Angiotensin-I converting enzyme (ACE): Structure, biological roles, and molecular basis for chloride ion dependence

Biological Chemistry

Volumn 395, Issue 10, 2014, Pages 1135-1149

  Masuyer, Geoffrey ^b   Yates, Christopher J ^a   Sturrock, Edward D ^a   Acharya, K Ravi ^b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b University of Bath   (United Kingdom)

Author keywords

Angiotensin I converting enzyme; Chloride activation; Hypertension

Indexed keywords

CHLORIDE ION; DIPEPTIDYL CARBOXYPEPTIDASE; CHLORIDE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR;

BINDING SITE; CONFERENCE PAPER; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; HUMAN; KALLIKREIN KININ SYSTEM; NONHUMAN; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; BINDING SITES; CHLORIDES; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; PEPTIDYL-DIPEPTIDASE A;

EID: 84926328056     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0157     Document Type: Conference Paper

References (130)

1. Abadir, P.M., Walston, J.D., and Carey, R.M. (2012). Subcellular characteristics of functional intracellular renin-angiotensin systems. Peptides 38, 437-445.
2. Andrade, M.C., Quinto, B.M., Carmona, A.K., Ribas, O.S., Boim, M.A., Schor, N., and Casarini, D.E. (1998). Purification and characterization of angiotensin I-converting enzymes from mesangial cells in culture. J. Hypertens. 16, 2063-2074.
3. Anthony, K.S., Corradi, H.R., Schwager, S.L., Redelinghuys, P., Georgiadis, D., Dive, V., Acharya, K.R. and Sturrock, E.D. (2010). The N domain of human angiotensin I-converting enzyme: the role of N-glycosylation and the crystal structure in complex with an N domain specific phosphinic inhibitor RXP407. J. Biol. Chem. 285, 35685-35693.
4. Anthony, C.S., Masuyer, G., Sturrock, E.D., and Acharya, K.R. (2012). Structure Based Drug Design of Angiotensin-I Converting Enzyme Inhibitors. Curr. Med. Chem. 19, 845-855.
5. Azizi, M., Rousseau, A., Ezan, E., Guyene, T.-T., Michelet, S., Grognet, J-M., Lenfant, M., Corvol, P., and Ménard, J. (1996). Acute angiotensin-converting enzyme inhibition increases the plasma level of the natural stem cell regulator N-acetyl-seryl-aspartyl- lysyl-proline. J. Clin. Invest. 97, 839-844.
6. Azizi, M., Ezan, E., Nicolet, L., Grognet, J.M., and Menard, J. (1997). High plasma level of N-acetyl-seryl-aspartyl-lysyl-proline: a new marker of chronic angiotensin-converting enzyme inhibition. Hypertension. 30, 1015-1019.
7. Barnes, K., Matsas, R., Hooper, N.M., Turner, A.J., and Kenny, A.J. (1988). Endopeptidase-24.11 is striosomally ordered in pig brain and, in contrast to aminopeptidase N and peptidyl dipeptidase A ('angiotensin converting enzyme'), is a marker for a set of striatal efferent fibres. Neuroscience. 27, 799-817.
8. Baudin, B. (2002). New aspects on angiotensin-converting enzyme: from gene to disease. Clin. Chem. Lab. Med. 40, 256-265.
9. Beneteau, B., Baudin, B., Morgant, G., Giboudeau, J., and Baumann, F.C. (1986). Automated kinetic assay of angiotensin-converting enzyme in serum. Clin. Chem. 32, 884-886.
10. Bernstein, K.E., Ong, F.S., Blackwell, W.L., Shah, K.H., Giani, J.F., Gonzalez-Villalobos, R.A., Shen, X.Z., Fuchs, S., Touyz, R.M. (2012). A modern understanding of the traditional and nontraditional biological functions of angiotensin-converting enzyme. Pharmacol. Rev. 65, 1-46.
11. Bernstein, K.E., Koronyo, Y., Salumbides, B.C., Sheyn, J., Pelissier, L., Lopes, D.H., Shah, K.H., Bernstein, E.A., Fuchs, D.T., Yu, J.J., et al. (2014). Angiotensin-converting enzyme overexpression in myelomonocytes prevents Alzheimer's-like cognitive decline. J. Clin. Invest. doi: 10.1172/JCI66541.
12. Bhoola, K.D., Figueroa, C.D., and Worthy, K. (1992). Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 44, 1-80.
13. Binevski, P.V., Sizova, E.A., Pozdnev, V.F., and Kost, O.A. (2003). Evidence for the negative cooperativity of the two active sites within bovine somatic angiotensin-converting enzyme. FEBS Lett. 550, 84-88.
