Effect of bradykinin metabolism inhibitors on evoked hypotension in rats: rank efficacy of enzymes associated with bradykinin-mediated angioedema
Open accessAbstract
Background and purpose: Inhibition of bradykinin metabolizing enzymes (BMEs) can cause acute angioedema, as demonstrated in a recent clinical trial in patients administered the antihypertensive, omapatrilat. However, the relative contribution of specific BMEs to this effect is unclear and confounded by the lack of a predictive pre‐clinical model of angioedema. Experimental approach: Rats were instrumented to record blood pressure and heart rate; inhibitors were infused for 35 min and bradykinin was infused during the last 5 min to elicit hypotension, as a functional marker of circulating bradykinin and relative angioedema risk. Key results: In the presence of omapatrilat bradykinin produced dose‐dependent hypotension, an effect abolished by B 2 blockade. In the presence of lisinopril (ACE inhibitor), but not candoxatril (NEP inhibitor) or apstatin (APP inhibitor), bradykinin also elicited hypotension. Lisinopril‐mediated hypotension was unchanged with concomitant blockade of NEP or NEP/DPPIV (candoxatril+A‐899301). However, hypotension was enhanced upon concomitant blockade of APP and further intensified in the presence of NEP inhibition to values not different from omapatrilat alone. Conclusions and implications: We demonstrated that bradykinin is degraded in vivo with an enzyme rank‐efficacy of ACE>APP≫NEP or DPPIV. These results suggest the effects of omapatrilat are mediated by inhibition of three BMEs, ACE/APP/NEP. However, dual inhibition of ACE/NEP or ACE/NEP/DPPIV elicits no increased risk of angioedema compared to ACE inhibition alone. Thus, novel BME inhibitors must display no activity against APP to avoid angioedema risk due to high prevalence of ACE inhibitor therapy in patients with diabetes and cardiovascular disease. British Journal of Pharmacology (2008) 153 , 947–955; doi: 10.1038/sj.bjp.0707641 ; published online 17 December 2007
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
APP inactivates both bradykinin and des-Arg9-bradykinin, a role of major importance when ACE is inhibited.
“Thus, APP inactivates bradykinin and des-Arg 9 -bradykinin [Turner and Cottrell, 2004], a role that is of major importance in the presence of ACEi [Cyr et al., 2001;Fryer et al., 2008;Kim et al., 2000].”
From A functional XPNPEP2 promoter haplotype leads to reduced plasma aminopeptidase P and increased risk of ACE inhibitor‐induced angioedema (2011) · cites this paper as Fryer et al., 2008
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Yung-Chi, C., & Prusoff, W. H. (1973) · Biochemical Pharmacology · doi:10.1016/0006-2952(73)90196-2 · Cited by 12,922 · see citing works
Fundamentals of Enzyme Kinetics
Cornish-Bowden, A. J. (1979) · Elsevier eBooks · doi:10.1016/c2013-0-04130-8 · Cited by 2,079 · see citing works
Lambeir, A.-M., Durinx, C., Scharpé, S., & De Meester, I. (2003) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/713609354 · Cited by 955 · see citing works
Plasma bradykinin in angio-oedema
Nussberger, J., Cugno, M., Amstutz, C., Cicardi, M., Pellacani, A., & Agostoni, A. (1998) · The Lancet · doi:10.1016/s0140-6736(97)09137-x · Cited by 706 · see citing works
Fundamentals of enzyme kinetics
(1996) · Choice Reviews Online · doi:10.5860/choice.33-4507 · Cited by 658 · see citing works
Kostis, J. (2004) · American Journal of Hypertension · doi:10.1016/j.amjhyper.2003.09.014 · Cited by 579 · see citing works
The Kallikrein-Kinin System: Current and Future Pharmacological Targets
Moreau, M. E., Garbacki, N., Molinaro, G., Brown, N. J., Marceau, F., & Adam, A. (2005) · Journal of Pharmacological Sciences · doi:10.1254/jphs.srj05001x · Cited by 457 · see citing works
Han, E. D., MacFarlane, R. C., Mulligan, A. N., Scafidi, J., & Davis, A. E. (2002) · Journal of Clinical Investigation · doi:10.1172/jci14211 · Cited by 363 · see citing works
Han, E. D., MacFarlane, R. C., Mulligan, A. N., et al. (2002) · Journal of Clinical Investigation · doi:10.1172/jci200214211 · Cited by 299 · see citing works
Bradykinin-Mediated Angioedema
Nussberger, J., Cugno, M., & Cicardi, M. (2002) · New England Journal of Medicine · doi:10.1056/nejm200208223470820 · Cited by 232 · see citing works
Bradykinin and the pathophysiology of angioedema
Cugno, M., Nussberger, J., Cicardi, M., & Agostoni, A. (2003) · International Immunopharmacology · doi:10.1016/s1567-5769(02)00162-5 · Cited by 215 · see citing works
Angioedema Associated With Angiotensin-Converting Enzyme Inhibitor Use
Cicardi, M., Zingale, L. C., Bergamaschini, L. C., & Agostoni, A. (2004) · Archives of Internal Medicine · doi:10.1001/archinte.164.8.910 · Cited by 210 · see citing works
Basic carboxypeptidases: regulators of peptide hormone activity
Skidgel, R. A. (1988) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(88)90015-6 · Cited by 209 · see citing works
Walters, P. E., Gaspari, T. A., & Widdop, R. E. (2005) · Hypertension · doi:10.1161/01.hyp.0000160325.59323.b8 · Cited by 206 · see citing works
