(Circulation. 1995;92:1387-1388.)
© 1995 American Heart Association, Inc.
Articles |
Angiotensin-Converting Enzyme in the Human Heart
Effect of the Deletion/Insertion Polymorphism
From the Cardiovasculair Onderzoeksinstituut Erasmus Universiteit Rotterdam (COEUR), Erasmus University, Rotterdam, Netherlands (A.H.J.D., M.A.D.H.S., W.A.B., A.M.vdB., P.R.S.), and the Medizinische Klinik II, University of Regensburg, Germany (G.A.J.R., H.S.).
Correspondence to A.H. Jan Danser, PhD, COEUR/Department of Pharmacology, Room EE1418b, Erasmus University, Dr Molewaterplein 50, 3015 GE Rotterdam, Netherlands.
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Abstract |
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 Top Abstract IntroductionMethods Results Discussion References |
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Background An insertion (I)/deletion (D) polymorphism of the angiotensin-converting enzyme (ACE) gene has been associated with differences in the plasma levels of ACE as well as with myocardial infarction, cardiomyopathy, left ventricular hypertrophy, and coronary artery disease.
Methods and Results We determined the cardiac ACE activity and the ACE genotype in 71 subjects who died of noncardiac disorders. Cardiac ACE activity was significantly higher (P<.01) in subjects with the ACE DD genotype (12.7±1.9 mU/g wet wt) compared with subjects with the ID (8.7±0.8 mU/g) and the II (9.1±1.0 mU/g) genotypes. This difference was independent of sex, age, and the time required for tissue collection.
Conclusions Cardiac ACE activity is highest in subjects with the DD genotype. Elevated cardiac ACE activity in these subjects may result in increased cardiac angiotensin II levels, and this may be a mechanism underlying the reported association between the ACE deletion polymorphism and the increased risk for several cardiovascular disorders.
Key Words: genetics • angiotensin
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Introduction |
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TopAbstractIntroductionMethods Results Discussion References |
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A deletion polymorphism in the gene encoding angiotensin-converting enzyme (ACE) has been associated with an increased risk of myocardial infarction,1 cardiomyopathy,2 3 left ventricular hypertrophy,4 and coronary artery disease.5 However, these associations could not be confirmed in all studies,6 7 and the mechanism underlying this increased genetic risk remains unclear.
Plasma ACE levels are known to be elevated in subjects homozygous for the deletion allele (DD) compared with heterozygotes (ID) or subjects homozygous for the insertion (II) allele.8 ACE levels in human T lymphocytes are genetically determined in a similar way.9
At present, no information is available on the ACE activity of cardiac tissue in relation to the deletion/insertion ACE genotype. We determined ACE activity and genotype in human cardiac tissue so as to study whether the cardiac ACE level is, in part, genetically determined as well.
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Methods |
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TopAbstractIntroductionMethods Results Discussion References |
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Subjects
Left ventricular cardiac tissue was obtained from 71 organ donors (38 men and 33 women 1 to 54 years old; median, 35 years) who died of noncardiac disorders (29 cerebrovascular accident, 32 polytrauma, 7 cerebral hypoxia, 1 encephalitis, 1 meningitis, and 1 hydrocephalus). The donor hearts were provided by the Rotterdam Heart Valve Bank (Bio Implant Services Foundation/Eurotransplant Foundation). Immediately after circulatory arrest, the hearts were stored at 0°C to 4°C in a sterile organ-protecting solution (University of Wisconsin, EuroCollins, or HTK-Bretschneider solution) for a maximum of 24 hours (cold ischemia time). After the aortic and pulmonary valves had been excised for homograft valve transplantation,
1 to 3 g of left ventricular free
wall was removed and stored at -70°C.
ACE Activity
Frozen tissue (100 to 200 mg) was homogenized
with a Polytron PT10/35 (Kinematica) in 1 mL 0.01 mol/L phosphate
buffer, pH 7.4, containing 0.15 mol/L NaCl. ACE activity in the
homogenate was measured in duplicate with a commercial kit
(ACEcolor, Fujirebio) containing
p-hydroxybenzoyl-glycyl-L-histidyl-L-leucine
as synthetic substrate.10 Multiple dilutions (50- or
100-µL aliquots containing 1 and 2 mg protein, respectively) of
the homogenate were incubated for 2 hours with 10 mmol/L
substrate (total incubation volume, 300 µL) at 37°C and pH 8.3.
