Anti-hypertensive effects of diminazene aceturate: An angiotensin-converting enzyme 2 activator in rats

Protein and Peptide Letters

Volumn 23, Issue 1, 2016, Pages 9-16

  De Maria, Marilda L A ^a   Araújo, Liliane D ^a   Fraga Silva, Rodrigo A ^a   Pereira, Letícia A S ^a   Ribeiro, Heder J ^a   Menezes, Gustavo B ^a   Shenoy, Vinayak ^b   Raizada, Mohan K ^b   Ferreira, Anderson J ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Angiotensin (1 7); Angiotensin converting enzyme 2; Aortic vessels; Intravital microscopy; Mas receptor; Renin angiotensin system; Renovascular hypertension

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN[1-7][7 DEXTRO ALANINE]; CAPTOPRIL; DIMINAZENE ACETURATE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PROTEIN; PROTEIN MAS; UNCLASSIFIED DRUG; 7-ALA-ANGIOTENSIN (1-7); ANGIOTENSIN II; ANTIHYPERTENSIVE AGENT; DIMINAZENE; DIPEPTIDYL CARBOXYPEPTIDASE; G PROTEIN COUPLED RECEPTOR; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO-ONCOGENE PROTEINS C-MAS-1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIHYPERTENSIVE ACTIVITY; ARTICLE; BLOOD PRESSURE MEASUREMENT; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; HEART RATE; HEART VENTRICLE HYPERTROPHY; INTRAVITAL MICROSCOPY; MALE; MESENTERY BLOOD FLOW; NONHUMAN; RAT; RENOVASCULAR HYPERTENSION; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD FLOW VELOCITY; BLOOD PRESSURE; DRUG EFFECTS; HYPERTENSION, RENOVASCULAR; METABOLISM; WISTAR RAT;

ANGIOTENSIN II; ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD FLOW VELOCITY; BLOOD PRESSURE; DIMINAZENE; HEART RATE; HYPERTENSION, RENOVASCULAR; MALE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; PROTO-ONCOGENE PROTEINS; RATS; RATS, WISTAR; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84953725349     PISSN: 09298665     EISSN: 18755305     Source Type: Journal    
DOI: 10.2174/0929866522666151013130550     Document Type: Article

References (42)