14. Bonnet, D., Lemoine, F.M., Pontvert-Delucq, S., Baillou, C., Najman, A., and Guigon, M. (1993). Direct and reversible inhibitory effect of the tetrapeptide acetyl-N-Ser-Asp-Lys-Pro (Seraspenide) on the growth of human CD34+ subpopulations in response to growth factors. Blood. 82, 3307-3314.
15. Chai, S.Y., McKinley, M.J., and Mendelsohn, F.A. (1987). Distribution of angiotensin converting enzyme in sheep hypothalamus and medulla oblongata visualized by in vitro autoradiography. Clin. Exp. Hypertens. A. 9, 449-460.
16. Chen, Y.N., and Riordan, J.F. (1990). Identification of essential tyrosine and lysine residues in angiotensin converting enzyme: evidence for a single active site. Biochemistry 29, 10493-10498.
17. Corradi, R., Acharya, R.K., and Sturrock, E.D. (2006). Structure of testis ACE glycosylation mutants and evidence for conserved domain movement. Biochemistry 45, 12654-12663.
18. Corradi, H.R., Chitapi, I., Sewell, B.T., Georgiadis, D., Dive, V., Sturrock, E.D., and Acharya, K.R. (2007). The structure of testis angiotensin-converting enzyme in complex with the C -domainspecific inhibitor RXPA380. Biochemistry 46, 5473-5478.
19. Cristovam, P.C., Arnoni, C.P., Andrade, M.C., Casarini, D.E., Pereira, L.G., Schor, N., and Boim, M.A. (2008). Glucose-stimulated human mesangial cells ACE-dependent and chymase-dependent angiotensin II generation in normal and glucose-stimulated human mesangial cells. Exp. Biol. Med. 233, 1035-1043.
20. Csikós, T., Chung, O., and Unger, T. (1998). Receptors and their classification: focus on angiotensin II and the AT2 receptor. J. Hum. Hypertens. 12, 311-318.
21. Danilov, S., Balyasnikova, I.V., Albrecht, R.F., and Kost, O.A. (2008). Simultaneous determination of ACE activity with 2 substrates provides information on the status of somatic ACE and allows detection of inhibitors in human blood. J. Cardiovasc. Pharmacol. 52, 90-103.
22. De Koninck, Y. (2007). Altered chloride homeostasis in neurological disorders: a new target. Curr. Opin. Pharmacol. 7, 93-99.
23. Deddish, P.A., Wang, J., Michel, B., Morris, P.W., Davidson, N.O., Skidgel, R.A., and Erdös, E.G. (1994). Naturally occurring active N-domain of human angiotensin I-converting enzyme. Proc. Natl. Acad. Sci. USA 91, 7807-7811.
24. Defendini, R., Zimmerman, E.A., Weare, J.A., Alhenc-Gelas, F., and Erdös, E.G. (1983). Angiotensin-converting enzyme in epithelial and neuroepithelial cells. Neuroendocrinology 37, 32-40.
25. Douglas, R.G., Sharma, R.K., Masuyer, G., Lubbe, L., Zamora, I., Acharya, K.R., Chibale, K., and Sturrock, E.D. (2014). Fragment-based design for the development of N-domain-selective angiotensin- 1-converting enzyme inhibitors. Clin. Sci. (Lond.) 126, 305-313.
26. Dutzler, R., Campbell, E.B., Cadene, M., Chait, B.T., and MacKinnon, R. (2002). X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature 415, 287-294.
27. Ehlers, M.R. and Riordan, J.F. (1989). Angiotensin-converting enzyme: new concepts concerning its biological role. Biochemistry 28, 5311-5318.
28. Ehlers, M.R., Chen, Y.N., and Riordan, J.F. (1991). Purification and characterization of recombinant human testis angiotensinconverting enzyme expressed in Chinese hamster ovary cells. Protein. Expr. Purif. 2, 1-9.
29. Ehlers, M.R., Chen, Y.N., and Riordan, J.F. (1992). The unique N-terminal sequence of testis angiotensin-converting enzyme is heavily O-glycosylated and unessential for activity or stability. Biochem. Biophys. Res. Commun. 183, 199-205.
30. Ehlers, M.R., Schwager, S.L., Scholle, R.R., Manji, G.A., Brandt, W.F., and Riordan, J.F. (1996). Proteolytic release of membranebound angiotensin-converting enzyme: role of the juxtamembrane stalk sequence. Biochemistry 35, 9549-9559.