Incubations of homogenate with substrate in the presence of
3.0 mmol/L disodium-EDTA served as blanks. After 2 hours, the reaction
of ACE on the synthetic substrate was stopped by addition of 750 µL
stopper/developer solution containing 3 mmol/L disodium-EDTA. The tubes
were mixed, incubated at 37°C for 10 minutes to allow formation of
index color from the converted substrate, and centrifuged at
3000g for 5 minutes at room temperature. Absorbance was then
read at 505 nm.
Generation of p-hydroxybenzoic acid over time
was linear,
and ACE activity, expressed as nanomoles of
p-hydroxybenzoic acid per minute per gram of tissue (or
milliunits per gram of tissue), was not different for the samples
containing 1 and 2 mg protein. The lower limit of detection was
1.5 mU/g tissue.
ACE Genotyping
To extract genomic DNA, 50 to 100 mg of left
ventricular tissue was homogenized in a buffer
containing 155 mmol/L ammonium chloride, 10 mmol/L potassium carbonate,
and 0.1 mmol/L EDTA (pH 8.0). The homogenate was then
centrifuged at 6000 rpm for 15 minutes at 4°C, and the
resulting supernatant (0.5 mL) was diluted in 4.5 mL of the same
buffer, incubated at 0°C for 10 minutes, and centrifuged at
13 000 rpm for 15 minutes at 4°C. The pellet was resuspended in 100
µL 10 mmol/L Tris-HCl buffer, pH 8.0, containing 1 mmol/L
disodium-EDTA, subjected to proteinase K digestion, and
ethanol-precipitated as described previously.4 The
genotype was then determined by the polymerase chain reaction
(PCR) and subsequent gel electrophoresis of the PCR
products.4 The laboratory responsible for genotyping
was blinded for values of cardiac ACE activity.
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Results |
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TopAbstractIntroductionMethods Results Discussion References |
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The distribution of the ACE genotypes in the present population was not different from that reported previously for normal populations.1 3 4 The frequency of the D allele was 0.53. Cardiac ACE activity (expressed per gram wet weight) was in the same range as plasma ACE activity measured normally in our laboratory (7 to 20 mU/mL), which indicates that the presence of ACE in cardiac tissue cannot be attributed to trapped blood plasma. Cardiac ACE activity (expressed per gram wet weight or per gram protein) was significantly higher in subjects with the DD genotype (Table
; P<.02 versus ID,
P<.01 versus ID+II). The difference remained statistically
significant (P<.01) after correction for sex, age, and cold
ischemia time. No difference in cardiac ACE activity was found
between subjects with the ID and the II genotypes.
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Discussion |
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TopAbstractIntroductionMethods Results Discussion References |
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Our results show that in subjects with the DD genotype in whom plasma ACE is known to be elevated, cardiac ACE activity is elevated as well. Previous studies in experimental animals have demonstrated that cardiac ACE activity is closely correlated with cardiac ACE mRNA levels.8 ACE, an ectoenzyme anchored in the cell membrane, is released into the circulation upon cleavage from its anchor. Both increased synthesis and accelerated release into the circulation would lead to elevated plasma ACE activity. Our finding that, besides plasma ACE activity, cardiac ACE activity is also increased in subjects with the DD genotype would favor increased synthesis as an explanation for the increased plasma ACE levels.
ACE activity in subjects with the II genotype was not different from that in subjects with the ID genotype. This contrasts with earlier findings in plasma, in which ACE activity was lowest in subjects with the II genotype.8 It resembles, however, the findings of Costerousse et al9 in human T lymphocytes. The absence of a gene dosage effect in cardiac tissue may be due to unknown genetic or environmental effects. Furthermore, the number of subjects in our study may have been too small to detect a statistical difference between II and ID subjects.
