Spironolactone attenuates bleomycin-induced pulmonary injury partially via modulating mononuclear phagocyte phenotype switching in circulating and alveolar compartments

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Ji, Wen E ^a   Yong Qiang, Ma ^a   Zhou, Xin ^a   Zhang, Yi Dan ^a   Lu, Rui Yi ^a   Guo, Zhao Zeng ^a   Sun, Hai Ying ^a   Hu, Dao Chuan ^a   Yang, Guo Hong ^a   Li, Yu Ming ^a   Wei, Lu Qing ^a  

^a MEDICAL COLLEGE OF CHINESE PEOPLE'S ARMED POLICE FORCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; CCL2 PROTEIN, MOUSE; INTERLEUKIN 1BETA; LEUKOCYTE ANTIGEN; LY ANTIGEN; LY6G ANTIGEN, MOUSE; MINERALOCORTICOID ANTAGONIST; MINERALOCORTICOID RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; SPIRONOLACTONE; TRANSFORMING GROWTH FACTOR BETA1;

ACUTE LUNG INJURY; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; LUNG ALVEOLUS; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MALE; METABOLISM; MONOCYTE; MOUSE; PATHOLOGY; PHENOTYPE; PULMONARY FIBROSIS;

ACUTE LUNG INJURY; ANIMALS; ANTIGENS, CD; ANTIGENS, LY; BLEOMYCIN; BRONCHOALVEOLAR LAVAGE FLUID; CHEMOKINE CCL2; GENE EXPRESSION; INTERLEUKIN-1BETA; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, INBRED C57BL; MINERALOCORTICOID RECEPTOR ANTAGONISTS; MONOCYTES; PHENOTYPE; PULMONARY ALVEOLI; PULMONARY FIBROSIS; RECEPTORS, MINERALOCORTICOID; SPIRONOLACTONE; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84894204578     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081090     Document Type: Article

References (69)

1. Russo RC, Guabiraba R, Garcia CC, Barcelos LS, Roffê E et al. (2009) Role of the chemokine receptor CXCR2 in bleomycin-induced pulmonary inflammation and fibrosis. Am J Respir Cell Mol Biol 40: 410-421. doi:10.1165/rcmb.2007-0364OC. PubMed: 18836137.
2. Nalysnyk L, Cid-Ruzafa J, Rotella P, Esser D (2012) Incidence and prevalence of idiopathic pulmonary fibrosis: review of the literature. Eur Respir Rev 21: 355-361. doi:10.1183/09059180.00002512. PubMed: 23204124.
3. King TE Jr, Pardo A, Selman M (2011) Idiopathic pulmonary fibrosis. Lancet 378: 1949-1961. doi:10.1016/S0140-6736(11)60052-4. PubMed: 21719092.
4. du Bois RM (2010) Strategies for treating idiopathic pulmonary fibrosis. Nat Rev Drug Discov 9: 129-140. doi:10.1038/nrd2958. PubMed: 20094055.
5. Reynolds HY (2005) Lung inflammation and fibrosis: an alveolar macrophage-centered perspective from the 1970s to 1980s. Am J Respir Crit Care Med 171: 98-102. doi:10.1164/rccm.200406-788PP. PubMed: 15557133.
6. Herold S, Mayer K, Lohmeyer J (2011) Acute lung injury: how macrophages orchestrate resolution of inflammation and tissue repair. Front Immunol 2: 65. PubMed: 22566854.
7. Bargagli E, Prasse A, Olivieri C, Muller-Quernheim J, Rottoli P (2011) Macrophage-derived biomarkers of idiopathic pulmonary fibrosis. Pulm Med 2011: 717130. PubMed: 21637368
8. Alber A, Howie SE, Wallace WA, Hirani N (2012) The role of macrophages in healing the wounded lung. Int J Exp Pathol 93: 243-251. doi:10.1111/j.1365- 2613.2012.00833.x. PubMed: 22774768.
9. Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496: 445-455. doi:10.1038/nature12034. PubMed: 23619691.