Bork, K., Frank, J., Grundt, B., Schlattmann, P., Nussberger, J., & Kreuz, W. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.02.012 · Cited by 203 · see citing works
EFFECTS OF UK 69 578: A NOVEL ATRIOPEPTIDASE INHIBITOR
Northridge, D. B., Alabaster, C. T., Connell, J. C., Dilly, S., Lever, A., Jardine, A. G., Barclay, P., Dargie, H., Findlay, I. N., & Samuels, G. M. R. (1989) · The Lancet · doi:10.1016/s0140-6736(89)90714-9 · Cited by 193 · see citing works
Aminopeptidase P in individuals with a history of angio-oedema on ACE inhibitors
Adam, A., Cugno, M., Molinaro, G., Perez, M., Lepage, Y., & Agostoni, A. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08914-6 · Cited by 181 · see citing works
Grundt, B., Bork, K., Frank, J., Schlattmann, P., Nussberger, J., Rosenkranz, B., Dong, L., Knolle, J., & Kreuz, W. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2006.12.459 · Cited by 169 · see citing works
Drug-Induced Angioedema without Urticaria: Incidence, Prevention and Management
Agostoni, A., & Cicardi, M. (2001) · Drug Safety · doi:10.2165/00002018-200124080-00004 · Cited by 154 · cited 4× · see citing works
“, 2004) and immune-related angioedema mediated by histamine (Agostoni and Cicardi, 2001; Nussberger et al., 2002).”
BackgroundInfluentialAngioedema due to angiotensin-converting enzyme inhibitors
Agostoni, A., Cicardi, M., Cugno, M., Zingale, L. C., Gioffré, D., & Nussberger, J. (1999) · Immunopharmacology · doi:10.1016/s0162-3109(99)00107-1 · Cited by 147 · see citing works
Molinaro, G., Cugno, M., Perez, M., Lepage, Y., Gervais, N., Agostoni, A., & Adam, A. (2002) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.038067 · Cited by 137 · see citing works
Duan, Q. L., Nikpoor, B., Dubé, M.-P., Molinaro, G., Meijer, I. A., Dion, P., Rochefort, D., Saint-Onge, J., Flury, L., Brown, N. J., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/496899 · Cited by 126 · cited 1× · see citing works
“…primary mechanism responsible for the large depressor response in rats (and subsequent angioedema in patients); a finding consistent with increased susceptibility to angioedema in patients with low APP activity on ACE inhibitor therapy (Adam et al., 2002; Duan et al., 2005; Nikpoor et al., 2005).”
BackgroundDipeptidyl peptidase IV activity in patients with ACE-inhibitor-associated angioedema
Lefebvre, J., Murphey, L. J., Hartert, T. V., Jiao Shan, R., Simmons, W. H., & Brown, N. J. (2002) · Hypertension · doi:10.1161/hy0202.103054 · Cited by 113 · see citing works
McClean, D. R., Ikram, H., Garlick, A. H., Richards, M., Nicholls, M. G., & Crozier, I. (2000) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(00)00741-5 · Cited by 110 · see citing works
Décarie, A., Raymond, P., Gervais, N., Couture, R., & Adam, A. A. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.4.h1340 · Cited by 107 · see citing works
Some Old and Some New Ideas on Kinin Metabolism
Erdös, E. G. (1990) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199000156-00005 · Cited by 97 · see citing works
Some Old and Some New Ideas on Kinin Metabolism
Erdös, E. G. (1990) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199015061-00005 · Cited by 92 · see citing works
Blais, C., Rouleau, J.-L., Brown, N. J., Lepage, Y., Spence, D., Munoz, C., Friborg, J., Geadah, D., Gervais, N., & Adam, A. (1999) · Immunopharmacology · doi:10.1016/s0162-3109(99)00133-2 · Cited by 78 · see citing works
Effect of angiotensin-converting enzyme inhibition on circulating and local kinin levels
Johnston, C. I., Clappison, B. H., Anderson, W. P., & Yasujima, M. (1982) · The American Journal of Cardiology · doi:10.1016/0002-9149(82)90350-2 · Cited by 78 · see citing works
Alves, M. F. M., Araújo, M. D. C., Juliano, M. A., de Oliveira, E. M., Krieger, J. E., Casarini, D. E., Juliano, L., & Carmona, A. K. (2005) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2005000600007 · Cited by 71 · see citing works
Angiotensin-converting enzyme inhibitor-related angioedema: how to deal with it
Beltrami, L., Zingale, L. C., Carugo, S., & Cicardi, M. (2006) · Expert Opinion on Drug Safety · doi:10.1517/14740338.5.5.643 · Cited by 66 · see citing works
Johnson, G. D., & Ahn, K. (2000) · Analytical Biochemistry · doi:10.1006/abio.2000.4772 · Cited by 61 · see citing works
The Plasma and Tissue Kininogen-kallikrein-kinin System: Role in the Cardiovascular System
Marcondes, S., & Antunes, E. (2005) · Current Medicinal Chemistry - Cardiovascular & Hematological Agents · doi:10.2174/1568016052773351 · Cited by 58 · see citing works
The role of enzymatic processing in the biological actions of substance P
Hall, M. E., Miley, F. B., & Stewart, J. M. (1989) · Peptides · doi:10.1016/0196-9781(89)90132-0 · Cited by 54 · see citing works
Byrd, J. B., Shreevatsa, A., Putlur, P., Foretia, D., McAlexander, L., Sinha, T., Does, M. D., & Brown, N. J. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.04.012 · Cited by 52 · see citing works
Role of angiotensin converting enzyme and other peptidases in in vivo metabolism of kinins.