31. Elkins, J.S., Douglas, V.C., and Johnston, S.C. (2004). Alzheimer disease risk and genetic variation in ACE: a meta-analysis. Neurology. 62, 363-368.
32. Erdos, E.G. and Yang, H.Y. (1967). An enzyme in microsomal fraction of kidney that inactivates bradykinin. Life Sci. 6, 569-574.
33. Eriksson, U., Danilczyk, U., and Penninger, J.M. (2002). Just the beginning: novel functions for angiotensin-converting enzymes. Curr. Biol. 12, R745-R752.
34. Esther, C.R., Howard, T.E., Marino, E.M., Goddard, J.M., Capecchi, M.R., and Bernstein, K.E. (1996). Mice lacking angiotensinconverting enzyme have low blood pressure, renal pathology, and reduced male fertility. Lab. Invest. 74, 953-965.
35. Fernandez, M., Liu, X., Wouters, M.A., Heyberger, S., and Husain, A. (2001). Angiotensin I-converting enzyme transition state stabilization by HIS1089: evidence for a catalytic mechanism distinct from other gluzincin metalloproteinases. J. Biol. Chem. 276, 4998-5004.
36. Fuchs, S., Xiao, H.D., Cole, J.M., Adams, J.W., Frenzel, K., Michaud, A., Zhao, H., Keshelava, G., Capecchi, M.R., Corvol, P., and Bernstein, K.E. (2004). Role of the N-terminal catalytic domain of angiotensin-converting enzyme investigated by targeted inactivation in mice. J. Biol. Chem. 279, 15946-15953.
37. Fuchs, S., Frenzel, K., Hubert, C., Lyng, R., Muller, L., Michaud, A., Xiao, H.D., Adams, J.W., Capecchi, M.R., Corvol, P., et al. (2005). Male fertility is dependent on dipeptidase activity of testis ACE. Nat. Med. 11, 1140-1142.
38. Fuchs, S., Xiao, H.D., Hubert, C., Michaud, A., Campbell, D.J., Adams, J.W., Capecchi, M.R., Corvol, P., and Bernstein, K.E. (2008). Angiotensin-converting enzyme C-terminal catalytic domain is the main site of angiotensin I cleavage in vivo. Hypertension 51, 267-274.
39. Gasparo, M., Husain, A., Alexander, W., Catt, K.J., Chiu, A.T., Drew, M., Goodfriend, T., Harding, J.W., Inagami, T., and Timmermans, P.B. (1995). Proposed update of angiotensin receptor nomenclature. Hypertension 25, 924-927.
40. Goldblatt, H., Lynch, J., Hanzal, R.F., and Summerville, W.N. (1934). Studies on experimental hypertension.I. The production of persistent elevation of systolic blood pressure by means of renal ischemia. J. Exp. Med. 59, 347-379.
41. Gonzalez-Villalobos, R.A., Shen, X.Z., Bernstein, E.A., Janjulia, T., Taylor, B., Giani, J.F., Blackwell, W.L., Shah, K.H., Shi, P.D., Fuchs, S., et al. (2013). Rediscovering ACE: novel insights into the many roles of the angiotensin-converting enzyme. J. Mol. Med. (Berl.) 91, 1143-1154.
42. Guimara&tild;es, P.B., Alvarenga, É.C., Siqueira, P.D., Paredes-Gamero, E.J., Sabatini, R.A., Morais, R.L., Reis, R.I., Santos, E.L., Teixeira, L.G., Casarini, D.E., et al. (2011). Angiotensin II binding to angiotensin I-converting enzyme triggers calcium signaling. Hypertension. 57, 965-972.
43. Guy, J.L., Jackson, R.M., Acharya, K.R., Sturrock, E.D., Hooper, N.M., and Turner, A.J. (2003). Angiotensin-converting enzyme-2 (ACE2): comparative modeling of the active site, specificity requirements, and chloride dependence. Biochemistry 42, 13185-13192.
44. Hagaman, J.R., Moyer, J.S., Bachman, E.S., Sibony, M., Magyar, P.L., Welch, J.E., Smithies, O., Krege, J.H., and O'Brien, D.A. (1998). Angiotensin-converting enzyme and male fertility. Proc. Natl. Acad. Sci. USA 95, 2552-2557.
45. Hanesworth, J.M., Sardinia, M.F., Krebs, L.T., Hall, K.L., and Harding, J.W. (1993). Elucidation of a specific binding site for angiotensin II(3-8), angiotensin IV, in mammalian heart membranes. J. Pharmacol. Exp. Ther. 266, 1036-1042.