1. Dilauro, M.; Burns, K. D. Angiotensin-(1-7) and its effects in the kidney. Sci. World J., 2009, 9, 522-535.
2. Donoghue, M.; Hsieh, F.; Baronas, E.; Godbout, K.; Gosselin, M.; Stagliano, N. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ. Res., 2000, 87, E1-E9.
3. Tipnis, S. R.; Hooper, N. M.; Hyde, R.; Karran, E.; Christie, G.; Turner, A. J. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J. Biol. Chem., 2000, 275, 33238-33243.
4. Santos, R. A.; Ferreira, A. J.; Simões e Silva, A. C. Recent advances in the angiotensin-converting enzyme 2-angiotensin (1-7)-Mas axis. Exp. Physiol., 2008, 93(5), 519-527.
5. Navar, L. G.; Harrison-Bernard, L. M.; Imig, J. D.; Mitchell, K. D. Renal actions of angiotensin II at AT1 receptor blockers. In: Epstein, M.; Brunner, H. R.; eds.; Angiotensin II Receptor Antagonists. Philadelphia, PA: Hanley & Belfus., 2000, Inc. 189-214.
6. Durand, M. J.; Raffai, G.; Weinberg, B. D.; Lombardi, J. H. Angiotensin-(1-7) and lowdose angiotensin II infusion reverse saltinduced endothelial dysfunction via different mechanisms in rat middle cerebral arteries. Am. J. Physiol. Heart Circ. Physiol., 2010, 299, 1024-1033.
7. Fernandes, L.; Fortes, Z. B.; Nigro, D.; Tostes, R. C.; Santos, R. A.; Castelli de Carvalho, M. H. Potentiation of bradykinin by angiotensin-(1-7) on arterioles of spontaneously hypertensive rats studied in vivo. Hypertension, 2001, 37(2 part 2), 703-709.
8. Oliveira, M. A.; Fortes, Z. B.; Santos, R. A.; Kosla, M. C.; De Carvalho, M. H. Synergistic effect of angiotensin-(1-7) on bradykinin arteriolar dilation in vivo. Peptides, 1999, 20, 1195-1201.
9. Trask, A. J.; Ferrario, C. M. Angiotensin-(1-7): pharmacology and new perspective in cardiovascular treatments. Cardiovasc. Drug Rev., 2007, 25, 162-174.
10. Murça, T. M.; Almeida, T. C. S.; Raizada, M. K.; Ferreira, A. J. Chronic activation of endogenous angiotensin-converting enzyme 2 protects diabetic rats form cardiovascular autonomic dysfunction. Exp. Physiolog., 2012, 97(6), 699-709.
11. Crackower, M. A.; Sarao, R.; Oudit, G. Y.; Yagil, C.; Kozieradzki, I.; Scanga, S. E. Angiotensinconverting enzyme 2 is an essential regulator of heart function. Nature, 2002, 417, 822-828.
12. Oudit, G. Y.; Liu, G. C.; Zhong, J.; Basu, R.; Chow, F. L.; Zhou, J. Human recombinant ACE2 reduces the progression of diabetic nephropathy. Diabetes, 2010, 59, 529-538.
13. Hernández Prada, J. A.; Ferreira, A. J.; Katovich, M. J.; Shenoy, V.; Qi, Y.; Santos, R. A.; Castellano, R. K.; Lampkins, A. J.; Gubala, V.; Ostrov, D. A.; Raizada, M. K. Structure-based identification of small-molecule angiotensin-converting enzyme 2 activators as novel antihypertensive agents. Hypertension, 2008, 51, 1312-1317.
14. Ferreira, A. J.; Shenoy, V.; Qi, Y.; Fraga-Silva, R. A.; Santos, R. A.; Katovich, M. J.; Raizada, M. K. Angiotensin-converting enzyme 2 activation protects against hypertension-induced cardiac fibrosis involving extracellular signal-regulated kinases. Exp. Physiol., 2011, 96(3), 287-294.
15. Kulemina, L. V.; Ostrov, D. A. Prediction of off-target effects on angiotensin-converting enzyme 2. J. Biomol. Screen., 2011, 16, 878-885.
16. Hwang, S. J.; Yamasaki, M.; Nakamura, K.; Sasaki, N.; Murakami, M.; Wickramasekara Rajapakshage B. K.; Ohta, H.; Maede, Y.; Takiguchi, M. Development and characterization of a strain of Babesia gibsoni resistant to diminazene aceturate in vitro. J. Vet. Med. Sci., 2010, 72(6), 765-771.