Ishida, H., Scicli, A. G., & Carretero, O. A. (1989) · Hypertension · doi:10.1161/01.hyp.14.3.322 · Cited by 51 · see citing works
Tripeptidyl carboxypeptidase activity of kininase II (angiotensin-converting enzyme)
Inokuchi, J., & Nagamatsu, A. (1981) · Biochimica et Biophysica Acta (BBA) - Enzymology · doi:10.1016/0005-2744(81)90042-5 · Cited by 50 · see citing works
Baş, M., Bier, H., Greve, J., Kojda, G., & Hoffmann, T. K. (2006) · Allergy · doi:10.1111/j.1398-9995.2006.01197.x · Cited by 45 · see citing works
Contributions of various rat plasma peptidases to kinin hydrolysis.
Ishida, H., Scicli, A. G., & Carretero, O. A. (1989) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)21083-7 · Cited by 42 · see citing works
Backes, B. J., Longenecker, K. L., Hamilton, G. L., Stewart, K. D., Lai, C., Kopecka, H., von Geldern, T. W., Madar, D. J., Pei, Z., Lubben, T. H., et al. (2007) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2007.01.026 · Cited by 39 · see citing works
Self-citationSubstance P in the baroreceptor reflex: 25 years
Helke, C. J., & Seagard, J. L. (2004) · Peptides · doi:10.1016/j.peptides.2004.02.016 · Cited by 39 · see citing works
Ahn, K., Herman, S. B., & Fahnoe, D. C. (1998) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1998.0913 · Cited by 38 · see citing works
MOLINARO, G., Carmona, A. K., Juliano, M. A., Juliano, L., Malitskaya, E., Yessine, M., Chagnon, M., LEPAGE, Y., Simmons, W. H., Boileau, G., et al. (2005) · Biochemical Journal · doi:10.1042/bj20040849 · Cited by 35 · see citing works
Effects of aminopeptidase P inhibition on kinin-mediated vasodepressor responses
Kitamura, S.-I., Carbini, L. A., Simmons, W. H., & Scicli, A. G. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.276.5.h1664 · Cited by 34 · see citing works
Nikpoor, B., Duan, Q., & Rouleau, G. A. (2005) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.6.11.1851 · Cited by 29 · see citing works
Bäcklund, T., Palojoki, E., Grönholm, T., Eriksson, A., Vuolteenaho, O. J., Laine, M., & Tikkanen, I. T. (2001) · Pharmacological Research · doi:10.1006/phrs.2001.0875 · Cited by 27 · see citing works
Dual ACE/NEP inhibitors – more than playing the ACE card
Jandeleit-Dahm, K. A. M. (2006) · Journal of Human Hypertension · doi:10.1038/sj.jhh.1002018 · Cited by 26 · see citing works
Kym, P. R., Souers, A. J., Campbell, T. J., Lynch, J. K., Judd, A. S., Iyengar, R., Vasudevan, A., Gao, J., Freeman, J. C., Wódka, D., et al. (2006) · Journal of Medicinal Chemistry · doi:10.1021/jm0512286 · Cited by 26 · see citing works
Self-citationAtrial Natriuretic Peptide and the Baroreflex Control of Circulation
Volpe, M. (1992) · American Journal of Hypertension · doi:10.1093/ajh/5.7.488 · Cited by 26 · see citing works
Sulpizio, A. C., Pullen, M. A., Edwards, R. M., Louttit, J. B., West, R., & Brooks, D. P. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.084749 · Cited by 24 · see citing works
Cleavage of des-Arg9-bradykinin by angiotensin I-converting enzyme from pig kidney cortex
Oshima, G., Hiraga, Y., Shirono, K., Oh‐ishi, S., Sakakibara, S., & Kinoshita, T. (1985) · Cellular and Molecular Life Sciences · doi:10.1007/bf02004493 · Cited by 22 · see citing works
ACE Inhibitors and Angiotensin Receptor Antagonists and the Incidence of New-Onset Diabetes Mellitus
Aguilar, D. A., & Solomon, S. D. (2006) · Drugs · doi:10.2165/00003495-200666090-00001 · Cited by 22 · see citing works
Omapatrilat. Bristol-Myers Squibb.
Tabrizchi, R. (2001) · PubMed · Cited by 21 · see citing works
Caligiorne, S. M., Santos, R. A. S., & Campagnole‐Santos, M. J. (1996) · Brain Research · doi:10.1016/0006-8993(95)01498-5 · Cited by 21 · see citing works
Barclay, P. L., Bennett, J. A., Samuels, G. M. R., & Shepperson, N. B. (1991) · Biochemical Pharmacology · doi:10.1016/0006-2952(91)90091-i · Cited by 19 · see citing works
Kubota, E., Dean, R. G., Hubner, R. A., CASLEY, D. J., Johnston, C. I., & Burrell, L. M. (2003) · Clinical Science · doi:10.1042/cs20030097 · Cited by 19 · see citing works
Johnson, A. G., Pearce, G. L., & Danoff, T. M. (2006) · Journal of Human Hypertension · doi:10.1038/sj.jhh.1002009 · Cited by 12 · see citing works
Lasher, R. S., Lutz, E. M., Mulholland, F., Sanderson, R., Stewart, J. M., & Bublitz, C. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90117-r · Cited by 11 · see citing works
[Bradykinin inhibits carotid sinus baroreflex in anesthetized rats].