46. Hemming, M.L. and Selkoe, D.J. (2005). Amyloid β-protein is degraded by cellular angiotensin-converting enzyme (ACE) and elevated by an ACE inhibitor. J. Biol. Chem. 280, 37644-37650.
47. Hille, B. (1992). Ionic channels of excitable membranes (Sunderland, MA, Sinauer Associates).
48. Ho, B.K., and Gruswitz, F. (2008). HOLLOW: Generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct. Biol. 8, 49.
49. Holmquist, B., Bünning, P., and Riordan, J.F. (1979). A continuous spectrophotometric assay for angiotensin converting enzyme. Anal. Biochem. 95, 540-548.
50. Horiuchi, M. (1996). Functional aspects of angiotensin type 2 receptor. Adv. Exp. Med. Biol. 396, 217-224.
51. Houssay, B.A. and Fasciolo, J.C. (1937). Secretion hipertensora del rinon isquemaido. Rev. Soc. Argent. Biol. 13, 284-294.
52. Howard, T.E., Shai, S.Y., Langford, K.G., Martin, B.M., and Bernstein, K.E. (1990). Transcription of testicular angiotensin-converting enzyme (ACE) is initiated within the 12th intron of the somatic ACE gene. Mol. Cell Biol. 10, 4294-4302.
53. Hubert, C., Houot, A.M., Corvol, P., and Soubrier, F. (1991). Structure of the angiotensin I-converting enzyme gene. Two alternate promoters correspond to evolutionary steps of a duplicated gene. J. Biol.Chem. 266, 15377-15383.
54. Inagami, T. (1994). The renin-angiotensin system. Essays Biochem. 28, 147-164.
55. Inoue, H., Mori, S., Morishima, S., and Okada, Y. (2005). Volumesensitive chloride channels in mouse cortical neurons: characterization and role in volume regulation. Eur. J. Neurosci. 21, 1648-1658.
56. Jaspard, E., Wei, L., and Alhenc-Gelas, F. (1993). Differences in the properties and enzymatic specificities of the two active sites of angiotensin I-converting enzyme (kininase II). Studies with bradykinin and other natural peptides. J. Biol. Chem. 268, 9496-9503.
57. Jenkins, T.A., Mendelsohn, F.A., and Chai, S.Y. (1997). Angiotensinconverting enzyme modulates dopamine turnover in the striatum. J. Neurochem. 68, 1304-1311.
58. Jeyendran, R.S., Van der Ven, H.H., Rosecrans, R., Perez-Pelaez, M., Al-Hasani, S., and Zaneveld, L.J.D. (1989). Chemical constituents of human seminal plasma: relationship to fertility. Andrologia 21, 423-428.
59. Junot, C., Gonzales, M.F., Ezan, E., Cotton, J., Vazeux, G., Michaud, A., Azizi, M., Vassiliou, S., Yiotakis, A., Corvol, P., et al. (2001). RXP 407, a selective inhibitor of the N-domain of angiotensin I-converting enzyme, blocks in vivo the degradation of hemoregulatory peptide acetyl-Ser-Asp-Lys-Pro with no effect on angiotensin I hydrolysis. J. Pharmacol. Exp. Ther. 297, 606-611.
60. Kehoe, P.G., Russ, C., McIlory, S., Williams, H., Holmans, P., Holmes, C., Liolitsa, D., Vahidassr, D., Powell, J., McGleenon, B. et al. (1999). Variation in DCP1, encoding ACE, is associated with susceptibility to Alzheimer disease. Nat. Genet. 21, 71-72.
61. Krege, J.H., John, S.W., Langenbach, L.L., Hodgin, J.B., Hagaman, J.R., Bachman, E.S., Jennette, J.C., O'Brien, D.A., and Smithies, O. (1995). Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 375, 146-148.
62. Kroger, W.L., Douglas, R.G., O'Neill, H.G., Dive, V. and Sturrock, E.D. (2009). Investigating the domain specificity of phosphinic inhibitors RXPA380 and RXP407 in angiotensin-converting enzyme. Biochemistry 48, 8405-8412.
63. Kroeger, D., Tamburri, A., Amzica, F., and Sík, A. (2010). Activitydependent layer-specific changes in the extracellular chloride concentration and chloride driving force in the rat hippocampus. J. Neurophysiol. 103, 1905-1914.