10. Johnston LK, Rims CR, Gill SE, McGuire JK, Manicone AM (2012) Pulmonary macrophage subpopulations in the induction and resolution of acute lung injury. Am J Respir Cell Mol Biol 47: 417-426. doi:10.1165/rcmb.2012-0090OC. PubMed: 22721830.
11. Martinez FO, Helming L, Gordon S (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27: 451-483. doi:10.1146/annurev.immunol.021908.132532. PubMed: 19105661.
12. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M et al. (2010) Development of monocytes, macrophages, and dendritic cells. Science 327: 656-661. doi:10.1126/science.1178331. PubMed: 20133564.
13. Ivashkiv LB (2013) Epigenetic regulation of macrophage polarization and function. Trends Immunol 34: 216-223. doi:10.1016/j.it.2012.11.001. PubMed: 23218730.
14. Spence S, Fitzsimons A, Boyd CR, Kessler J, Fitzgerald D et al. (2013) Suppressors of cytokine signaling 2 and 3 diametrically control macrophage polarization. Immunity 38: 66-78. doi:10.1016/j.immuni.2012.09.013. PubMed: 23177319.
15. Liu G, Abraham E (2013) MicroRNAs in immune response and macrophage polarization. Arterioscler Thromb Vasc Biol 33: 170-177. doi:10.1161/ATVBAHA. 112.300068. PubMed: 23325473.
16. Usher MG, Duan SZ, Ivaschenko CY, Frieler RA, Berger S et al. (2010) Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J Clin Invest 120: 3350-3364. doi:10.1172/JCI41080. PubMed: 20697155.
17. Kikuchi N, Ishii Y, Morishima Y, Yageta Y, Haraguchi N et al. (2011) Aggravation of bleomycin-induced pulmonary inflammation and fibrosis in mice lacking peroxiredoxin I. Am J Respir Cell Mol Biol 45: 600-609. doi:10.1165/rcmb.2010-0137OC. PubMed: 21239607.
18. Zhou X, Yun JL, Han ZQ, Gao F, Li H et al. (2011) Postinfarction healing dynamics in the mechanically unloaded rat left ventricle. Am J Physiol Heart Circ Physiol 300: H1863-H1874. doi:10.1152/ajpheart.00830.2010. PubMed: 21398590.
19. Szapiel SV, Elson NA, Fulmer JD, Hunninghake GW, Crystal RG (1979) Bleomycin-induced interstitial pulmonary disease in the nude, athymic mouse. Am Rev Respir Dis 120: 893-899. PubMed: 92208.
20. Wilson MS, Madala SK, Ramalingam TR, Gochuico BR, Rosas IO et al. (2010) Bleomycin and IL-1beta-mediated pulmonary fibrosis is IL-17A dependent. J Exp Med 207: 535-552. doi:10.1084/jem.20092121. PubMed: 20176803.
21. Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie AN et al. (2011) Innate lymphoid cells mediate influenza-induced airway hyperreactivity independently of adaptive immunity. Nat Immunol 12: 631-638. doi:10.1038/ni.2045. PubMed: 21623379.
22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609. (Pubitemid 34164012)
23. Imai Y, Kuba K, Rao S, Huan Y, Guo F et al. (2005) Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 436: 112-116. doi:10.1038/nature03712. PubMed: 16001071. (Pubitemid 40966195)
24. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK et al. (2003) Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426: 450-454. doi:10.1038/nature02145. PubMed: 14647384. (Pubitemid 37490132)
25. Kuba K, Imai Y, Rao S, Gao H, Guo F et al. (2005) A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat Med 11: 875-879. doi:10.1038/nm1267. PubMed: 16007097. (Pubitemid 41161120)
26. Mancini GB, Khalil N (2005) Angiotensin II type 1 receptor blocker inhibits pulmonary injury. Clin Invest Med 28: 118-126. PubMed: 16021985. (Pubitemid 40978706)
27. Tanaka J, Tajima S, Asakawa K, Sakagami T, Moriyama H et al. (2013) Preventive effect of irbesartan on bleomycin-induced lung injury in mice. Respir Investig 51: 76-83. doi:10.1016/j.resinv.2012.12.005. PubMed: 23790735.