Wu, Y.-M., & Rr, H. (1999) · PubMed · Cited by 5 · see citing works
Gardiner, S. M., March, J. E., Kemp, P. A., Ballard, S. A., & Bennett, T. M. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.106781 · Cited by 4 · see citing works
Johnston, W. D., Tobis, J. M., Nalcioğlu, O., Seibert, J. A., Roeck, W. W., Iseri, L. T., Elkayam, U., & Henry, W. L. (1982) · The American Journal of Cardiology · doi:10.1016/0002-9149(82)92149-x · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Angiotensin-neprilysin inhibition versus enalapril in heart failure
McMurray, J. J. V., Packer, M., Desai, A. S., Gong, J., Lefkowitz, M. P., Rizkala, A. R., Rouleau, J. L., Shi, V. C., Solomon, S. D., Swedberg, K., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1409077 · Cited by 6,957 · see citing works
Solomon, S. D., Zile, M. R., Pieske, B. M., Voors, A. A., Shah, A. M., Kraigher‐Krainer, E., Shi, V. C., Bransford, T. L., Takeuchi, M., Gong, J., et al. (2012) · The Lancet · doi:10.1016/s0140-6736(12)61227-6 · Cited by 1,171 · see citing works
Ruilope, L. M., Dukát, A., Böhm, M., Lacourcière, Y., Gong, J., & Lefkowitz, M. P. (2010) · The Lancet · doi:10.1016/s0140-6736(09)61966-8 · Cited by 598 · see citing works
Gu, J., Noè, A., Chandra, P., Al‐Fayoumi, S., Ligueros‐Saylan, M., Sarangapani, R., Maahs, S., Ksander, G. M., Rigel, D. F., Jeng, A. Y., et al. (2009) · The Journal of Clinical Pharmacology · doi:10.1177/0091270009343932 · Cited by 505 · see citing works
McMurray, J. J. V., Packer, M., Desai, A. S., Gong, J., Lefkowitz, M. P., Rizkala, A. R., Rouleau, J. L., Shi, V. C., Solomon, S. D., Swedberg, K. B., et al. (2013) · European Journal of Heart Failure · doi:10.1093/eurjhf/hft052 · Cited by 458 · see citing works
Coulson, L. B., Danser, A. H. J., Poglitsch, M., Touyz, R. M., Burnett, J. C. J., Llorens‐Cortés, C., Ehlers, M. R., & Sturrock, E. D. (2019) · Pharmacological Reviews · doi:10.1124/pr.118.017129 · Cited by 341 · see citing works
Mangiafico, S., Costello‐Boerrigter, L. C., Andersen, I. A., Cataliotti, A., & Burnett, J. C. J. (2012) · European Heart Journal · doi:10.1093/eurheartj/ehs262 · Cited by 275 · see citing works
Kario, K., Sun, N., Chiang, F., Supasyndh, O., Baek, S. H., Inubushi-Molessa, A., Zhang, Y., Gotou, H., Lefkowitz, M. P., & Zhang, J. Y. (2014) · Hypertension · doi:10.1161/hypertensionaha.113.02002 · Cited by 232 · see citing works
On the origin of serum CD26 and its altered concentration in cancer patients
Cordero, O. J., Salgado, F. J., & Nogueira, M. (2009) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-009-0728-1 · Cited by 199 · see citing works
Inhibiting the breakdown of endogenous opioids and cannabinoids to alleviate pain
Roques, B. P., Fournié‐Zaluski, M., & Wurm, M. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3673 · Cited by 193 · see citing works
McMurray, J. J. V., Packer, M., Desai, A. S., Gong, J., Lefkowitz, M. P., Rizkala, A. R., Rouleau, J. L., Shi, V. C., Solomon, S. D., Swedberg, K. B., et al. (2014) · European Journal of Heart Failure · doi:10.1002/ejhf.115 · Cited by 178 · see citing works
Suematsu, Y., Miura, S., Goto, M., Matsuo, Y., Arimura, T., Kuwano, T., Imaizumi, S., Iwata, A., Yahiro, E., & Saku, K. (2016) · European Journal of Heart Failure · doi:10.1002/ejhf.474 · Cited by 154 · see citing works
New drugs, procedures, and devices for hypertension
Laurent, S., Schlaich, M. P., & Esler, M. (2012) · The Lancet · doi:10.1016/s0140-6736(12)60825-3 · Cited by 151 · see citing works
Cilia La Corte, A. L., Carter, A. M., Rice, G. I., Duan, Q. L., Rouleau, G. A., Adam, A., Grant, P. J., & Hooper, N. M. (2011) · Human Mutation · doi:10.1002/humu.21579 · Cited by 154 · see citing works
Long-term neprilysin inhibition — implications for ARNIs
Campbell, D. J. (2016) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2016.200 · Cited by 147 · see citing works
Natriuretic peptides and cardio-renal disease
Volpe, M. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.08.032 · Cited by 137 · see citing works
Hoover, T. A., Lippmann, M. L., Grouzmann, E., Marceau, F., & Herscu, P. (2009) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2009.03323.x · Cited by 127 · see citing works
Neprilysin Inhibition to Treat Heart Failure: A Tale of Science, Serendipity, and Second Chances
McMurray, J. J. V. (2015) · European Journal of Heart Failure · doi:10.1002/ejhf.250 · Cited by 124 · see citing works
