and nepri-lysin. Life Sci 52: 1461-1480, 1993.
53. Wong DW, Oudit GY, Reich H, Kassiri Z, Zhou J, Liu QC, Backx PH, Penninger JM, Herzenberg AM, Scholey JW. Loss of angiotensin-converting enzyme-2 (Ace2) accelerates diabetic kidney injury. Am J Pathol 171: 438-451, 2007.
54. Wysocki J, Ye M, Rodriguez E, Gonzalez-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 55: 90-98, 2010.
55. 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 55: 2132-2139, 2006.
56. Xiao L, Gao L, Lazartigues E, Zucker IH. Brain-selective overexpres-sion of angiotensin-converting enzyme 2 attenuates sympathetic nerve activity and enhances baroreflex function in chronic heart failure. Hyper-tension 58: 1057-1065, 2011.
57. Yamamoto K, Chappell MC, Brosnihan KB, Ferrario CM. In vivo metabolism of angiotensin I by neutral endopeptidase (EC 3.42411) in spontaneously hypertensive rats. Hypertension 19: 692-696, 1992.
58. Yamamoto K, Ohishi M, Katsuya T, Ito N, Ikushima M, Kaibe M, Tatara Y, Shiota A, Sugano S, Takeda S, Rakugi H, Ogihara T. Deletion of angiotensin-converting enzyme 2 accelerates pressure over-load-induced cardiac dysfunction by increasing local angiotensin II. Hy-pertension 47: 718-726, 2006.
59. Yamazato Y, Ferreira AJ, Hong KH, Sriramula S, Francis J, Yamazato M, Yuan L, Bradford CN, Shenoy V, Oh SP, Katovich MJ, Raizada MK. Prevention of pulmonary hypertension by angiotensin-converting enzyme 2 gene transfer. Hypertension 54: 365-371, 2009.
60. 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 43: 1120-1125, 2004.
61. Ye M, Wysocki J, William J, Soler MJ, Cokic I, Batlle D. Glomerular localization and expression of angiotensin-converting enzyme 2 and ang-iotensin-converting enzyme: implications for albuminuria in diabetes. J Am Soc Nephrol 17: 3067-3075, 2006.
62. Zhong J, Guo D, Chen CB, Wang W, Schuster M, Loibner H, Penninger JM, Scholey JW, Kassiri Z, Oudit GY. Prevention of angiotensin II-mediated renal oxidative stress, inflammation, and fibrosis by angiotensin-converting enzyme 2. Hypertension 57: 314-322, 2011.