28. Rey-Parra GJ, Vadivel A, Coltan L, Hall A, Eaton F et al. (2012) Angiotensin converting enzyme 2 abrogates bleomycin-induced lung injury. J Mol Med (Berl) 90: 637-647. doi:10.1007/s00109-012-0859-2. PubMed: 22246130.
29. Li P, Xiao HD, Xu J, Ong FS, Kwon M et al. (2010) Angiotensin-converting enzyme N-terminal inactivation alleviates bleomycin-induced lung injury. Am J Pathol 177: 1113-1121. doi:10.2353/ajpath.2010.081127. PubMed: 20651228.
30. Molina-Molina M, Serrano-Mollar A, Bulbena O, Fernandez-Zabalegui L, Closa D et al. (2006) Losartan attenuates bleomycin induced lung fibrosis by increasing prostaglandin E2 synthesis. Thorax 61: 604-610. doi:10.1136/thx.2005. 051946. PubMed: 16601095. (Pubitemid 44035141)
31. Waseda Y, Yasui M, Nishizawa Y, Inuzuka K, Takato H et al. (2008) Angiotensin II type 2 receptor antagonist reduces bleomycin-induced pulmonary fibrosis in mice. Respir Res 9: 43. doi:10.1186/1465-9921-9-43. PubMed: 18500976.
32. Zhao L, Zhao M, Fang Q (1998) [Spironolactone ameliorates rat pulmonary fibrosis induced by bleomycin A5]. Zhonghua Jie He He Hu Xi Za Zhi 21: 300-302. PubMed: 11326957.
33. Lieber GB, Fernandez X, Mingo GG, Jia Y, Caniga M et al. (2013) Mineralocorticoid receptor antagonists attenuate pulmonary inflammation and bleomycin-evoked fibrosis in rodent models. Eur J Pharmacol (doi:10.1016/j. ejphar.2013.08.019. PubMed: 24012780.
34. Misharin AV, Scott Budinger GR, Perlman H (2011) The lung macrophage: a Jack of all trades. Am J Respir Crit Care Med 184: 497-498. doi:10.1164/rccm. 201107-1343ED. PubMed: 21885631.
35. Janssen WJ, Barthel L, Muldrow A, Oberley-Deegan RE, Kearns MT et al. (2011) Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med 184: 547-560. doi:10.1164/rccm.201011-1891OC. PubMed: 21471090.
36. Gibbons MA, MacKinnon AC, Ramachandran P, Dhaliwal K, Duffin R et al. (2011) Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis. Am J Respir Crit Care Med 184: 569-581. doi:10.1164/rccm.201010-1719OC. PubMed: 21680953.
37. Rickard AJ, Morgan J, Tesch G, Funder JW, Fuller PJ et al. (2009) Deletion of mineralocorticoid receptors from macrophages protects against deoxycorticosterone/salt-induced cardiac fibrosis and increased blood pressure. Hypertension 54: 537-543. doi:10.1161/HYPERTENSIONAHA.109.131110. PubMed: 19635989.
38. Chawla A, Nguyen KD, Goh YP (2011) Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 11: 738-749. doi:10.1038/nri3071. PubMed: 21984069.
39. Frieler RA, Meng H, Duan SZ, Berger S, Schütz G et al. (2011) Myeloid-specific deletion of the mineralocorticoid receptor reduces infarct volume and alters inflammation during cerebral ischemia. Stroke 42: 179-185. doi:10.1161/STROKEAHA.110.598441. PubMed: 21106954.
40. Frieler RA, Ramnarayanan S, Mortensen RM (2012) Nuclear receptor control of opposing macrophage phenotypes in cardiovascular disease. Front Biosci 17: 1917-1930. doi:10.2741/4028. PubMed: 22201845.