Elevated ACE levels in cardiac tissue may, through increased conversion of angiotensin I to angiotensin II,11 12 lead to higher cardiac angiotensin II levels.13 Since angiotensin II affects cardiac function as well as cardiovascular growth and remodeling, our findings may help to explain the associations between the ACE deletion polymorphism and cardiac disease.1 2 3 4 5
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Acknowledgments |
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This work was supported in part by a grant from the Netherlands Heart Foundation (NHS 93.004), the Deutsche Forschungsgemeinschaft (Schu 672/3), and the Bundesministerium für Forschung und Technologie (KBF 01GB9403). We wish to acknowledge the excellent technical support by Susanne Kürzinger, as well as advice for statistical analysis by Dr M. Gliese.
Received April 26, 1995; revision received June 13, 1995; accepted July 5, 1995.
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R. Maestri, A. F. Milia, M. B. Salis, G. Graiani, C. Lagrasta, M. Monica, D. Corradi, C. Emanueli, and P. Madeddu Cardiac Hypertrophy and Microvascular Deficit in Kinin B2 Receptor Knockout Mice Hypertension, May 1, 2003; 41(5): 1151 - 1155. [Abstract] [Full Text] [PDF]
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 X. Li, Y. Du, Y. Du, and X. Huang Correlation of Angiotensin-Converting Enzyme Gene Polymorphism with Effect of Antihypertensive Therapy by Angiotensin-Converting Enzyme Inhibitor Journal of Cardiovascular Pharmacology and Therapeutics, March 1, 2003; 8(1): 25 - 30. [Abstract] [PDF]
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W. T Abraham, M. V Raynolds, D. B Badesch, K. M Wynne, B. M Groves, R. L Roden, A. D Robertson, B. D Lowes, L. S Zisman, N. F Voelkel, et al. Angiotensin-converting enzyme DD genotype in patients with primary pulmonary hypertension: increased frequency and association with preserved haemodynamics Journal of Renin-Angiotensin-Aldosterone System, March 1, 2003; 4(1): 27 - 30. [Abstract] [PDF]
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M. T. Sciarrone, P. Stella, C. Barlassina, P. Manunta, C. Lanzani, G. Bianchi, and D. Cusi ACE and {alpha}-Adducin Polymorphism as Markers of Individual Response to Diuretic Therapy Hypertension, March 1, 2003; 41(3): 398 - 403. [Abstract] [Full Text] [PDF]
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A. C. Pereira, G. F.A. Mota, R. S. Cunha, F. L. Herbenhoff, J. G. Mill, and J. E. Krieger Angiotensinogen 235T Allele "Dosage" Is Associated With Blood Pressure Phenotypes Hypertension, January 1, 2003; 41(1): 25 - 30. [Abstract] [Full Text] [PDF]
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D. R. Woods, A. J. Pollard, D. J. Collier, Y. Jamshidi, V. Vassiliou, E. Hawe, S. E. Humphries, and H. E. Montgomery Insertion/Deletion Polymorphism of the Angiotensin I-Converting Enzyme Gene and Arterial Oxygen Saturation at High Altitude Am. J. Respir. Crit. Care Med., August 1, 2002; 166(3): 362 - 366. [Abstract] [Full Text] [PDF]
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H. Montgomery, S. Humphries, and S. Danilov Is genotype or phenotype the better tool for investigating the role of ACE in human cardiovascular disease? Eur. Heart J., July 2, 2002; 23(14): 1083 - 1086. [Full Text] [PDF]
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 H. Volzke, J. Engel, V. Kleine, C. Schwahn, J. B. Dahm, L. Eckel, and R. Rettig Angiotensin I-Converting Enzyme Insertion/Deletion Polymorphism and Cardiac Mortality and Morbidity After Coronary Artery Bypass Graft Surgery* Chest, July 1, 2002; 122(1): 31 - 36. [Abstract] [Full Text] [PDF]
