Exudate macrophages attenuate lung injury by the release of IL-1 receptor antagonist in gram-negative pneumonia

American Journal of Respiratory and Critical Care Medicine

Volumn 183, Issue 10, 2011, Pages 1380-1390

  Herold, Susanne ^a   Tabar, Tannaz Shafiei ^a   Janßen, Hermann ^b   Hoegner, Katrin ^a   Cabanski, Maciej ^a   Lewe Schlosser, Peter ^a   Albrecht, Jens ^a   Driever, Frank ^a   Vadasz, Istvan ^a   Seeger, Werner ^a   Steinmueller, Mirko ^a   Lohmeyer, Juergen ^a  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b Hospital Dueren   (Germany)

Author keywords

Acute lung injury; Apoptosis; CC chemokine receptor 2; Interleukin 1; Klebsiella pneumoniae

Indexed keywords

CHEMOKINE RECEPTOR CCR2; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; ATTENUATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; KLEBSIELLA PNEUMONIAE; KLEBSIELLA PNEUMONIAE INFECTION; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; LUNG EXTRAVASCULAR FLUID; LUNG INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SURVIVAL;

ACUTE LUNG INJURY; ANIMALS; APOPTOSIS; CELL CULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; EXUDATES AND TRANSUDATES; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LUNG; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; PNEUMONIA, BACTERIAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 79956200862     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201009-1431OC     Document Type: Article

References (50)