41. Durante A, Peretto G, Laricchia A, Ancona F, Spartera M et al. (2012) Role of the renin-angiotensin-aldosterone system in the pathogenesis of atherosclerosis. Curr Pharm Des 18: 981-1004. doi:10.2174/138161212799436467. PubMed: 22283771.
42. Re RN (2004) Mechanisms of disease: local renin-angiotensinaldosterone systems and the pathogenesis and treatment of cardiovascular disease. Nat Clin Pract Cardiovasc Med 1: 42-47. PubMed: 16265259.
43. Fujita T (2010) Mineralocorticoid receptors, salt-sensitive hypertension, and metabolic syndrome. Hypertension 55: 813-818. doi:10.1161/HYPERTENSIONAHA. 109.149062. PubMed: 20176994.
44. Nguyen Dinh Cat A, Jaisser F (2012) Extrarenal effects of aldosterone. Curr Opin Nephrol Hypertens 21: 147-156. doi:10.1097/MNH.0b013e32834fb25b. PubMed: 22240440.
45. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C et al. (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13: 1118-1128. doi:10.1038/ni.2419. PubMed: 23023392.
46. Maus UA, Janzen S, Wall G, Srivastava M, Blackwell TS et al. (2006) Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation. Am J Respir Cell Mol Biol 35: 227-235. doi:10.1165/rcmb.2005-0241OC. PubMed: 16543608. (Pubitemid 44175323)
47. Yona S, Kim KW, Wolf Y, Mildner A, Varol D et al. (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38: 79-91. doi:10.1016/j.immuni.2012.12.001. PubMed: 23273845.
48. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB et al. (2013) Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38: 792-804. doi:10.1016/j.immuni.2013.04.004. PubMed: 23601688.
49. Prasse A, Pechkovsky DV, Toews GB, Jungraithmayr W, Kollert F et al. (2006) A vicious circle of alveolar macrophages and fibroblasts perpetuates pulmonary fibrosis via CCL18. Am J Respir Crit Care Med 173: 781-792. doi:10.1164/rccm.200509-1518OC. PubMed: 16415274.
50. Pechkovsky DV, Prasse A, Kollert F, Engel KM, Dentler J et al. (2010) Alternatively activated alveolar macrophages in pulmonary fibrosis-mediator production and intracellular signal transduction. Clin Immunol 137: 89-101. doi:10.1016/j.clim.2010.06.017. PubMed: 20674506.
51. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GR, Perlman H (2013) Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am J Respir Cell Mol Biol 49: 503-510. doi:10.1165/rcmb.2013-0086MA. PubMed: 23672262.
52. Bessich JL, Nymon AB, Moulton LA, Dorman D, Ashare A (2013) Low Levels of Insulin-like Growth Factor-1 Contribute to Alveolar Macrophage Dysfunction in Cystic Fibrosis. J Immunol 191: 378-385. doi:10.4049/jimmunol.1300221. PubMed: 23698746.
53. Shaykhiev R, Krause A, Salit J, Strulovici-Barel Y, Harvey BG et al. (2009) Smoking-dependent reprogramming of alveolar macrophage polarization: implication for pathogenesis of chronic obstructive pulmonary disease. J Immunol 183: 2867-2883. doi:10.4049/jimmunol.0900473. PubMed: 19635926.
54. Osterholzer JJ, Olszewski MA, Murdock BJ, Chen GH, Erb-Downward JR et al. (2013) Implicating exudate macrophages and Ly-6C(high) monocytes in CCR2-dependent lung fibrosis following gene-targeted alveolar injury. J Immunol 190: 3447-3457. doi:10.4049/jimmunol.1200604. PubMed: 23467934.
55. Vyas SP, Khatri K (2007) Liposome-based drug delivery to alveolar macrophages. Expert Opin Drug Deliv 4: 95-99. doi: 10.1517/17425247.4.2.95. PubMed: 17335407. (Pubitemid 46389908)
56. Maus UA, Waelsch K, Kuziel WA, Delbeck T, Mack M et al. (2003) Monocytes are potent facilitators of alveolar neutrophil emigration during lung inflammation: role of the CCL2-CCR2 axis. J Immunol 170: 3273-3278. PubMed: 12626586. (Pubitemid 36302205)
57. Kreisel D, Nava RG, Li W, Zinselmeyer BH, Wang B et al. (2010) In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc Natl Acad Sci U S A 107: 18073-18078. doi:10.1073/pnas.1008737107. PubMed: 20923880.