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 B.-M. Taute, C. Glaser, R. Taute, and H. Podhaisky Progression of Atherosclerosis in Patients with Peripheral Arterial Disease as a Function of Angiotensin-Converting Enzyme Gene Insertion/Deletion Polymorphism Angiology, July 1, 2002; 53(4): 375 - 382. [Abstract] [PDF]
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H. Tokuyama, K. Hayashi, H. Matsuda, E. Kubota, M. Honda, K. Okubo, I. Takamatsu, S. Tatematsu, Y. Ozawa, S. Wakino, et al. Differential Regulation of Elevated Renal Angiotensin II in Chronic Renal Ischemia Hypertension, July 1, 2002; 40(1): 34 - 40. [Abstract] [Full Text] [PDF]
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 A. Goette, U. Lendeckel, and H. U Klein Signal transduction systems and atrial fibrillation Cardiovasc Res, May 1, 2002; 54(2): 247 - 258. [Abstract] [Full Text] [PDF]
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D. Harding, P. B. Baines, D. Brull, V. Vassiliou, I. Ellis, A. Hart, A. P. J. Thomson, S. E. Humphries, and H. E. Montgomery Severity of Meningococcal Disease in Children and the Angiotensin-Converting Enzyme Insertion/Deletion Polymorphism Am. J. Respir. Crit. Care Med., April 15, 2002; 165(8): 1103 - 1106. [Abstract] [Full Text] [PDF]
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 F. G. H. van der Kleij, P. E. de Jong, R. H. Henning, D. de Zeeuw, and G. Navis Enhanced Responses of Blood Pressure, Renal Function, and Aldosterone to Angiotensin I in the DD Genotype Are Blunted by Low Sodium Intake J. Am. Soc. Nephrol., April 1, 2002; 13(4): 1025 - 1033. [Abstract] [Full Text]
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N. Lapointe and J.-L. Rouleau Activation of vascular tissue angiotensin-converting enzyme (ACE) in heart failure: Effects of ACE inhibitors J. Am. Coll. Cardiol., March 6, 2002; 39(5): 776 - 779. [Full Text] [PDF]
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 D. P. Kelly Peroxisome Proliferator-Activated Receptor {alpha} as a Genetic Determinant of Cardiac Hypertrophic Growth: Culprit or Innocent Bystander? Circulation, March 5, 2002; 105(9): 1025 - 1027. [Full Text] [PDF]
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 N J Mayer, A Forsyth, S Kantachuvesiri, J J Mullins, and S Fleming Association of the D allele of the angiotensin I converting enzyme polymorphism with malignant vascular injury Mol. Pathol., February 1, 2002; 55(1): 29 - 33. [Abstract] [Full Text] [PDF]
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F. Mehraban and J. E. Tomlinson Application of industrial scale genomics to discovery of therapeutic targets in heart failure Eur J Heart Fail, December 1, 2001; 3(6): 641 - 650. [Abstract] [Full Text] [PDF]
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M. Cicoira, L. Zanolla, A. Rossi, G. Golia, L. Franceschini, G. Cabrini, A. Bonizzato, M. Graziani, S. D. Anker, A. J. S. Coats, et al. Failure of aldosterone suppression despite angiotensin-converting enzyme (ACE) inhibitor administration in chronic heart failure is associated with ACE DD genotype J. Am. Coll. Cardiol., June 1, 2001; 37(7): 1808 - 1812. [Abstract] [Full Text] [PDF]
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J. Mathew, K. Basheeruddin, and S. Prabhakar Differences in Frequency of the Deletion Polymorphism of the Angiotensin-Converting Enzyme Gene in Different Ethnic Groups Angiology, June 1, 2001; 52(6): 375 - 379. [Abstract] [PDF]
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D. Woods, G. Onambele, R. Woledge, D. Skelton, S. Bruce, S. E. Humphries, and H. Montgomery Angiotensin-I Converting Enzyme Genotype-Dependent Benefit from Hormone Replacement Therapy in Isometric Muscle Strength and Bone Mineral Density J. Clin. Endocrinol. Metab., May 1, 2001; 86(5): 2200 - 2204. [Abstract] [Full Text]
