Chronic allergic pulmonary inflammation is aggravated in angiotensin-(1–7) mas receptor knockout mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 311, Issue 6, 2016, Pages L1141-L1148

  Magalhães, Giselle S ^a   Rodrigues Machado, Maria Glória ^a   Motta Santos, Daisy ^a   Alenina, Natalia ^b   Bader, Michael ^b   Santos, Robson A ^a   Barcelos, Lucíola S ^a   Campagnole Santos, Maria José ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Airway remodeling; Angiotensin (1 7); Asthma; Mas receptor; Pulmonary remodeling

Indexed keywords

ANGIOTENSIN[1-7]; INTERLEUKIN 13; MAS RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; OVALBUMIN; RANTES; RECEPTOR; SODIUM CHLORIDE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ANGIOTENSIN I; ANGIOTENSIN I (1-7); CYTOKINE; G PROTEIN COUPLED RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO-ONCOGENE PROTEINS C-MAS-1;

ALLERGIC PNEUMONITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOLE; ARTICLE; CELL INFILTRATION; CHRONIC DISEASE; CONTROLLED STUDY; EXERCISE; EXTRACELLULAR MATRIX; INFLAMMATORY CELL; KNOCKOUT MOUSE; LUNG PARENCHYMA; MOUSE; NEBULIZATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE; TASK PERFORMANCE; WILD TYPE MOUSE; ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; COMPLICATION; HYPERSENSITIVITY; LUNG; METABOLISM; PATHOLOGY; PNEUMONIA; SWIMMING;

ANGIOTENSIN I; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HYPERSENSITIVITY; LUNG; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; PHYSICAL CONDITIONING, ANIMAL; PNEUMONIA; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SWIMMING;

EID: 85006274901     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00029.2016     Document Type: Article

References (36)