58. Dhaliwal K, Scholefield E, Ferenbach D, Gibbons M, Duffin R et al. (2012) Monocytes control second-phase neutrophil emigration in established lipopolysaccharide-induced murine lung injury. Am J Respir Crit Care Med 186: 514-524. doi:10.1164/rccm.201112-2132OC. PubMed: 22822022.
59. Voltz JW, Card JW, Carey MA, Degraff LM, Ferguson CD et al. (2008) Male sex hormones exacerbate lung function impairment after bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 39: 45-52. doi:10.1165/rcmb.2007- 0340OC. PubMed: 18276795. (Pubitemid 351883957)
60. Redente EF, Jacobsen KM, Solomon JJ, Lara AR, Faubel S et al. (2011) Age and sex dimorphisms contribute to the severity of bleomycin-induced lung injury and fibrosis. Am J Physiol Lung Cell Mol Physiol 301: L510-L518. doi:10.1152/ajplung.00122.2011. PubMed: 21743030.
61. Tschernig T, Pabst R (2009) What is the clinical relevance of different lung compartments? BMC Pulm Med 9: 39. doi:10.1186/1471-2466-9-39. PubMed: 19671154.
62. Maron BA, Zhang YY, White K, Chan SY, Handy DE et al. (2012) Aldosterone inactivates the endothelin-B receptor via a cysteinyl thiol redox switch to decrease pulmonary endothelial nitric oxide levels and modulate pulmonary arterial hypertension. Circulation 126: 963-974. doi:10.1161/CIRCULATIONAHA.112. 094722. PubMed: 22787113.
63. Preston IR, Sagliani KD, Warburton RR, Hill NS, Fanburg BL et al. (2013) Mineralocorticoid receptor antagonism attenuates experimental pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 304: L678-L688. doi:10.1152/ajplung.00300.2012. PubMed: 23457185.
64. Van Rheen Z, Fattman C, Domarski S, Majka S, Klemm D et al. (2011) Lung extracellular superoxide dismutase overexpression lessens bleomycin-induced pulmonary hypertension and vascular remodeling. Am J Respir Cell Mol Biol 44: 500-508. doi:10.1165/rcmb.2010-0065OC. PubMed: 20539010.
65. Sewing AC, Kantores C, Ivanovska J, Lee AH, Masood A et al. (2012) Therapeutic hypercapnia prevents bleomycin-induced pulmonary hypertension in neonatal rats by limiting macrophage-derived tumor necrosis factor-alpha. Am J Physiol Lung Cell Mol Physiol 303: L75-L87. doi:10.1152/ajplung.00072.2012. PubMed: 22582114.
66. Bergmann A, Eulenberg C, Wellner M, Rolle S, Luft F et al. (2010) Aldosterone abrogates nuclear factor kappaB-mediated tumor necrosis factor alpha production in human neutrophils via the mineralocorticoid receptor. Hypertension 55: 370-379. doi:10.1161/HYPERTENSIONAHA.109.141309. PubMed: 20065153.
67. Lawrence T, Natoli G (2011) Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 11: 750-761. doi:10.1038/nri3088. PubMed: 22025054.
68. Łabuzek K, Liber S, Bułdak L, Machnik G, Liber J et al. (2013) Eplerenone promotes alternative activation in human monocyte-derived macrophages. Pharmacol Rep 65: 226-234. PubMed: 23563043.
69. Zaynagetdinov R, Sherrill TP, Kendall PL, Segal BH, Weller KP et al. (2013) Identification of myeloid cell subsets in murine lungs using flow cytometry. Am J Respir Cell Mol Biol 49: 180-189. doi:10.1165/rcmb.2012-0366MA. PubMed: 23492192.