Pioglitazone attenuates endotoxin-induced acute lung injury by reducing neutrophil recruitment

European Respiratory Journal

Volumn 40, Issue 2, 2012, Pages 416-423

  Grommes, Jochen ^a   Mörgelin, Mathias ^c   Soehnlein, Oliver ^a,b,d  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c LUND UNIVERSITY   (Sweden)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Acute lung injury; Neutrophils; Pioglitazone

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; PIOGLITAZONE; REACTIVE OXYGEN METABOLITE; SODIUM CHLORIDE;

ACUTE LUNG INJURY; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ADHESION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; DEGRANULATION; DRUG EFFECT; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG ALVEOLUS; LUNG BLOOD VESSEL; LUNG LAVAGE; MALE; MEMBRANE PERMEABILITY; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN CONTENT; SALMONELLA ENTERITIDIS;

ACUTE LUNG INJURY; ADULT; AEROSOLS; ANIMALS; ANTI-INFLAMMATORY AGENTS; BRONCHOALVEOLAR LAVAGE FLUID; ENDOTOXINS; ESCHERICHIA COLI; FIBRONECTINS; FLOW CYTOMETRY; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; NEUTROPHILS; PERMEABILITY; REACTIVE OXYGEN SPECIES; SALMONELLA ENTERITIDIS; THIAZOLIDINEDIONES;

EID: 84862196286     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00091011     Document Type: Article

References (44)

1. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000; 342: 1334-1349. (Pubitemid 30408719)
2. Matute-Bello G, Frevert CW, Martin TR. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 2008; 295: L379-L399.
3. Grommes J, Soehnlein O. Contribution of neutrophils to acute lung injury. Mol Med 2011; 17: 293-307.
4. Looney MR, Su X, Van Ziffle JA, et al. Neutrophils and their Fcγ receptors are essential in a mouse model of transfusion-related acute lung injury. J Clin Invest 2006; 116: 1615-1623.
5. Soehnlein O, Oehmcke S, Ma X, et al. Neutrophil degranulation mediates severe lung damage triggered by streptococcal M1 protein. Eur Respir J 2008; 32: 405-412.
6. Gautam N, Olofsson AM, Herwald H, et al. Heparin-binding protein (HBP/CAP37): a missing link in neutrophil-evoked alteration of vascular permeability. Nat Med 2001; 7: 1123-1127. (Pubitemid 33010020)
7. Bdeir K, Higazi A, Kulikovskaya I, et al. Neutrophil alpha-defensins cause lung injury by disrupting the capillary-epithelial barrier. Am J Respir Crit Care Med 2010; 181: 935-946.
8. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 2006; 6: 541-550. (Pubitemid 43980526)
9. Massberg S, Grahl L, von Bruehl ML, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16: 887-896.
10. Brown JD, Plutzky J. Peroxisome proliferator-activated receptors as transcriptional nodal points and therapeutic targets. Circulation 2007; 115: 518-533. (Pubitemid 46184203)
11. Ricote M, Li AC, Willson TM, et al. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 1998; 391: 79-82. (Pubitemid 28079218)
12. Jiang C, Ting AT, Seed B. PPAR-γ agonists inhibit production of monocyte inflammatory cytokines. Nature 1998; 391: 82-86. (Pubitemid 28079219)
13. Becker J, Delayre-Orthez C, Frossard N, et al. Regulation of inflammation by PPARs: a future approach to treat lung inflammatory diseases? Fundam Clin Pharmacol 2006; 20: 429-447. (Pubitemid 44393958)
14. Park SJ, Lee KS, Kim SR, et al. Peroxisome proliferator-activated receptor γ agonist down-regulates IL-17 expression in a murine model of allergic airway inflammation. J Immunol 2009; 183: 3259-3267.
15. Aoki Y, Maeno T, Aoyagi K, et al. Pioglitazone, a peroxisome proliferator-activated receptor γ ligand, suppresses bleomycin-induced acute lung injury and fibrosis. Respiration 2009; 77: 311-319.
16. Soehnlein O, Kai-Larsen Y, Frithiof R, et al. Neutrophil primary granule proteins HBP and HNP1-3 boost bacterial phagocytosis by human and murine macrophages. J Clin Invest 2008; 118: 3491-3502.
17. Soehnlein O, Kenne E, Rotzius P, et al. Neutrophil secretion products regulate anti-bacterial activity in monocytes and macrophages. Clin Exp Immunol 2008; 151: 139-145. (Pubitemid 350230985)
18. Campia U, Matuskey LA, Panza JA. Peroxisome proliferator-activated receptor-γ activation with pioglitazone improves endothelium-dependent dilation in nondiabetic patients with major cardiovascular risk factors. Circulation 2006; 113: 867-875.
19. Marx N, Wöhrle J, Nusser T, et al. Pioglitazone reduces neointima volume after coronary stent implantation: a randomized, placebo-controlled, double-blind trial in nondiabetic patients. Circulation 2005; 112: 2792-2798.
20. Schaefer MB, Pose A, Ott J, et al. Peroxisome proliferator-activated receptor-alpha reduces inflammation and vascular leakage in a murine model of acute lung injury. Eur Respir J 2008; 32: 1344-1353.
21. Reddy RC, Narala VR, Keshamouni VG, et al. Sepsis-induced inhibition of neutrophil chemotaxis is mediated by activation of peroxisome proliferator-activated receptor-γ. Blood 2008; 112: 4250-4258.
22. Belperio JA, Keane MP, Burdick MD, et al. Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J Clin Invest 2002; 110: 1703-1716. (Pubitemid 35424249)
23. Moreland JG, Fuhrman RM, Pruessner JA, et al. CD11b and intercellular adhesion molecule-1 are involved in pulmonary neutrophil recruitment in lipopolysaccharide-induced airway disease. Am J Respir Cell Mol Biol 2002; 27: 474-480.
24. Haraguchi G, Kosuge H, Maejima Y, et al. Pioglitazone reduces systematic inflammation and improves mortality in apolipoprotein E knockout mice with sepsis. Intensive Care Med 2008; 34: 1304-1312. (Pubitemid 351904288)
25. Imamoto E, Yoshida N, Uchiyama K, et al. Inhibitory effect of pioglitazone on expression of adhesion molecules on neutrophils and endothelial cells. Biofactors 2004; 20: 37-47. (Pubitemid 38586208)
26. Cuzzocrea S, Pisano B, Dugo L, et al. Rosiglitazone, a ligand of the peroxisome proliferator-activated receptor-γ, reduces acute inflammation. Eur J Pharmacol 2004; 483: 79-93. (Pubitemid 38056607)
27. Kaundal RK, Iyer S, Kumar A, et al. Protective effects of pioglitazone against global cerebral ischemic-reperfusion injury in gerbils. J Pharmacol Sci 2009; 109: 361-367.
28. Yamashita M, Kushihara M, Hirasawa N, et al. Inhibition by troglitazone of the antigen-induced production of leukotrienes in immunoglobulin E-sensitized RBL-2H3 cells. Br J Pharmacol 2000; 129: 367-373. (Pubitemid 30072658)
29. Soehnlein O, Lindbom L. Neutrophil-derived azurocidin alarms the immune system. J Leukoc Biol 2009; 85: 344-351.
30. Gautam N, Herwald H, Hedqvist P, et al. Signaling via β2 integrins triggers neutrophil-dependent alteration in endothelial barrier function. J Exp Med 2000; 191: 1829-1839. (Pubitemid 30390347)
31. Herwald H, Cramer H, Mörgelin M, et al. M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 2004; 116: 367-379. (Pubitemid 38366314)
32. DiStasi MR, Ley K. Opening the flood-gates: how neutrophil-endothelial interactions regulate permeability. Trends Immunol 2009; 30: 547-556.
33. Ginzberg HH, Cherapanov V, Dong Q, et al. Neutrophil-mediated epithelial injury during transmigration: role of elastase. Am J Physiol Gastrointest Liver Physiol 2001; 281: G705-G717.
34. Hirche TO, Crouch EC, Espinola M, et al. Neutrophil serine proteinases inactivate surfactant protein D by cleaving within a conserved subregion of the carbohydrate recognition domain. J Biol Chem 2004; 279: 27688-27698. (Pubitemid 38812610)
35. Suzuki T, Yamashita C, Zemans RL, et al. Leukocyte elastase induces lung epithelial apoptosis via a PAR-1-, NF-κB-, and p53-dependent pathway. Am J Respir Cell Mol Biol 2009; 41: 742-755.
36. Tkalcevic J, Novelli M, Phylactides M, et al. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 2000; 12: 201-210. (Pubitemid 30398634)
37. Kawabata K, Hagio T, Matsumoto S, et al. Delayed neutrophil elastase inhibition prevents subsequent progression of acute lung injury induced by endotoxin inhalation in hamsters. Am J Respir Crit Care Med 2000; 161: 2013-2018. (Pubitemid 30418145)
38. Carnesecchi S, Deffert C, Pagano A, et al. NADPH oxidase-1 plays a crucial role in hyperoxia-induced acute lung injury in mice. Am J Respir Crit Care Med 2009; 180: 972-981.
39. Auten RL, Richardson RM, White JR, et al. Nonpeptide CXCR2 antagonist prevents neutrophil accumulation in hyperoxia-exposed newborn rats. J Pharmacol Exp Ther 2001; 299: 90-95. (Pubitemid 32905122)
40. Auten RL, Whorton MH, Mason SN. Blocking neutrophil influx reduces DNA damage in hyperoxia-exposed newborn rat lung. Am J Respir Cell Mol Biol 2002; 26: 391-397. (Pubitemid 34253922)
41. Chiarugi P, Pani G, Giannoni E, et al. Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J Cell Biol 2003; 161: 933-944. (Pubitemid 36718426)
42. Kubo H, Morgenstern D, Quinian WM, et al. Preservation of complement-induced lung injury in mice with deficiency of NADPH oxidase. J Clin Invest 1996; 97: 2680-2684. (Pubitemid 26187356)
43. Wang W, Suzuki Y, Tanigaki T, et al. Effect of the NADPH oxidase inhibitor apocynin on septic lung injury in guinea pigs. Am J Respir Crit Care Med 1994; 150: 1449-1452. (Pubitemid 24356666)
44. Soehnlein O. Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins. J Mol Med 2009; 87: 1157-1164.