Jordan, J., Stinkens, R., Jax, T. W., Engeli, S., Blaak, E. E., May, M., Havekes, B., Schindler, C., Albrecht, D., Pal, P., et al. (2016) · Clinical Pharmacology & Therapeutics · doi:10.1002/cpt.455 · Cited by 123 · see citing works
Endothelial Targeting of Antibody-Decorated Polymeric Filomicelles
Shuvaev, V. V., Ilies, M. A., Simone, E. A., Zaitsev, S. V., Kim, Y., Cai, S., Mahmud, A., Dziubla, T. D., Muro, S., Discher, D. E., et al. (2011) · ACS Nano · doi:10.1021/nn2015453 · Cited by 116 · see citing works
Bavishi, C., Messerli, F. H., KADOSH, B. S., Ruilope, L. M., & Kario, K. (2015) · European Heart Journal · doi:10.1093/eurheartj/ehv142 · Cited by 108 · see citing works
Targeting the renin–angiotensin–aldosterone system in heart failure
Lang, C. C., & Struthers, A. D. (2013) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2012.196 · Cited by 94 · see citing works
Langenickel, T., & Dole, W. P. (2012) · Drug Discovery Today Therapeutic Strategies · doi:10.1016/j.ddstr.2013.11.002 · Cited by 83 · see citing works
Next generation multifunctional angiotensin receptor blockers
Kurtz, T. W., & Klein, U. (2009) · Hypertension Research · doi:10.1038/hr.2009.135 · Cited by 79 · see citing works
Kusaka, H., Sueta, D., Koibuchi, N., Hasegawa, Y., Nakagawa, T., Lin, B., Ogawa, H., & Kim‐Mitsuyama, S. (2015) · American Journal of Hypertension · doi:10.1093/ajh/hpv015 · Cited by 73 · see citing works
Neprilysin Inhibitors and Bradykinin
Campbell, D. J. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00257 · Cited by 72 · see citing works
Cheung, D. G., Aizenberg, D., Gorbunov, V. M., Hafeez, K., Chen, C., & Zhang, J. Y. (2018) · Journal of Clinical Hypertension · doi:10.1111/jch.13153 · Cited by 71 · see citing works
Solomon, S. D., Claggett, B. L., McMurray, J. J. V., Hernandez, A. F., & Fonarow, G. C. (2016) · European Journal of Heart Failure · doi:10.1002/ejhf.603 · Cited by 70 · see citing works
Hegde, L. G., Yu, C., Renner, T., Thibodeaux, H., Armstrong, S. R., Park, T., Cheruvu, M., Olsufka, R., Sandvik, E., Lane, C. E., et al. (2011) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0b013e318210fc7e · Cited by 63 · see citing works
Angioedema: Etiology, Pathophysiology, Current and Emerging Therapies
Lewis, L. M. (2013) · Journal of Emergency Medicine · doi:10.1016/j.jemermed.2013.03.045 · Cited by 62 · see citing works
Packer, M., & McMurray, J. J. V. (2016) · The Lancet · doi:10.1016/s0140-6736(16)30969-2 · Cited by 51 · see citing works
Targeted modulation of reactive oxygen species in the vascular endothelium
Shuvaev, V. V., & Muzykantov, V. R. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2011.03.022 · Cited by 50 · see citing works
Dalzell, J. R., Seed, A., Berry, C., Whelan, C. J., Petrie, M. C., Padmanabhan, N., Clarke, A., Biggerstaff, F., Hillier, C., & McMurray, J. J. V. (2013) · Cardiovascular Therapeutics · doi:10.1111/1755-5922.12053 · Cited by 49 · see citing works
Current pharmacotherapy of bradykinin-mediated angioedema
Farkas, H. (2013) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.2013.778826 · Cited by 45 · see citing works
Renin Angiotensin Blockers and Cardiac Protection: From Basics to Clinical Trials
Levy, B. I., & Mourad, J. (2021) · American Journal of Hypertension · doi:10.1093/ajh/hpab108 · Cited by 43 · see citing works
Bradykinin Metabolism and Drug-Induced Angioedema
Smolińska, S., Antolín‐Amérigo, D., & Popescu, F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411649 · Cited by 41 · see citing works
Angiotensin Receptor Neprilysin Inhibition in Heart Failure: Mechanistic Action and Clinical Impact
Buggey, J., Mentz, R. J., DeVore, A. D., & Velazquez, E. J. (2015) · Journal of Cardiac Failure · doi:10.1016/j.cardfail.2015.07.008 · Cited by 40 · see citing works
Potential of soluble CD26 as a serum marker for colorectal cancer detection
Cordero, O. J. (2011) · World Journal of Clinical Oncology · doi:10.5306/wjco.v2.i6.245 · Cited by 40 · see citing works
Shi, V. C., Senni, M., Streefkerk, H. J., Modgill, V., Zhou, W., & Kaplan, A. P. (2018) · International Journal of Cardiology · doi:10.1016/j.ijcard.2018.03.121 · Cited by 40 · see citing works
Neprilysin Inhibition in Heart Failure with Reduced Ejection Fraction: A Clinical Review
King, J. B., Bress, A. P., Reese, A. D., & Munger, M. A. (2015) · Pharmacotherapy The Journal of Human Pharmacology and Drug Therapy · doi:10.1002/phar.1629 · Cited by 39 · see citing works