64. Lazard, D., Briend-Sutren, M.M., Villageois, P., Mattei, M.G., Strosberg, A.D., and Nahmias, C. (1994). Molecular characterization and chromosome localization of a human angiotensin I AT2 receptor gene highly expressed in fetal tissues. Receptors Channels 2, 271-280.
65. Lehmann, D.J., Cortina-Borja, M., Warden, D.R., Smith, A.D., Sleegers, K., Prince, J.A., van Duijn, C.M., and Kehoe, P.G. (2005). Large meta-analysis establishes the ACE insertiondeletion polymorphism as a marker of Alzheimer's disease. Am. J. Epidemiol. 162, 305-317.
66. Lenfant, M., Wdzieczak-Bakala, J., Guittet, E., Prome, J.C., Sotty, D., and Frindel, E. (1989). Inhibitor of hematopoietic pluripotent stem cell proliferation: purification and determination of its structure. Proc. Natl. Acad. Sci. USA 86, 779-782.
67. Liu, X., Fernandez, M., Wouters, M.A., Heyberger, S., and Husain, A. (2001). Arg(1098) is critical for the chloride dependence of human angiotensin I-converting enzyme C-domain catalytic activity. J. Biol. Chem. 276, 33518-33525.
68. Lodish, H.F. (1999). Molecular Cell Biology (NY, USA: Freeman, W.H).
69. Masuyer, G., Schwager, S.L., Sturrock, E.D., Isaac, R.E., and Acharya, K.R. (2012). Molecular recognition and regulation of human angiotensin-I converting enzyme (ACE) activity by natural inhibitory peptides Sci. Rep. 2, 717.
70. Matsas, R., Kenny, A.J., and Turner, A.J. (1984). The metabolism of neuropeptides. The hydrolysis of peptides, including enkephalins, tachykinins and their analogues, by endopeptidase-24.11. Biochem. J. 223, 433-440.
71. Matthews, B.W. (1988). Structural basis of the action of thermolysin and related zinc peptidases. Acc. Chem. Res. 21, 333-340.
72. McKinley, M.J., Albiston, A.L., Allen, A.M., Mathai, M.L., May, C.N., McAllen, R.M, Oldfield, B.J., Mendelsohn, F.A., and Chai, S.Y. (2003). The brain renin-angiotensin system: location and physiological roles. Int. J. Biochem. Cell Biol. 35, 901-918.
73. Michaud, A., Williams T.A., Chauvet, M.T., and Corvol, P. (1997). Substrate dependence of angiotensin I-converting enzyme inhibition: captopril displays a partial selectivity for inhibition of N-Acetyl-Seryl-Aspartyl-Lysyl-Proline hydrolysis compared with that of angiotensin. Mol. Pharmacol. 51, 1070-1076.
74. Moiseeva, N.A., Binevski, P.V., Baskin, I.I., Palyulin, V.A. and Kost, O.A. (2005). Role of two chloride-binding sites in functioning of testicular angiotensin-converting enzyme. Biochemistry (Mosc.) 70, 1167-1172.
75. Natesh, R., Schwager, S.L.U., Sturrock, E.D., and Acharya, K.R. (2003). Crystal structure of the human angiotensin-converting enzyme-lisinopril complex. Nature 421, 551-554.
76. Natesh, R., Schwager, S.L., Evans, H.R., Sturrock, E.D., and Acharya, K.R. (2004). Structural details on the binding of antihypertensive drugs captopril and enalaprilat to human testicular angiotensin I-converting enzyme. Biochemistry 43, 8718-8724.
77. O'Neill, H.G., Redelinghuys, P., Schwager, S.L., and Sturrock, E.D. (2008). The role of glycosylation and domain interactions in the thermal stability of human angiotensin-converting enzyme. Biol. Chem. 389, 1153-1161.
78. Oba, R., Igarashi, A., Kamata, M., Nagata, K., Takano, S., and Nakagawa, H. (2005). The N-terminal active centre of human angiotensin-converting enzyme degrades Alzheimer amyloid β-peptide. Eur. J. Neurosci. 21, 733-740.
79. Oblin, A., Danse, M.J., and Zivkovic, B. (1988). Degradation of substance P by membrane peptidases in the rat substantia nigra: effect of selective inhibitors. Neurosci. Lett. 84, 91-96.
80. Okwan-Duodu, D., Datta, V., Shen, X.Z., Goodridge, H.S., Bernstein, E.A., Fuchs, S., Liu, G.Y., and Bernstein, K.E. (2010). Angiotensin-converting enzyme overexpression in mouse myelomonocytic cells augments resistance to Listeria and methicillin-resistant Staphylococcus aureus. J. Biol. Chem. 285, 39051-39060.
