Activation of angiotensin-converting enzyme 2 (ACE2) attenuates allergic airway inflammation in rat asthma model

Toxicology and Applied Pharmacology

Volumn 306, Issue , 2016, Pages 17-26

  Dhawale, Vaibhav Shrirang ^a   Amara, Venkateswara Rao ^a   Karpe, Pinakin Arun ^a   Malek, Vajir ^a   Patel, Deep ^a   Tikoo, Kulbhushan ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

Author keywords

Airway response; Angiotensin converting enzyme 2 (ACE2); Asthma; Diminazene aceturate; Fibrosis; Renin angiotensin system (RAS)

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; CARBACHOL; DIMINAZENE ACETURATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 4; OVALBUMIN; PROTEIN BCL 2; PROTEIN KINASE B; SYNAPTOPHYSIN; ANTIASTHMATIC AGENT; BCL2 PROTEIN, RAT; DIMINAZENE; DIPEPTIDYL CARBOXYPEPTIDASE; GLUTATHIONE; I KAPPA B; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTHMA; BLOOD SAMPLING; BONE MARROW; CONTROLLED STUDY; DRUG MEGADOSE; EOSINOPHILIA; HEART; HEART RIGHT VENTRICLE HYPERTROPHY; HISTOPATHOLOGY; LEUKOCYTE COUNT; LOW DRUG DOSE; LUNG; MALE; NEUTROPHILIA; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; SENSITIZATION; TRACHEA; TREATMENT DURATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; BRONCHOALVEOLAR LAVAGE FLUID; CARDIAC MUSCLE; CHEMISTRY; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; WISTAR RAT;

ANIMALS; ANTI-ASTHMATIC AGENTS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; DIMINAZENE; DISEASE MODELS, ANIMAL; GLUTATHIONE; I-KAPPA B PROTEINS; INTERLEUKIN-1BETA; INTERLEUKIN-4; LEUKOCYTE COUNT; LUNG; MALE; MALONDIALDEHYDE; MYOCARDIUM; NF-KAPPA B; NITRIC OXIDE; OVALBUMIN; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDYL-DIPEPTIDASE A; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS, WISTAR;

EID: 84978033718     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2016.06.026     Document Type: Article

References (46)