Sacubitril/Valsartan: A Review in Chronic Heart Failure with Reduced Ejection Fraction
McCormack, P. L. (2016) · Drugs · doi:10.1007/s40265-016-0544-9 · Cited by 36 · see citing works
Zhang, H., Huang, T., Shen, W., Xu, X., Yang, P., Zhu, D., Fang, H., Wan, H., Wu, T., Wu, Y., et al. (2020) · ESC Heart Failure · doi:10.1002/ehf2.12974 · Cited by 36 · see citing works
The potential role of valsartan + AHU377 (LCZ696) in the treatment of heart failure
Voors, A. A., Dorhout, B., & van der Meer, P. (2013) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2013.797963 · Cited by 32 · see citing works
Sacubitril/Valsartan in Asian Patients with Heart Failure with Reduced Ejection Fraction
Dewan, P., Docherty, K. F., & McMurray, J. J. V. (2019) · Korean Circulation Journal · doi:10.4070/kcj.2019.0136 · Cited by 33 · see citing works
Marceau, F., Rivard, G., Gauthier, J., Binkley, K. E., Bonnefoy, A., Boccon‐Gibod, I., Bouillet, L., Picard, M., Lévesque, G., Elfassy, H. L., et al. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.00358 · Cited by 30 · see citing works
Yandrapalli, S., Aronow, W. S., Mondal, P., & Chabbott, D. R. (2017) · Archives of Medical Science · doi:10.5114/aoms.2017.68813 · Cited by 30 · see citing works
Cozier, G. E., Arendse, L. B., Schwager, S. L. U., Sturrock, E. D., & Acharya, K. R. (2018) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.8b01309 · Cited by 30 · see citing works
Neutral Endopeptidase (Neprilysin) in Therapy and Diagnostics: Yin and Yang
Feygina, E. E., Katrukha, A., & Semenov, A. G. (2019) · Biochemistry (Moscow) · doi:10.1134/s0006297919110105 · Cited by 27 · see citing works
Marceau, F., Bawolak, M., Fortin, J., Morissette, G., Roy, C. S., Bachelard, H., Gera, L., & Charest‐Morin, X. (2018) · Peptides · doi:10.1016/j.peptides.2018.05.007 · Cited by 26 · see citing works
Sharma, U., Cozier, G. E., Sturrock, E. D., & Acharya, K. R. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.0c00441 · Cited by 26 · see citing works
DPP-4 inhibitors and angioedema: a cause for concern?
Byrd, J. S., Minor, D. S., Elsayed, R., & Marshall, G. D. (2011) · Annals of Allergy Asthma & Immunology · doi:10.1016/j.anai.2011.02.012 · Cited by 26 · see citing works
Dual neurohormonal intervention in CV disease: angiotensin receptor and Neprilysin inhibition
Segura, J., Salazar, J. B., & Ruilope, L. M. (2013) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2013.797962 · Cited by 25 · see citing works
Alves-Lopes, R., Montezano, A. C. I., Neves, K. B., Harvey, A., Rios, F. J. O., Skiba, D. S., Arendse, L. B., Guzik, T. J., Graham, D., Poglitsch, M., et al. (2021) · Hypertension · doi:10.1161/hypertensionaha.121.17041 · Cited by 24 · see citing works
The bradykinin-degrading aminopeptidase P is increased in women taking the oral contraceptive pill
La Corte, A. L. C., Carter, A. M., Turner, A. J., Grant, P. J., & Hooper, N. M. (2008) · Journal of the Renin-Angiotensin-Aldosterone System · doi:10.1177/1470320308096405 · Cited by 21 · see citing works
Sacubitril/valsartan (LCZ696) for the treatment of heart failure
Gori, M., & Senni, M. (2015) · Expert Review of Cardiovascular Therapy · doi:10.1586/14779072.2016.1128827 · Cited by 19 · see citing works
Update on bradykinin-mediated angioedema in 2020
Lepelley, M., Bernardeau, C., Defendi, F., Crochet, J., Mallaret, M., & Bouillet, L. (2020) · Therapies · doi:10.1016/j.therap.2020.02.011 · Cited by 19 · see citing works
Sible, A. M., Nawarskas, J. J., Alajajian, D., & Anderson, J. R. (2015) · Cardiology in Review · doi:10.1097/crd.0000000000000093 · Cited by 19 · see citing works
Research progress and perspectives of dual-target inhibitors
Pang, X., Xu, W., Liang, J. Y., Liu, Y., Li, H., & Chen, L. (2025) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2025.117453 · Cited by 18 · see citing works
Macdonald, P. S. (2015) · Clinical Therapeutics · doi:10.1016/j.clinthera.2015.08.013 · Cited by 18 · see citing works
Spotlight on valsartan–sacubitril fixed-dose combination for heart failure: the evidence to date
Vilela-Martin, J. F. (2016) · Drug Design Development and Therapy · doi:10.2147/dddt.s84782 · Cited by 20 · see citing works
Modulation of RAAS-natriuretic peptides in the treatment of HF: Old guys and newcomers
Mollace, V., Gliozzi, M., Capuano, A., & Rossi, F. (2016) · International Journal of Cardiology · doi:10.1016/j.ijcard.2016.03.085 · Cited by 18 · see citing works