17. Turnipseed, S. B.; Clark, S. B.; Andersen, W. C.; Karbiwnyk, C. M.; Miller, K. E.; Hurlbut, J. A. Confirmation of diminazene diaceturate in bovine plasma using electrospray liquid chromatography-mass spectrometry. J. Chromatogr., 2006, 844, 127-133.
18. Rashid, H. B.; Chaudhry, M.; Rashid, H.; Pervez, K.; Khan, M. A.; Mahmood, A. K. Comparative efficacy of diminazene diaceturate and diminazene aceturate for the treatment of babesiosis in horses. Trop. Anim. Health Prod., 2007, 40, 463-467.
19. Jean-Moreno, R. R.; Goyeneche, D.; Coombs, G. H.; Walker, J. Leishmania donovani: differential activities of classical topoisomerase inhibitors and antileishmanials against parasite and host cells at the level of DNA topoisomerase I and in cytotoxicity assays. Exper. Parasitol., 2006, 112, 21-30.
20. Kroubi, M.; Daulouede, S.; Karembe, H.; Jallouli, Y.; Howsam, M.; Mossalayi, D.; Vincendeau, P.; Betbeder, D. Development of a nanoparticulate formulation of diminazene to treat African trypanosomiasis. Nanotechnology, 2010, 21(50), 505102.
21. Rigatto, K.; Casali, K. R.; Shenoy, V.; Katovich, M. J.; Raizada, M. K. Diminazene aceturate improves autonomic modulation in pulmonary hypertension. Eur. J. Pharmacol., 2013, 713, 89-93.
22. Shenoy, V.; Gjymishka, A.; Jarajapu, Y. P.; Qi, Y.; Afzal, A.; Rigatto, K.; Ferreira, A. J.; Fraga-Silva, R. A.; Kearns, P.; Douglas, J. Y.; Agarwal, D.; Mubarak, K. K.; Bradford, C.; Kennedy, W. R.; Jun, J. Y.; Rathinasabapathy, A.; Bruce, E.; Gupta, D.; Cardounel, A. J.; Mocco, J.; Patel, J. M.; Francis, J.; Grant, M. B.; Katovich, M. J.; Raizada, M. K. Diminazene attenuates pulmonary hypertension and improves angiogenic progenitor cell functions in experimental models. Am. J. Respir. Crit. Care Med., 2013, 187, 648-657.
23. Qi, Y.; Zhang, J.; Cole-Jeffrey, C. T.; Shenoy, V.; Espejo, A.; Hanna, M.; Song, C.; Pepine, C. J.; Katovich, M. J.; Raizada, M. K. Diminazene aceturate enhances angiotensin-converting enzyme 2 activity and attenuates ischemia-induced cardiac pathophysiology. Hypertension, 2013, 62, 746-752.
24. Coutinho, D. C.; Monnerat-Cahli, G.; Ferreira, A. J.; Medei, E. Activation of angiotensin-converting enzyme 2 improves cardiac electrical changes in ventricular repolarization in streptozotocininduced hyperglycaemic rats. Europace, 2014, 16(11), 1689-1696.
25. Foureaux, G.; Nogueira, J. C.; Nogueira, B. S.; Fulgêncio, G. O.; Menezes, G. B.; Fernandes, S. O.; Cardoso, V. N.; Fernandes, R. S.; Oliveira, G. P.; Franca, J. R.; Faraco, A. A.; Raizada, M. K.; Ferreira, A. J. Antiglaucomatous effects of the activation of intrinsic Angiotensinconverting enzyme 2. Invest. Ophthalmol. Vis. Sci., 2013, 54(6), 4296-4306.
26. Qiu, Y.; Shil, P. K.; Zhu, P.; Yang, H.; Verma, A.; Lei, B.; Li, Q. Angiotensin-converting enzyme 2 (ACE2) activator diminazene aceturate ameliorates endotoxin-induced uveitis in mice. Invest. Ophthalmol. Vis. Sci., 2014, 55(6), 3809-3818.
27. Macêdo, S. M.; Antunes, T.; Oliveira Andrade, J. M.; Guimarães, A. L.; Batista de Paula, A. M.; Ferreira, A. J.; Santos, S. H. S. Angiotensin Converting Enzyme 2 Activator DIZE Modulates Metabolic Profile in Mice Decreasing Lipogenesis. Protein Pept Lett., 2015, 22(4), 332-40.
28. Kubes, P.; Heit, B.; van Marle, G.; Johnston, J. B.; Knight, D.; Khan, A.; Power, C. In vivo impairment of neutrophil recruitment during lentivirus infection. J. Immunol., 2003, 171(9), 4801-4808.