1. Abdel-Fattah, M.M., Salama, A.A., Shehata, B.A., Ismaiel, I.E., The potential effect of the angiotensin II receptor blocker telmisartan in regulating OVA-induced airway remodeling in experimental rats. Pharmacol. Rep. 67 (2015), 943–951.
2. Belvisi, M.G., Bundschuh, D.S., Stoeck, M., Wicks, S., Underwood, S., Battram, C.H., Haddad, E.-B., Webber, S.E., Foster, M.L., Preclinical profile of ciclesonide, a novel corticosteroid for the treatment of asthma. J. Pharmacol. Exp. Ther. 314 (2005), 568–574.
3. Benetti, L.R., Campos, D., Gurgueira, S.A., Vercesi, A.E., Guedes, C.E., Santos, K.L., Wallace, J.L., Teixeira, S.A., Florenzano, J., Costa, S.K., Muscara, M.N., Ferreira, H.H., Hydrogen sulfide inhibits oxidative stress in lungs from allergic mice in vivo. Eur. J. Pharmacol. 698 (2013), 463–469.
4. Bitar, M.S., Wahid, S., Mustafa, S., Al-Saleh, E., Dhaunsi, G.S., Al-Mulla, F., Nitric oxide dynamics and endothelial dysfunction in type II model of genetic diabetes. Eur. J. Pharmacol. 511 (2005), 53–64.
5. Blume, C., Davies, D.E., In vitro and ex vivo models of human asthma. Eur. J. Pharm. Biopharm. 84 (2013), 394–400.
6. Bousquet, J., JEFFERY, P.K., Busse, W.W., Johnson, M., Vignola, A.M., Asthma: from bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. 161 (2000), 1720–1745.
7. Bramley, A.M., Roberts, C.R., Schellenberg, R.R., Collagenase increases shortening of human bronchial smooth muscle in vitro. Am. J. Respir. Crit. Care Med. 152 (1995), 1513–1517.
8. Bundschuh, D.S., Eltze, M., Barsig, J., Wollin, L., Hatzelmann, A., Beume, R., In vivo efficacy in airway disease models of roflumilast, a novel orally active PDE4 inhibitor. J. Pharmacol. Exp. Ther. 297 (2001), 280–290.
9. Chen, K.-H., Weng, M.-S., Lin, J.-K., Tangeretin suppresses IL-1β-induced cyclooxygenase (COX)-2 expression through inhibition of p38 MAPK, JNK, and AKT activation in human lung carcinoma cells. Biochem. Pharmacol. 73 (2007), 215–227.
10. Cho, Y.S., Lee, J., Lee, T.H., Lee, E.Y., Lee, K.U., Park, J.Y., Moon, H.B., alpha-Lipoic acid inhibits airway inflammation and hyperresponsiveness in a mouse model of asthma. J. Allergy Clin. Immunol. 114 (2004), 429–435.
11. Deng, Y., Guan, M., Xie, X., Yang, X., Xiang, H., Li, H., Zou, L., Wei, J., Wang, D., Deng, X., Geniposide inhibits airway inflammation and hyperresponsiveness in a mouse model of asthma. Int. Immunopharmacol. 17 (2013), 561–567.
12. DiGiovanni, F.A., Ellis, R., Wattie, J., Hirota, J.A., Southam, D.S., Inman, M.D., Concurrent dual allergen exposure and its effects on airway hyperresponsiveness, inflammation and remodeling in mice. Dis. Model. Mech. 2 (2009), 275–282.
13. Durrani, S.R., Viswanathan, R.K., Busse, W.W., What effect does asthma treatment have on airway remodeling? Current perspectives. J. Allergy Clin. Immunol. 128 (2011), 439–448.
14. El-Hashim, A.Z., Renno, W.M., Raghupathy, R., Abduo, H.T., Akhtar, S., Benter, I.F., Angiotensin-(1–7) inhibits allergic inflammation, via the MAS1 receptor, through suppression of ERK1/2-and NF-κB-dependent pathways. Br. J. Pharmacol. 166 (2012), 1964–1976.
15. Ezeamuzie, C.I., El-Hashim, A., Renno, W., Edafiogho, I.O., Anti-Allergic and anti-asthmatic effects of a novel enhydrazinone ester (CEE-1): inhibition of activation of both mast cells and eosinophils. J. Pharmacol. Exp. Ther., 2014, jpet.114.213751.
16. Ferreira, A.J., Santos, R.A., Bradford, C.N., Mecca, A.P., Sumners, C., Katovich, M.J., Raizada, M.K., Therapeutic implications of the vasoprotective axis of the renin-angiotensin system in cardiovascular diseases. Hypertension 55 (2010), 207–213.
17. Hussain, S., Laumbach, R., Coleman, J., Youssef, H., Kelly-McNeil, K., Ohman-Strickland, P., Zhang, J., Kipen, H., Controlled exposure to diesel exhaust causes increased nitrite in exhaled breath condensate among subjects with asthma. J. Occup. Environ. Med. 54 (2012), 1186–1191.
18. Jarajapu, Y.P., Bhatwadekar, A.D., Caballero, S., Hazra, S., Shenoy, V., Medina, R., Kent, D., Stitt, A.W., Thut, C., Finney, E.M., Activation of the ACE2/angiotensin-(1–7)/Mas receptor axis enhances the reparative function of dysfunctional diabetic endothelial progenitors. Diabetes 62 (2013), 1258–1269.
19. Kandhare, A.D., Bodhankar, S.L., Singh, V., Mohan, V., Thakurdesai, P.A., Anti-asthmatic effects of type-A procyanidine polyphenols from cinnamon bark in ovalbumin-induced airway hyperresponsiveness in laboratory animals. Biomed. Aging Pathol. 3 (2013), 23–30.
20. Kaparianos, A., Argyropoulou, E., Local renin-angiotensin II systems, angiotensin-converting enzyme and its homologue ACE2: their potential role in the pathogenesis of chronic obstructive pulmonary diseases, pulmonary hypertension and acute respiratory distress syndrome. Curr. Med. Chem. 18 (2011), 3506–3515.