Lillyblad, M. P. (2015) · Annals of Pharmacotherapy · doi:10.1177/1060028015593093 · Cited by 17 · see citing works
Dual-Acting Angiotensin Receptor–Neprilysin Inhibition
Segura, J., & Ruilope, L. M. (2010) · Current Hypertension Reports · doi:10.1007/s11906-010-0166-7 · Cited by 17 · see citing works
Modulation of the Renin-Angiotensin-Aldosterone System in Heart Failure
Casella, G., Struthers, A. D., & Lang, C. C. (2014) · Current Atherosclerosis Reports · doi:10.1007/s11883-014-0403-7 · Cited by 17 · see citing works
Angioedema: a rare and sometimes delayed side effect of angiotensin-converting enzyme inhibitors
Davin, L., Maréchal, P., Lancellotti, P., Martinez, C., Piérard, L., & Radermecker, R. P. (2018) · Acta cardiologica. Supplementum · doi:10.1080/00015385.2018.1507477 · Cited by 17 · see citing works
New drug therapies for hypertension
Azizi, M., Tuttle, K. R., Brown, J. M., Piskorz, D. L., Kario, K., & Williams, B. (2026) · The Lancet · doi:10.1016/s0140-6736(25)02064-1 · Cited by 17 · see citing works
Rationale and Therapeutic Opportunities for Natriuretic Peptide System Augmentation in Heart Failure
McKie, P. M., & Burnett, J. C. J. (2014) · Current Heart Failure Reports · doi:10.1007/s11897-014-0235-3 · Cited by 15 · see citing works
Charest‐Morin, X., Hébert, J., Rivard, G., Bonnefoy, A., Wagner, É., & Marceau, F. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02183 · Cited by 15 · see citing works
Marceau, F., Bachelard, H., Rivard, G., & Hébert, J. (2019) · BMC Research Notes · doi:10.1186/s13104-019-4335-8 · Cited by 14 · see citing works
Using a bradykinin blocker in ACE inhibitor-associated angioedema in the emergency department
Volans, A. P., & FERGUSON, R. L. (2013) · BMJ Case Reports · doi:10.1136/bcr-2012-008295 · Cited by 14 · see citing works
Pai, P., Vijeev, A., Phadke, S., Shetty, M. G., & Babitha, K. S. (2024) · Inflammopharmacology · doi:10.1007/s10787-024-01486-z · Cited by 13 · see citing works
Potential beneficial effects of sacubitril-valsartan in renal disease: a new field for a new drug
Gervasini, G., & Robles, N. R. (2017) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2017.1317345 · Cited by 13 · see citing works
McKinnell, R. M., Fatheree, P. R., Choi, S. K., Gendron, R. A. L., Jendza, K. C., Blair, B. O., Budman, J., Hill, C. M., Hegde, L. G., Yu, C., et al. (2018) · ACS Medicinal Chemistry Letters · doi:10.1021/acsmedchemlett.8b00462 · Cited by 13 · see citing works
Role of Angiotensin Receptor-Neprilysin Inhibition in Heart Failure
Prenner, S. B., Shah, S. J., & Yancy, C. W. (2016) · Current Atherosclerosis Reports · doi:10.1007/s11883-016-0603-4 · Cited by 12 · see citing works
Docherty, K. F., & McMurray, J. J. V. (2018) · International Journal of Cardiology · doi:10.1016/j.ijcard.2018.05.124 · Cited by 12 · see citing works
Angioedema Spotlight: A Closer Examination of Sacubitril/Valsartan Safety Results
Owens, R. E., & Oliphant, C. S. (2017) · The Journal of the American Board of Family Medicine · doi:10.3122/jabfm.2017.04.170111 · Cited by 12 · see citing works
Estrela, G. R., Wasinski, F., Gregnani, M. F., Freitas‐Lima, L. C., Arruda, A. C., Morais, R. L., Malheiros, D. M., Câmara, N. O. S., Pesquero, J. B., Bäder, M., et al. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.00096 · Cited by 12 · see citing works
Volterrani, M., Iellamo, F., Senni, M., & Piepoli, M. F. (2016) · International Journal of Cardiology · doi:10.1016/j.ijcard.2016.04.180 · Cited by 12 · see citing works
Focus on the Novel Cardiovascular Drug LZC696: from Evidence to Clinical Consideration
Lin, L., Wu, Y., Wu, M., & Lin, J. (2016) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-016-6699-5 · Cited by 12 · see citing works
New antihypertensive medications and clinical implications
Wong, D., Tsai, P. N. W., Ip, K. Y., & Irwin, M. G. (2018) · Best practice & research. Clinical anaesthesiology · doi:10.1016/j.bpa.2018.06.013 · Cited by 11 · see citing works
Drugs of the Kallikrein–Kinin System: An Overview
Marceau, F. (2023) · Drugs and Drug Candidates · doi:10.3390/ddc2030028 · Cited by 10 · see citing works
Marceau, F., Rivard, G., Hébert, J., Gauthier, J., Bachelard, H., Gangnus, T., & Burckhardt, B. B. (2022) · Frontiers in Allergy · doi:10.3389/falgy.2022.837463 · Cited by 9 · see citing works
Gera, L., Charest‐Morin, X., Jean, M., Bachelard, H., & Marceau, F. (2016) · BMC Research Notes · doi:10.1186/s13104-016-2258-1 · Cited by 8 · see citing works