81. Page, I.H. and Helmer, O.M. (1940). A crystalline pressor substance (angiotonin) resulting from the interaction between renin and renin activator. J. Exp. Med. 71, 29.
82. Peng, H., Carretero, O.A., Peterson, E.L., and Rhaleb, N-E. (2010). Ac-SDKP inhibits transforming growth factor-β 1-induced differentiation of human cardiac fibroblasts into myofibroblasts. Am. J. Physiol. Heart. Circ. Physiol. 298, H1357-H1364.
83. Rasoul, S., Carretero, O.A., Peng, H., Cavasin, M.A., Zhuo, J., Sanchez-Mendoza, A., Brigstock, D.R., and Rhaleb, N.E. (2004). Antifibrotic effect of Ac-SDKP and angiotensin-converting enzyme inhibition in hypertension. J. Hypertens. 22, 593-603.
84. Regoli, D., Rhaleb, N.E., Drapeau, G., Dion, S., Tousignant, C., D'Orléans-Juste, P., and Devillier, P. (1989). Basic pharmacology of kinins: pharmacologic receptors and other mechanisms. Adv. Exp. Med. Biol. 247A, 399-407.
85. Rice, G.I., Thomas, D.A., Grant, P.J., Turner, A.J., and Hooper, N.M. (2004). Evaluation of angiotensin converting enzyme (ACE), its homologue ACE2 and neprilysin in angiotensin peptide metabolism. Biochem. J. 383, 45-51.
86. Rigat, B., Hubert, C., Alhenc-Gelas, F., Cambien, F., Corvol, P., and Soubrier, F. (1990). An insertion/deletion polymorphism in the angiotensin I-converting enzyme gene accounting for half the variance of serum enzyme levels. J. Clin. Invest. 86, 1343-1346.
87. Rosecrans, R.R., Jeyendran, R.S., Perez-Pelaez, M., and Kennedy W.P. (1987). Comparison of biochemical parameters of human blood serum and seminal plasma. Andrologia 19, 625-628.
88. Rousseau, A., Michaud, A., Chauvet, M.T., and Corvol, P. (1995). The hemoregulatory peptide N-acetyl-Ser-Asp-Lys-Pro is a natural and specific substrate of the N-terminal active site of human angiotensin-converting enzyme. J. Biol. Chem. 270, 3656-3661.
89. Rousseau-Plasse, A., Lenfant, M., and Potier, P. (1996). Catabolism of the hemoregulatory peptide N-Acetyl-Ser-Asp-Lys-Pro: a new insight into the physiological role of the angiotensin-I-converting enzyme N-active site. Bioorg. Med. Chem. 4, 1113-1119.
90. Rushworth, C.A., Guy, J.L., and Turner, A.J. (2008). Residues affecting the chloride regulation and substrate selectivity of the angiotensin-converting enzymes (ACE and ACE2) identified by site-directed mutagenesis. FEBS J. 275, 6033-6042.
91. Sadhukhan, R. and Sen, I. (1996). Different glycosylation requirements for the synthesis of enzymatically active angiotensinconverting enzyme in mammalian cells and yeast. J. Biol. Chem. 271, 6429-6434.
92. Sasaguri, M., Ideishi, M., Ogata, S., Miura, S., Ikeda, M., and Arakawa, K. (1995). Human urinary kallikrein can generate angiotensin II from homologous renin substrates. Hypertens. Res. 18, 33-37.
93. Savaskan, E. (2005). The role of the brain renin-angiotensin system in neurodegenerative disorders. Curr. Alzheimer Res. 2, 29-35.
94. Sealey, J.E., Atlas, S.A., Laragh, J.H., Silverberg, M., and Kaplan, A.P. (1979). Initiation of plasma prorenin activation by Hageman factor-dependent conversion of plasma prekallikrein to kallikrein. Proc. Natl. Acad. Sci. USA 76, 5914-5918.
95. Sen, I., Kasturi, S., Abdul Jabbar, M., and Sen, G.C. (1993). Mutations in two specific residues of testicular angiotensin-converting enzyme change its catalytic properties. J. Biol. Chem. 268, 25748-25754.
96. Shanmugam, S. and Sandberg, K. (1996). Ontogeny of angiotensin II receptors. Cell Biol. Int. 20, 169-176.
97. Shapiro, R. and Riordan J.F. (1984). Inhibition of angiotensin converting enzyme: mechanism and substrate dependence. Biochemistry 23, 5225-5233.