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D.R. Woods, D. Brull, and H. Montgomery Increased QT dispersion with the D-allele of the ACE polymorphism Eur. Heart J., April 2, 2001; 22(8): 618 - 621. [PDF]
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E. Abro, C. D Griffiths, T. O Morgan, and L. M. Delbridge Regression of cardiac hypertrophy in the SHR by combined renin-angiotensin system blockade and dietary sodium restriction Journal of Renin-Angiotensin-Aldosterone System, March 1, 2001; 2(1_suppl): S148 - S153. [Abstract] [PDF]
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S. G. Myerson, H. E. Montgomery, M. Whittingham, M. Jubb, M. J. World, S. E. Humphries, and D. J. Pennell Left Ventricular Hypertrophy With Exercise and ACE Gene Insertion/Deletion Polymorphism : A Randomized Controlled Trial With Losartan Circulation, January 16, 2001; 103(2): 226 - 230. [Abstract] [Full Text] [PDF]
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A. Prasad, S. Narayanan, M. A. Waclawiw, N. Epstein, and A. A. Quyyumi The insertion/deletion polymorphism of the angiotensin-converting enzyme gene determines coronary vascular tone and nitric oxide activity J. Am. Coll. Cardiol., November 1, 2000; 36(5): 1579 - 1586. [Abstract] [Full Text] [PDF]
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N. E. S. Sibinga and J. A. Ware A Pair of ACEs, for Openers? Circ. Res., September 29, 2000; 87(7): 523 - 525. [Full Text] [PDF]
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G. K. Davis, R. W.J. Millner, and D. H. Roberts Angiotensin converting enzyme (ACE) gene expression in the human left ventricle: effect of ACE gene insertion/deletion polymorphism and left ventricular function Eur J Heart Fail, September 1, 2000; 2(3): 253 - 256. [Abstract] [Full Text] [PDF]
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 D. Crisan and J. Carr Angiotensin I-Converting Enzyme: Genotype and Disease Associations J. Mol. Diagn., August 1, 2000; 2(3): 105 - 115. [Full Text]
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A. Prasad, S. Narayanan, S. Husain, F. Padder, M. Waclawiw, N. Epstein, and A. A. Quyyumi Insertion-Deletion Polymorphism of the ACE Gene Modulates Reversibility of Endothelial Dysfunction With ACE Inhibition Circulation, July 4, 2000; 102(1): 35 - 41. [Abstract] [Full Text] [PDF]
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P. P. van Geel, Y. M. Pinto, A. A. Voors, H. Buikema, M. Oosterga, H. J. G. M. Crijns, and W. H. van Gilst Angiotensin II Type 1 Receptor A1166C Gene Polymorphism Is Associated With an Increased Response to Angiotensin II in Human Arteries Hypertension, March 1, 2000; 35(3): 717 - 721. [Abstract] [Full Text] [PDF]
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 B. Schieffer ACE Gene Polymorphism and Coronary Artery Disease : A Question of Persuasion or Statistical Confusion? Arterioscler Thromb Vasc Biol, February 1, 2000; 20(2): 281 - 282. [Full Text] [PDF]
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A. J. Marian, F. Safavi, L. Ferlic, J. K. Dunn, A. M. Gotto, and C. M. Ballantyne Interactions between angiotensin-I converting enzyme insertion/deletion polymorphism and response of plasma lipids and coronary atherosclerosis to treatment with fluvastatin: The lipoprotein and coronary atherosclerosis study J. Am. Coll. Cardiol., January 1, 2000; 35(1): 89 - 95. [Abstract] [Full Text] [PDF]
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A.H.J. Danser, J. J Saris, M. P Schuijt, and J. P van Kats Is there a local renin--angiotensin system in the heart? Cardiovasc Res, November 1, 1999; 44(2): 252 - 265. [Abstract] [Full Text] [PDF]
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S. Myerson, H. Hemingway, R. Budget, J. Martin, S. Humphries, and H. Montgomery Human angiotensin I-converting enzyme gene and endurance performance J Appl Physiol, October 1, 1999; 87(4): 1313 - 1316. [Abstract] [Full Text] [PDF]