29. Xavier, C. H.; Nalivaiko, E.; Beig, M. I.; Menezes, G. B.; Cara, D. C.; Campagnole-Santos, M. J.; Fontes, M. A. Functional asymmetry in the descending cardiovascular pathways from dorsomedial hypothalamic nucleus. Neuroscience, 2009, 164(13), 1360-1368.
30. Goldblatt, H.; Lynch, J.; Hanzal, R. F.; Summerville, W. W. Studies on experimental hypertension: The production of persistent elevation of systolic blood pressure by means of renal ischemia. J. Exp. Med. Sci., 1934;9, 347-378.
31. Valenti, V. E.; Imaizumi, C.; de Abreu, L. C.; Colombari, E.; Sato, M. A.; Ferreira, C. Intra-strain variations of baroreflex sensitivity in young Wistar-Kyoto rats. Clin. Invest. Med., 2009, 32(6), E251.
32. Fraga-Silva, R. A.; Costa-Fraga, F. P.; Murça, T. M.; Moraes, P. L.; Martins Lima, A.; Lautner, R. Q.; Castro, C. H.; Soares, C. M.; Borges, C. L.; Nadu, A. P.; Oliveira, M. L.; Shenoy, V.; Katovich, M. J.; Santos, R. A.; Raizada, M. K.; Ferreira, A. J. Angiotensinconverting enzyme 2 activation improves endothelial function. Hypertension, 2013, 61, 1233-8.
33. Ferreira, A. J.; Shenoy, V.; Yamazato, Y.; Sriramula, S.; Francis, J.; Yuan, L.; Castellano, R. K.; Ostrov, D. A.; Oh, S. P.; Katovich, M. J.; Raizada, M. K. Evidence for angiotensin-converting enzyme 2 as a therapeutic target for the prevention of pulmonary hypertension. Am. J. Respir. Crit. Care Med., 2009, 179, 1048-54.
34. Mecca, A. P.; Regenhardt, R. W.; O'Connor, T. E.; Joseph, J. P.; Raizada, M. K.; Katovich, M. J.; Sumners, C. Cerebroprotection by angiotensin-(1-7) in endothelin-1-induced ischaemic stroke. Exp. Physiol., 2011, 96, 1084-96.
35. Ferreira, A. J.; Santos, R. A. S. Cardiovascular actions of angiotensin-(1-7). Braz. J. Med. Biol. Res., 2005, 38(4), 499-507.
36. Keidar, S.; Kaplan, M.; Gamliel-Lazarovich, A. ACE2 of the heart: form angiotensin I to angiotensin-(1-7). Cardiovasc. Res., 2007;73, 463-469.
37. Almeida, A. P.; Frábregas, B. C.; Madureira, M. M.; Santos, R. J.; Campagnole-Santos, M. J.; Santos, R. A. S. Angiotensin-(1-7) potentiates the coronary vasodilatatory effect of bradykinin in the isolated rat heart. Braz. J. Med. Biol. Res., 2000, 33(6), 709-713.
38. Savergnini, S. Q.; Beiman, M.; Lautner, R. Q. Vascular relaxation, antihypertensive effects, and cardioprotection of a novel peptide agonist of the Mas receptor. Hypertension, 2010, 56, 112-120.
39. Gomes, E. R. M.; Lara, A. A.; Almeida, P. W. M.; Guimarães, D.; Resende, R. R.; Campagnole-Santos, M. J.; Bader, M.; Santos, R. A. S.; Guatimosin, S. Angiotensin-(1-7) prevents cardiomyocyte pathological remodeling through a nitric oxide/guanosine 3', 5'-Cyclic Monophosphate-Dependent Pathaway. Hypertension, 2010, 55, 153-160.
40. Gwathmey, T. Y. M.; Pendergrass, K. D.; Reid, S. D.; Rose, J. C.; Diz, D. I.; Chappell, M. C. Angiotensin-(1-7)-Angiotensin-Converting Enzime 2 attenuates reactive oxygen species formation to angiotensin II within the cell nucleus. Hypertension, 2010, 55, 166-171.
41. Haber, P. K.; Ye, M.; Wysocki, J.; Maier, C.; Haque, S. K.; Batlle, D. Angiotensin-converting enzyme 2-independent action of presumed angiotensin-converting enzyme 2 activators: studies in vivo, ex vivo, and in vitro. Hypertension, 2014, 63(4), 774-782.
42. Fraga-Silva, R.; Sorg, B. S.; Wankhede, M.; Deugd, C.; Jun, J. Y.; Baker, M. B.; Li, Y.; Castellano, R. K.; Katovich, M. J.; Raizada, M. K.; Ferreira, A. J. ACE2 activation promotes antithrombotic activity. Mol. Med., 2010, 16(5-6), 210-215.