1. Almeida PW, Gomes-Filho A, Ferreira AJ, Rodrigues CE, Dias- Peixoto MF, Russo RC, Teixeira MM, Cassali GD, Ferreira E, Santos IC, Garcia AM, Silami-Garcia E, Wisløff U, Pussieldi GA. Swim training suppresses tumor growth in mice. J Appl Physiol 107: 261–265, 2009.
2. Almeida PW, Melo MB, Lima RF, Gavioli M, Santiago NM, Greco L, Jesus IC, Nocchi E, Parreira A, Alves MN, Mitraud L, Resende RR, Campagnole-Santos MJ, Santos RA, Guatimosim S. Beneficial effects of angiotensin-(1–7) against deoxycorticosterone acetate-induced diastolic dysfunction occur independently of changes in blood pressure. Hypertension 66: 389–395, 2015.
3. Conrad ML, Yildirim AO, Sonar SS, Kılıc A, Sudowew S, Lunowz M, Teich R, Renz H, Garn H. Comparison of adjuvant and adjuvant-free murine experimental asthma models. Clin Exper Allergy 39: 1246–1254, 2009.
4. da Silveira KD, Coelho FM, Vieira AT, Sachs D, Barroso LC, Costa VV, Bretas TL, Bader M, de Sousa LP, da Silva TA, dos Santos RA, Simões e Silva AC, Teixeira MM. Anti-inflammatory effects of the activation of the angiotensin-(1–7) receptor, MAS, in experimental models of arthritis. J Immunol 185: 5569–5576, 2010.
5. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart RE, Acton S. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1–9. Circ Res 87: E1–9, 2000.
6. El-Hashim AZ, Renno WM, Raghupathy R, Abduo HT, Akhtar S, Benter IF. Angiotensin-(1–7) inhibits allergic inflammation, via the MAS1 receptor, through suppression of ERK1/2- and NF-κB-dependent pathways. Br J Pharmacol 166: 1964–1976, 2012.
7. Holgate ST. Asthma: a simple concept but in reality a complex disease. Eur J Clin Invest 41: 1339–1352, 2011.
8. Hosoki K, Ying S, Corrigan C, Qi H, Kurosky A, Jennings K, Sun Q, Boldogh I, Sur S. Analysis of a panel of 48 cytokines in BAL fluids specifically identifies IL-8 levels as the only cytokine that distinguishes controlled asthma from uncontrolled asthma, and correlates inversely with FEV1. PLoS One 10: e0126035, 2015.
9. Ingram JL, Kraft M. IL-13 in asthma and allergic disease: asthma phenotypes and targeted therapies. J Allergy Clin Immunol 130: 829–842, 2012.
10. Jiang T, Gao L, Lu J, Zhang YD. ACE2-Ang-(1–7)-Mas axis in brain: a potential target for prevention and treatment of ischemic stroke. Curr Neuropharmacol 11: 209–217, 2013.
11. Kumar RK, Herbert C, Foster PS. The “classical” ovalbumin challenge model of asthma in mice. Curr Drug Targets 9: 485–494, 2008.
12. Lee PJ, Zhang X, Shan P, Ma B, Lee CG, Homer RJ, Zhu Z, Rincon M, Mossman BT, Elias JA. ERK1/2 mitogen-activated protein kinase selectively mediates IL-13-induced lung inflammation and remodeling in vivo. J Clin Invest 116: 163–173, 2006.
13. Liang B, Wang X, Zhang N, Yang H, Bai R, Liu M, Bian Y, Xiao C, Yang Z. Angiotensin-(1–7) attenuates angiotensin II-induced ICAM-1, VCAM-1, and MCP-1 expression via the MAS receptor through suppression of P38 and NF-κB pathways in HUVECs. Cell Physiol Biochem 35: 2472–2482, 2015.
14. Lin TY, Venkatesan N, Nishioka M, Kyoh S, Al-Alwan L, Baglole CJ, Eidelman DH, Ludwig MS, Hamid Q. Monocyte-derived fibrocytes induce an inflammatory phenotype in airway smooth muscle cells. Clin Exp Allergy 44: 1347–1360, 2014.
15. Ma B, Zhu Z, Homer RJ, Gerard C, Strieter R, Elias JA. The C10/CCL6 chemokine and CCR1 play critical roles in the pathogenesis of IL-13-induced inflammation and remodeling. J Immunol 172: 1872–1881, 2004.
16. Ma B, Liu W, Homer RJ, Lee PJ, Coyle AJ, Lora JM, Lee CG, Elias JA. Role of CCR5 in the pathogenesis of IL-13-induced inflammation and remodeling. J Immunol 176: 4968–4978, 2006.
17. Magalhães GS, Rodrigues-Machado MG, Motta-Santos D, Silva AR, Caliari MV, Prata LO, Abreu SC, Rocco PR, Barcelos LS, Santos RA, Campagnole-Santos MJ. Angiotensin-(1–7) attenuates airway remodelling and hyperresponsiveness in a model of chronic allergic lung inflammation. Br J Pharmacol 172: 2330–2342, 2015.