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B. T. Heijmans, R. G. J. Westendorp, D. L. Knook, C. Kluft, and P. E. Slagboom Angiotensin I-converting enzyme and plasminogen activator inhibitor-1 gene variants: risk of mortality and fatal cardiovascular disease in an elderly population-based cohort J. Am. Coll. Cardiol., October 1, 1999; 34(4): 1176 - 1183. [Abstract] [Full Text] [PDF]
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K. F. Hilgers, M. R. W. Langenfeld, M. Schlaich, R. Veelken, and R. E. Schmieder 1166 A/C Polymorphism of the Angiotensin II Type 1 Receptor Gene and the Response to Short-Term Infusion of Angiotensin II Circulation, September 28, 1999; 100(13): 1394 - 1399. [Abstract] [Full Text] [PDF]
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D. Henrion, J. Benessiano, I. Philip, S. Vuillaumier-Barrot, M. Iglarz, G. Plantefeve, D. Chatel, U. Hvass, G. Durand, J.-M. Desmonts, et al. The deletion genotype of the angiotensin I-converting enzyme is associated with an increased vascular reactivity in vivo and in vitro J. Am. Coll. Cardiol., September 1, 1999; 34(3): 830 - 836. [Abstract] [Full Text] [PDF]
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R. R. Taylor, C. D. S. Mamotte, K. Fallon, and F. M. van Bockxmeer Elite athletes and the gene for angiotensin-converting enzyme J Appl Physiol, September 1, 1999; 87(3): 1035 - 1037. [Abstract] [Full Text] [PDF]
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J. Hung, B. M. McQuillan, M. Nidorf, P. L. Thompson, and J. P. Beilby Angiotensin-Converting Enzyme Gene Polymorphism and Carotid Wall Thickening in a Community Population Arterioscler Thromb Vasc Biol, August 1, 1999; 19(8): 1969 - 1974. [Abstract] [Full Text] [PDF]
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A. Prasad, S. Husain, and A. A. Quyyumi Abnormal flow-mediated epicardial vasomotion in human coronary arteries is improved by angiotensin-converting enzyme inhibition: A potential role of bradykinin J. Am. Coll. Cardiol., March 1, 1999; 33(3): 796 - 804. [Abstract] [Full Text] [PDF]
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S. Ueda, P. A. Meredith, J. J. Morton, J. M. C. Connell, and H. L. Elliott ACE (I/D) Genotype as a Predictor of the Magnitude and Duration of the Response to an ACE Inhibitor Drug (Enalaprilat) in Humans Circulation, November 17, 1998; 98(20): 2148 - 2153. [Abstract] [Full Text] [PDF]
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A. P. R. M. Osterop, M. J. M. Kofflard, L. A. Sandkuijl, F. J. t. Cate, R. Krams, M. A. D. H. Schalekamp, and A. H. J. Danser AT1 Receptor A/C1166 Polymorphism Contributes to Cardiac Hypertrophy in Subjects With Hypertrophic Cardiomyopathy Hypertension, November 1, 1998; 32(5): 825 - 830. [Abstract] [Full Text] [PDF]
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 E. Villard, A. Alonso, M. Agrapart, M. Challah, and F. Soubrier Induction of Angiotensin I-converting Enzyme Transcription by a Protein Kinase C-dependent Mechanism in Human Endothelial Cells J. Biol. Chem., September 25, 1998; 273(39): 25191 - 25197. [Abstract] [Full Text] [PDF]
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M. Challah, E. Villard, M. Philippe, A. Ribadeau-Dumas, B. Giraudeau, P. Janiak, J.-P. Vilaine, F. Soubrier, and J.-B. Michel Angiotensin I-Converting Enzyme Genotype Influences Arterial Response to Injury in Normotensive Rats Arterioscler Thromb Vasc Biol, February 1, 1998; 18(2): 235 - 243. [Abstract] [Full Text] [PDF]