98. Shapiro, R., Holmquist, B., and Riordan, J.F. (1983). Anion activation of angiotensin converting enzyme: dependence on nature of substrate. Biochemistry 22, 3850-3857.
99. Shen, X.Z., Li, P., Weiss, D., Fuchs, S., Xiao, H.D., Adams, J.A., Williams, I.R., Capecchi, M.R., Taylor, W.R., and Bernstein, K.E. (2007). Mice with enhanced macrophage angiotensinconverting enzyme are resistant to melanoma. Am. J. Pathol. 170, 2122-2134.
100. Shen, X.Z., Lukacher, A.E., Billet, S., Williams, I.R., and Bernstein, K.E. (2008). Expression of angiotensin-converting enzyme changes major histocompatibility complex class I peptide presentation by modifying C-termini of peptide precursors. J. Biol. Chem. 283, 9957-9965.
101. Shen, X.Z., Billet, S., Lin, C., Okwan-Duodu, D., Chen, X., Lukacher, A.E., and Bernstein, K.E. (2011). The carboxypeptidase ACE shapes the MHC class I peptide repertoire. Nat. Immunol. 12, 1078-1085.
102. Sibony, M., Gasc, J.M., Soubrier, F., Alhenc-Gelas, F., and Corvol, P. (1993). Gene expression and tissue localization of the two isoforms of angiotensin I converting enzyme. Hypertension 21, 827-835.
103. Skeggs, L.T., Marsh, W.H., Kahn, J.R., and Shumway, N.P. (1954). The purification of hypertensin I. J. Exp. Med. 100, 363-370.
104. Skeggs, L.T., Kahn, J.R., and Shumway, N.P. (1956). The preparation and function of the hypertensin-converting enzyme. J. Exp. Med. 103, 295-299.
105. Skidgel, R.A. and Erdös, E.G. (1985). Novel activity of human angiotensin I converting enzyme: release of the NH2- and COOHterminal tripeptides from the luteinizing hormone-releasing hormone. Proc. Natl. Acad. Sci. USA 82, 1025-1029.
106. Skidgel, R.A. and Erdös, E.G. (2004). Angiotensin converting enzyme (ACE) and neprilysin hydrolyze neuropeptides: a brief history, the beginning and follow-ups to early studies. Peptides 25, 521-525.
107. Skidgel, R.A., Defendini, R., and Erdos, E.G. (1987). In: Neuropeptides and their Neuropeptidases. A.J. Turner, ed. (Chichester, UK: V.C.H. Ellis- Horwood), pp. 165-182.
108. Soubrier, F., Alhenc-Gelas, F., Hubert, C., Allegrini, J., John, M., Tregear, G., and Corvol, P. (1988). Two putative active centers in human angiotensin I-converting enzyme revealed by molecular cloning. Proc. Natl. Acad. Sci. USA 85, 9386-9390.
109. Strittmatter, S.M., Lo, M.M., Javitch, J.A., and Snyder, S.H. (1984). Autoradiographic visualization of angiotensin-converting enzyme in rat brain with [3H]captopril: localization to a striatonigral pathway. Proc. Natl. Acad. Sci. USA 81, 1599-1603.
110. Sturrock, E.D., Natesh, R., van Rooyen, J.M., and Acharya, K.R. (2004). Structure of angiotensin I-converting enzyme. Cell. Mol. Life Sci. 61, 2677-2686.
111. Takada, Y., Hiwada, K., Akutsu, H., Hashimoto, A., and Kokubu, T. (1984). The immunocytochemical detection of angiotensinconverting enzyme in alveolar macrophages from patients with sarcoidosis. Lung 162, 317-323.
112. Timmermans, P.B., Benfield, P., Chiu, A.T., Herblin, W.F., Wong, P.C., and Smith, R.D. (1992). Angiotensin II receptors and functional correlates. Am. J. Hypertens. 5, 221S-235S.
113. Timmermans, P.B., Wong, P.C., Chiu, A.T., Herblin, W.F., Benfield, P., Carini, D.J., Lee, R.J., Wexler, R.R., Saye, J.A., and Smith, R.D. (1993). Angiotensin II receptors and angiotensin II receptor antagonists. Pharmacol. Rev. 45, 205-251.
114. Turner, A.J. and Hooper, N.M. (2002). The angiotensin-converting enzyme gene family: genomics and pharmacology. Trends Pharmacol. Sci. 23, 177-183.
115. Tzakos, A.G., Galanis, A.S., Spyroulias, G.A., Cordopatis, P., Manessi-Zoupa, E., and Gerothanassis, I.P. (2003). Structurefunction discrimination of the N- and C- catalytic domains of human angiotensin-converting enzyme: implications for Cl- activation and peptide hydrolysis mechanisms. Protein Eng. 16, 993-1003.