18. Marques FD, Ferreira AJ, Sinisterra RD, Jacoby BA, Sousa FB, Caliari MV, Silva GA, Melo MB, Nadu AP, Souza LE, Irigoyen MC, Almeida AP, Santos RA. An oral formulation of angiotensin-(1–7) produces cardioprotective effects in infarcted and isoproterenol-treated rats. Hypertension 57: 477–483, 2011.
19. Meng Y, Yu CH, Li W, Li T, Luo W, Huang S, Wu PS, Cai SX, Li X. Angiotensin-converting enzyme 2/angiotensin-(1–7)/Mas axis protects against lung fibrosis by inhibiting the MAPK/NF-κB pathway. Am J Respir Cell Mol Biol 50: 723–736, 2014.
20. Modi WS, Yoshimura T. Isolation of novel GRO genes and a phylogenetic analysis of the CXC chemokine subfamily in mammals. Mol Biol Evol 16: 180–93, 1999.
21. Rael EL, Lockey RF. Interleukin-13 signaling and its role in asthma. World Allergy Organ J 4: 54–64, 2011.
22. Regenhardt RW, Desland F, Mecca AP, Pioquinto DJ, Afzal A, Mocco J, Sumners C. Anti-inflammatory effects of angiotensin-(1–7) in ischemic stroke. Neuropharmacology 71: 154–163, 2013.
23. Rincon M, Irvin CG. Role of IL-6 in asthma and other inflammatory pulmonary diseases. Int J Biol Sci 8: 1281–1290, 2012.
24. Rodrigues-Machado MG, Magalhães GS, Cardoso JA, Kangussu LM, Murari A, Caliari MV, Oliveira ML, Cara DC, Noviello ML, Marques FD, Pereira JM, Lautner RQ, Santos RA, Campagnole-Santos MJ. AVE 0991, a non-peptide mimic of angiotensin-(1–7) effects, attenuates pulmonary remodelling in a model of chronic asthma. Br J Pharmacol 170: 835–846, 2013.
25. Santos RA. Angiotensin-(1–7). Hypertension 63: 1138–1147, 2014.
26. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SV, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss HP, Speth R, Walther T. Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci USA 100: 8258–8263, 2003.
27. Seumois G, Chavez L, Gerasimova A, Lienhard M, Omran N, Kalinke L, Vedanayagam M, Ganesan AP, Chawla A, Djukanović R, Ansel KM, Peters B, Rao A, Vijayanand P. Epigenomic analysis of primary human T cells reveals enhancers associated with TH2 memory cell differentiation and asthma susceptibility. Nat Immunol 15: 777–788, 2014.
28. Shenoy V, Ferreira AJ, Qi Y, Fraga-Silva RA, Díez-Freire C, Dooies A, Jun JY, Sriramula S, Mariappan N, Pourang D, Venugopal CS, Francis J, Reudelhuber T, Santos RA, Patel JM, Raizada MK, Katovich MJ. The angiotensin-converting enzyme 2/angiogenesis-(1–7)/Mas axis confers cardiopulmonary protection against lung fibrosis and pulmonary hypertension. Am J Respir Crit Care Med 182: 1065–1072, 2010.
29. Simões e Silva AC, Silveira KD, Ferreira AJ, Teixeira MM. ACE2, angiotensin-(1–7) and Mas receptor axis in inflammation and fibrosis. Br J Pharmacol 169: 477–492, 2013.
30. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem 275: 3238–3242, 2000.
31. Vieira RP, Claudino RC, Duarte AC, Santos AB, Perini A, Faria Neto HC, Mauad T, Martins MA, Dolhnikoff M, Carvalho CR. Aerobic exercise decreases chronic allergic lung inflammation and airway remodeling in mice. Am J Respir Crit Care Med 176: 871–877, 2007.
32. Vieira RP, de Andrade VF, Duarte AC, Dos Santos AB, Mauad T, Martins MA, Dolhnikoff M, Carvalho CR. Aerobic conditioning and allergic pulmonary inflammation in mice. II. Effects on lung vascular and parenchymal inflammation and remodeling. Am J Physiol Lung Cell Mol Physiol 295: L670–L679, 2008.
33. Vogiatzis I, Zakynthinos G, Andrianopoulos V. Mechanisms of physical activity limitation in chronic lung diseases. Pulm Med 2012: 634–761, 2012.
34. Wong CK, Wang CB, Li ML, Ip WK, Tian YP, Lam CW. Induction of adhesion molecules upon the interaction between eosinophils and bronchial epithelial cells: involvement of p38 MAPK and NF-kappaB. Int Immunopharmacol 6: 1859–1871, 2006.
35. Yalcin AD, Bisgin A, Gorczynski RM. IL-8, IL-10, TGF-, and GCSF levels were increased in severe persistent allergic asthma patients with the anti-IgE treatment. Mediators Inflamm 2012: 720976, 2012.
36. Zhu Z, Bing Ma Zheng T, Homer RJ, Lee CG, Charo IF, Noble P, Elias JA. IL-13-induced chemokine responses in the lung: role of CCR2 in the pathogenesis of IL-13-induced inflammation and remodeling. J Immunol 168: 2953–2962, 2002.