21. Karpe, P.A., Gupta, J., Marthong, R.F., Ramarao, P., Tikoo, K., Insulin resistance induces a segmental difference in thoracic and abdominal aorta: differential expression of AT1 and AT2 receptors. J. Hypertens. 30 (2012), 132–146.
22. Keller, A.C., Rodriguez, D., Russo, M., Nitric oxide paradox in asthma. Mem. Inst. Oswaldo Cruz 100:Suppl. 1 (2005), 19–23.
23. Kuba, K., Imai, Y., Penninger, J.M., Angiotensin-converting enzyme 2 in lung diseases. Curr. Opin. Pharmacol. 6 (2006), 271–276.
24. Kulemina, L.V., Ostrov, D.A., Prediction of off-target effects on angiotensin-converting enzyme 2. J. Biomol. Screen. 16 (2011), 878–885.
25. Li, N., Nel, A.E., Role of the Nrf2-mediated signaling pathway as a negative regulator of inflammation: implications for the impact of particulate pollutants on asthma. Antioxid. Redox Signal. 8 (2006), 88–98.
26. Li, X., Molina-Molina, M., Abdul-Hafez, A., Uhal, V., Xaubet, A., Uhal, B.D., Angiotensin converting enzyme-2 is protective but downregulated in human and experimental lung fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 295 (2008), L178–L185.
27. Li, X., Chen, Q., Chu, C., You, H., Jin, M., Zhao, X., Zhu, X., Zhou, W., Ji, W., Ovalbumin-induced experimental allergic asthma is Toll-like receptor 2 dependent. Allergy Asthma Proc. 35 (2014), e15–e20.
28. Milanese, M., Crimi, E., Scordamaglia, A., Riccio, A., Pellegrino, R., Canonica, G.W., Brusasco, V., On the functional consequences of bronchial basement membrane thickening. J. Appl. Physiol. 91 (2001), 1035–1040 (Bethesda, Md.: 1985).
29. Nagai, H., Recent research and developmental strategy of anti-asthma drugs. Pharmacol. Ther. 133 (2012), 70–78.
30. Nials, A.T., Uddin, S., Mouse models of allergic asthma: acute and chronic allergen challenge. Dis. Model. Mech. 1 (2008), 213–220.
31. Nicklas, R.A., National and international guidelines for the diagnosis and treatment of asthma. Curr. Opin. Pulm. Med. 3 (1997), 51–55.
32. Palmans, E., Kips, J.C., Pauwels, R.A., Prolonged allergen exposure induces structural airway changes in sensitized rats. Am. J. Respir. Crit. Care Med. 161 (2000), 627–635.
33. Patel, K., Animal models of asthma. J. Pharm. Res. Opin., 1, 2014.
34. Rey-Parra, G.J., Vadivel, A., Coltan, L., Hall, A., Eaton, F., Schuster, M., Loibner, H., Penninger, J.M., Kassiri, Z., Oudit, G.Y., Thebaud, B., Angiotensin converting enzyme 2 abrogates bleomycin-induced lung injury. J. Mol. Med. 90 (2012), 637–647 (Berl.).
35. Rodrigues-Machado, M.G., Magalhaes, G.S., Cardoso, J.A., Kangussu, L.M., Murari, A., Caliari, M.V., Oliveira, M.L., Cara, D.C., Noviello, M.L., Marques, F.D., Pereira, J.M., Lautner, R.Q., Santos, R.A., Campagnole-Santos, M.J., AVE 0991, a non-peptide mimic of angiotensin-(1-7) effects, attenuates pulmonary remodelling in a model of chronic asthma. Br. J. Pharmacol. 170 (2013), 835–846.
36. Said, S.I., Hamidi, S.A., Gonzalez Bosc, L., Asthma and pulmonary arterial hypertension: do they share a key mechanism of pathogenesis?. Eur. Respir. J. 35 (2010), 730–734.
37. Santos, R.A., Ferreira, A.J., Pharmacological effects of AVE 0991, a nonpeptide angiotensin-(1–7) receptor agonist. Cardiovasc. Drug Rev. 24 (2006), 239–246.
38. 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., Diminazene attenuates pulmonary hypertension and improves angiogenic progenitor cell functions in experimental models. Am. J. Respir. Crit. Care Med. 187 (2013), 648–657.
39. Silkoff, P.E., Sylvester, J.T., Zamel, N., Permutt, S., Airway nitric oxide diffusion in asthma: role in pulmonary function and bronchial responsiveness. Am. J. Respir. Crit. Care Med. 161 (2000), 1218–1228.
40. Stevenson, C.S., Birrell, M.A., Moving towards a new generation of animal models for asthma and COPD with improved clinical relevance. Pharmacol. Ther. 130 (2011), 93–105.
41. Tikoo, K., Sane, M.S., Gupta, C., Tannic acid ameliorates doxorubicin-induced cardiotoxicity and potentiates its anti-cancer activity: potential role of tannins in cancer chemotherapy. Toxicol. Appl. Pharmacol. 251 (2011), 191–200.
42. 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. 275 (2000), 33238–33243.
43. Wang, T., Yin, K.S., Liu, K.Y., Lu, G.J., Li, Y.H., Chen, J.D., Effect of valsartan on the expression of angiotensin II receptors in the lung of chronic antigen exposure rats. Chin. Med. J. 121 (2008), 2312–2319.
44. Warner, F., Lubel, J., McCaughan, G., Angus, P., Liver fibrosis: a balance of ACEs?. Clin. Sci. 113 (2007), 109–118.
45. Wiemer, G., Dobrucki, L.W., Louka, F.R., Malinski, T., Heitsch, H., AVE 0991, a nonpeptide mimic of the effects of angiotensin-(1–7) on the endothelium. Hypertension 40 (2002), 847–852.
46. Yan, G.H., Choi, Y.H., Phellinus linteus extract exerts anti-asthmatic effects by suppressing NF-kappaB and p38 MAPK activity in an OVA-induced mouse model of asthma. Immune Netw. 14 (2014), 107–115.