116. van den Buuse, M., Zheng, T.W., Walker, L.L., and Denton, D.A. (2005). Angiotensin-converting enzyme (ACE) interacts with dopaminergic mechanisms in the brain to modulate prepulse inhibition in mice. Neurosci. Lett. 380, 6-11.
117. Voronov, S., Zueva, N., Orlov, V., Arutyunyan, A., and Kost, O. (2002). Temperature-induced selective death of the C-domain within angiotensin-converting enzyme molecule. FEBS Lett. 522, 77-82.
118. Wang, D., Carretero, O.A., Yang, X.Y., Rhaleb, N.-E., Liu, Y.-H., Liao, T.-D., and Yang, X.-P. (2004). N-acetyl-seryl-aspartyl-lysyl proline stimulates angiogenesis in vitro and in vivo. Am. J. Physiol. Heart. Circ. Physiol. 287, H2099-H2105.
119. Watermeyer, J.M., Sewell, B.T., Schwager, S.L., Natesh, R., Corradi, H.R., Acharya, K.R., and Strurrock, E.D. (2006). Structure of testis ACE glycosylation mutants and evidence for conserved domain movement. Biochemistry 45, 12654-12663.
120. Wei, L., Alhenc-Gelas, F., Corvol, P., and Clauser, E. (1991a). The two homologous domains of human angiotensin I-converting enzyme are both catalytically active. J. Biol. Chem. 266, 9002-9008.
121. Wei, L., Alhenc-Gelas, F., Soubrier, F., Michaud, A., Corvol, P., and Clauser, E. (1991b). Expression and characterization of recombinant human angiotensin I-converting enzyme. Evidence for a C-terminal transmembrane anchor and for a proteolytic processing of the secreted recombinant and plasma enzymes. J. Biol. Chem. 266, 5540-5546.
122. Wei, L., Clauser, E., Alhenc-Gelas, F., and Corvol, P. (1992). The two homologous domains of human angiotensin I-converting enzyme interact differently with competitive inhibitors. J. Biol. Chem. 267, 13398-13405.
123. Woodman, Z.L., Oppong, S.Y., Cook, S., Hooper, N.M., Schwager, S.L.U., Brandt, W.F., Ehlers, M.R.W., and Sturrock, E.D. (2000). Shedding of somatic angiotensin-converting enzyme (ACE) is inefficient compared with testis ACE despite cleavage at identical stalk sites. Biochemical J. 347, 711-718.
124. Wright, J.W. and Harding, J.W. (2004). The brain angiotensin system and extracellular matrix molecules in neural plasticity, learning, and memory. Progr. Neurobiol. 72, 263-293.
125. Yamaguchi, T., Carretero, O.A., and Scicli, A.G. (1991). A novel serine protease with vasoconstrictor activity coded by the kallikrein gene S3. J. Biol. Chem. 266, 5011-5017.
126. Yang, H.Y., Erdös, E.G., and Levin, Y. (1970). A dipeptidyl carboxypeptidase that converts angiotensin I and inactivates bradykinin. Biochim. Biophys. Acta 214, 374-376.
127. Yang, H.Y., Erdös, E.G., and Levin, Y. (1971). Characterization of a dipeptide hydrolase (kininase II: angiotensin I converting enzyme). J. Pharmacol. Exp. Ther. 177, 291-300.
128. Yates, C.J., Masuyer, G., Schwager, S.L., Akif, M., Sturrock, E.D., and Acharya, K.R. (2014). Molecular and thermodynamic mechanisms of the chloride-dependent human angiotensin-I-converting enzyme (ACE). J. Biol Chem. 289, 1798-1814.
129. Yu, X.C., Sturrock, E.D., Wu, Z.C., Biemann, K., Ehlers, M.R.W., and Riordan, J.F. (1997). Identification of N-linked glycosylation sites in human testis angiotensin-converting enzyme and expression of an active deglycosylated forms. J. Biol. Chem. 272, 3511-3519.
130. Zou, K., Yamaguchi, H., Akatsu, H., Sakamoto, T., Ko, M., Mizoguchi, K., Gong, J.S., Yu, W., Yamamoto, T., Kosaka, K., et al. (2007). Angiotensin-converting enzyme converts amyloid beta-protein 1-42 (Aβ(1-42)) to Aβ(1-40), and its inhibition enhances brain Aβ deposition. J. Neurosci. 27, 8628-8635.