Angiotensin Receptor–Neprilysin Inhibition
Havakuk, O., & Elkayam, U. (2016) · Journal of Cardiovascular Pharmacology and Therapeutics · doi:10.1177/1074248416683049 · Cited by 8 · see citing works
Bachelard, H., Charest‐Morin, X., & Marceau, F. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00273 · Cited by 8 · see citing works
Ye, L., Wang, J., Chen, Q., & Yang, X. (2017) · Oncotarget · doi:10.18632/oncotarget.22442 · Cited by 8 · see citing works
Nowak, W., Errasti, A. E., Armesto, A. R., Velazque, N. L. S., & Rothlin, R. P. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.05.045 · Cited by 8 · see citing works
Charest‐Morin, X., Bachelard, H., Jean, M., & Marceau, F. (2017) · PeerJ · doi:10.7717/peerj.2911 · Cited by 7 · see citing works
Vasopeptidase-activated latent ligands of the histamine receptor-1
Gera, L., Roy, C. S., Charest‐Morin, X., & Marceau, F. (2013) · International Immunopharmacology · doi:10.1016/j.intimp.2013.08.014 · Cited by 7 · see citing works
In Vitro Modeling of Bradykinin-Mediated Angioedema States
Marceau, F., Bachelard, H., Charest‐Morin, X., Hébert, J., & Rivard, G. (2020) · Pharmaceuticals · doi:10.3390/ph13090201 · Cited by 7 · see citing works
Kjeldsen, S. E., Hedner, T., Narkiewicz, K., & Oparil, S. (2012) · Blood Pressure · doi:10.3109/10582452.2012.741765 · Cited by 7 · see citing works
Manzur, F., Villarreal, T., & Moneriz, C. (2013) · Revista Colombiana de Cardiología · doi:10.1016/s0120-5633(13)70090-1 · Cited by 6 · see citing works
Yu, W., Zhang, H., Shen, W., Luo, F., Yang, S., Gan, L., Zhao, Y., Yang, P., & Wu, Q. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.897423 · Cited by 6 · see citing works
Kaplinsky, E. (2016) · PubMed Central · doi:10.11909/j.issn.1671-5411.2016.11.006 · Cited by 6 · see citing works
Marceau, F., & Bachelard, H. (2021) · Pharmaceuticals · doi:10.3390/ph14030177 · Cited by 6 · see citing works
Sacubitril/Valsartan: From Clinical Trials to Real-world Experience
Joly, J. M., & Desai, A. S. (2018) · Current Treatment Options in Cardiovascular Medicine · doi:10.1007/s11936-018-0638-7 · Cited by 5 · see citing works
Hypertension in Patients with Heart Failure with Reduced Ejection Fraction
Volpe, M., Santolamazza, C., & Tocci, G. (2016) · Current Cardiology Reports · doi:10.1007/s11886-016-0807-9 · Cited by 5 · see citing works
Hayman, S. M., & Atherton, J. J. (2016) · Cardiac failure review · doi:10.15420/cfr.2016:2:2 · Cited by 5 · see citing works
5 Drugs in the kallikrein-kinin system
Marceau, F. (2011) · De Gruyter eBooks · doi:10.1515/9783110252354.69 · Cited by 4 · see citing works
Renin Angiotensin Aldosterone System Blockers
Shibata, S., & Fujita, T. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-88369-6.00022-0 · Cited by 5 · see citing works
- Authors
- Fryer, R. M., Segreti, J., Banfor, P. N., Widomski, D. L., Backes, B. J., Lin, C. W., Ballaron, S. J., Cox, B. F., Trevillyan, J. M., Reinhart, G. A., & von Geldern, T. W.
- Affiliations
- Abbott (United States) (US)
- Corresponding author
- Fryer, R M
- Venue
- British Journal of Pharmacology
- Publisher
- Wiley
- Published
- 2008-03
- Volume
- 153
- Issue
- 5
- Pages
- 947-955
- ISSN
- 0007-1188 (ISSN-L)
- 1476-5381
- PMC
- PMC2267285
- OpenAlex
- W1560143001
- Cited by
- 130
- References
- 59
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 5 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 7 · 2019: 5 · 2018: 12 · 2017: 7 · 2016: 18 · 2015: 14 · 2014: 6 · 2013: 14 · 2012: 8
- FWCI
- 1.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- British Journal of Pharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Genetics › Coagulation, Bradykinin, Polyphosphates, and Angioedema
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Renin-Angiotensin System Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Eicosanoids and Hypertension Pharmacology
- Keywords
- angioedema, omapatrilat, lisinopril, ACE inhibitors, aprotinin, neprilysin, dipeptidyl peptidase IV, bradykinin degradation, drug safety
- MeSH terms
- Aminopeptidases, Angioedema, Angiotensin-Converting Enzyme Inhibitors, Animals, Bradykinin, Dose-Response Relationship, Drug, Drug Evaluation, Preclinical, Enzyme Inhibitors, Hypotension, Indans, Male, Peptides, Propionates, Pyridines, Thiazepines, Neprilysin, Rats, Sprague-Dawley, Lisinopril, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review