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D.-K. Kim, J.-W. Kim, S. Kim, H.-C. Gwon, J.-C. Ryu, J.-E. Huh, J.-A Choo, Y. Choi, C.-H. Rhee, and W.-R. Lee Polymorphism of Angiotensin Converting Enzyme Gene Is Associated With Circulating Levels of Plasminogen Activator Inhibitor-1 Arterioscler Thromb Vasc Biol, November 1, 1997; 17(11): 3242 - 3247. [Abstract] [Full Text]
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M. Margaglione, E. Grandone, G. Vecchione, G. Cappucci, N. Giuliani, D. Colaizzo, E. Celentano, S. Panico, and G. Di Minno Plasminogen Activator Inhibitor-1 (PAI-1) Antigen Plasma Levels in Subjects Attending a Metabolic Ward: Relation to Polymorphisms of PAI-1 and Angiontensin Converting Enzyme (ACE) Genes Arterioscler Thromb Vasc Biol, October 1, 1997; 17(10): 2082 - 2087. [Abstract] [Full Text]
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Y. Watanabe, T. Ishigami, Y. Kawano, T. Umahara, A. Nakamori, S. Mizushima, K. Hibi, I. Kobayashi, K. Tamura, H. Ochiai, et al. Angiotensin-Converting Enzyme Gene I/D Polymorphism and Carotid Plaques in Japanese Hypertension, September 1, 1997; 30(3): 569 - 573. [Abstract] [Full Text]
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K. Hibi, T. Ishigami, K. Kimura, M. Nakao, T. Iwamoto, K. Tamura, T. Nemoto, T. Shimizu, Y. Mochida, H. Ochiai, et al. Angiotensin-Converting Enzyme Gene Polymorphism Adds Risk for the Severity of Coronary Atherosclerosis in Smokers Hypertension, September 1, 1997; 30(3): 574 - 579. [Abstract] [Full Text]
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D. N. Muller, J. Bohlender, K. F. Hilgers, D. Dragun, O. Costerousse, J. Menard, and F. C. Luft Vascular Angiotensin-Converting Enzyme Expression Regulates Local Angiotensin II Hypertension, January 1, 1997; 29(1): 98 - 104. [Abstract] [Full Text]
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A. Busjahn, H. Knoblauch, M. Knoblauch, J. Bohlender, M. Menz, H.-D. Faulhaber, A. Becker, H. Schuster, and F. C. Luft Angiotensin-Converting Enzyme and Angiotensinogen Gene Polymorphisms, Plasma Levels, Cardiac Dimensions A Twin Study: A Twin Study Hypertension, January 1, 1997; 29(1): 165 - 170. [Abstract] [Full Text] [PDF]
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K. J. McLaughlin, P. N. Harden, S. Ueda, J. M. Boulton-Jones, J. M.C. Connell, and A. G. Jardine The Role of Genetic Polymorphisms of Angiotensin-Converting Enzyme in the Progression of Renal Diseases Hypertension, November 1, 1996; 28(5): 912 - 915. [Abstract] [Full Text]
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A. Benetos, S. Gautier, S. Ricard, J. Topouchian, R. Asmar, O. Poirier, E. Larosa, L. Guize, M. Safar, F. Soubrier, et al. Influence of Angiotensin-Converting Enzyme and Angiotensin II Type 1 Receptor Gene Polymorphisms on Aortic Stiffness in Normotensive and Hypertensive Patients Circulation, August 15, 1996; 94(4): 698 - 703. [Abstract] [Full Text]
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M. Hosoi, Y. Nishizawa, K. Kogawa, T. Kawagishi, T. Konishi, K. Maekawa, M. Emoto, S. Fukumoto, A. Shioi, T. Shoji, et al. Angiotensin-Converting Enzyme Gene Polymorphism Is Associated With Carotid Arterial Wall Thickness in Non–Insulin-Dependent Diabetic Patients Circulation, August 15, 1996; 94(4): 704 - 707. [Abstract] [Full Text]
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D. R.J. Singer, C. G. Missouris, and S. Jeffery Angiotensin-Converting Enzyme Gene Polymorphism: What to Do About All the Confusion? Circulation, August 1, 1996; 94(3): 236 - 239. [Full Text]
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M. Eyries, A. Michaud, J. Deinum, M. Agrapart, J. Chomilier, C. Kramers, and F. Soubrier Increased Shedding of Angiotensin-converting Enzyme by a Mutation Identified in the Stalk Region J. Biol. Chem., February 16, 2001; 276(8): 5525 - 5532. [Abstract] [Full Text] [PDF]
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