1. Rubenfeld GD, Herridge MS. Epidemiology and outcomes of acute lung injury. Chest 2007;131:554-562. (Pubitemid 46280419)
2. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-1349. (Pubitemid 30408719)
3. Ganter MT, Roux J, Miyazawa B, Howard M, Frank JA, Su G, Sheppard D, Violette SM,Weinreb PH, Horan GS, et al. Interleukin-1beta causes acute lung injury via alphavbeta5 and alphavbeta6 integrin-dependent mechanisms. Circ Res 2008;102:804-812. (Pubitemid 351521585)
4. Frank JA, Pittet JF, Wray C, Matthay MA. Protection from experimental ventilator-induced acute lung injury by IL-1 receptor blockade. Thorax 2008;63:147-153. (Pubitemid 351236482)
5. Pugin J, Ricou B, Steinberg KP, Suter PM, Martin TR. Proinflammatory activity in bronchoalveolar lavage fluids from patients with ARDS, a prominent role for interleukin-1. Am J Respir Crit Care Med 1996;153:1850-1856. (Pubitemid 26187910)
6. Arend WP. The balance between IL-1 and IL-1ra in disease. Cytokine Growth Factor Rev 2002;13:323-340.
7. Donnelly SC, Strieter RM, Reid PT, Kunkel SL, Burdick MD, Armstrong I, Mackenzie A, Haslett C. The association between mortality rates and decreased concentrations of interleukin-10 and interleukin-1 receptor antagonist in the lung fluids of patients with the adult respiratory distress syndrome. Ann Intern Med 1996;125:191-196. (Pubitemid 126449261)
8. Alexander HR, Doherty GM, Buresh CM, Venzon DJ, Norton JA. A recombinant human receptor antagonist to interleukin 1 improves survival after lethal endotoxemia in mice. J ExpMed 1991;173:1029-1032.
9. Hirsch E, Irikura VM, Paul SM, Hirsh D. Functions of interleukin 1 receptor antagonist in gene knockout and overproducing mice. Proc Natl Acad Sci USA 1996;93:11008-11013. (Pubitemid 26333108)
10. Jacobs RF, Tabor DR, Burks AW, Campbell GD. Elevated interleukin-1 release by human alveolar macrophages during the adult respiratory distress syndrome. Am Rev Respir Dis 1989;140:1686-1692. (Pubitemid 20041055)
11. Toews GB. Cytokines and the lung. Eur Respir J Suppl 2001;34:3s-17s.
12. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 2007;117:902-909. (Pubitemid 46556746)
13. Herold S, Steinmueller M, von Wulffen W, Cakarova L, Pinto R, Pleschka S, Mack M, Kuziel WA, Corazza N, Brunner T, et al. Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J Exp Med 2008;205:3065-3077.
14. Rosseau S, Hammerl P, Maus U, Walmrath HD, Schutte H, Grimminger F, Seeger W, Lohmeyer J. Phenotypic characterization of alveolar monocyte recruitment in acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol 2000;279:L25-L35. (Pubitemid 30619520)
15. Winter C, Taut K, Srivastava M, Langer F, Mack M, Briles DE, Paton JC, Maus R, Welte T, Gunn MD, et al. Lung-specific overexpression of CC chemokine ligand (CCL) 2 enhances the host defense to streptococcus pneumoniae infection in mice: role of the CCL2-CCR2 axis. J Immunol 2007;178:5828-5838. (Pubitemid 46674380)
16. Xu F, Droemann D, Rupp J, Shen H, Wu X, Goldmann T, Hippenstiel S, Zabel P, Dalhoff K. Modulation of the inflammatory response to streptococcus pneumoniae in a model of acute lung tissue infection. Am J Respir Cell Mol Biol 2008;39:522-529.
17. Amano H, Morimoto K, Senba M, Wang H, Ishida Y, Kumatori A, Yoshimine H, Oishi K, Mukaida N, Nagatake T. Essential contribution of monocyte chemoattractant protein-1/C-C chemokine ligand-2 to resolution and repair processes in acute bacterial pneumonia. J Immunol 2004;172:398-409. (Pubitemid 38020494)
18. Cakarova L, Marsh LM, Wilhelm J, Mayer K, Grimminger F, Seeger W, Lohmeyer J, Herold S. Macrophage tumor necrosis factor-alpha induces epithelial expression of granulocyte-macrophage colony-stimulating factor: impact on alveolar epithelial repair. Am J Respir Crit Care Med 2009;180:521-532.
19. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008;8:958-969.
20. Herold S, Shafiei Tabar T, Cabanski M, Kuziel WA, Seeger W, Lohmeyer J, Steinmueller M. IL-1 receptor antagonist exerts antiapoptotic and barrier-protective effects towards alveolar epithelium in a murine model of LPS-induced acute lung injury [abstract]. Am J Respir Crit Care Med 2010;181:A2325.
21. Herold S, von Wulffen W, Steinmueller M, Pleschka S, Kuziel WA, Mack M, Srivastava M, Seeger W, Maus UA, Lohmeyer J. Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J Immunol 2006;177:1817-1824. (Pubitemid 44092519)
22. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 2000;20:4106-4114. (Pubitemid 30314508)
23. von Wulffen W, Steinmueller M, Herold S, Marsh LM, Bulau P, Seeger W, Welte T, Lohmeyer J, Maus UA. Lung dendritic cells elicited by Fms-like tyrosine 3-kinase ligand amplify the lung inflammatory response to lipopolysaccharide. Am J Respir Crit Care Med 2007;176:892-901. (Pubitemid 350097079)
24. Sunderkotter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, Drevets DA, Leenen PJ. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 2004;172:4410-4417. (Pubitemid 38375256)
25. Rosseau S, Wiechmann K, Moderer S, Selhorst J, Mayer K, Krull M, Hocke A, Slevogt H, Seeger W, Suttorp N, et al. Moraxella catarrhalis-infected alveolar epithelium induced monocyte recruitment and oxidative burst. Am J Respir Cell Mol Biol 2005;32:157-166. (Pubitemid 40189698)
26. Panos RJ, Rubin JS, Csaky KG, Aaronson SA, Mason RJ. Keratinocyte growth factor and hepatocyte growth factor/scatter factor are heparin-binding growth factors for alveolar type II cells in fibroblast-conditioned medium. J Clin Invest 1993;92:969-977. (Pubitemid 23262421)
27. Li CM, Khosla J, Hoyle P, Sannes PL. Transforming growth factor-beta(1) modifies fibroblast growth factor-2 production in type ii cells. Chest 2001;120:60S-61S.
28. Buff SM, Yu H, McCall JN, Caldwell SM, Ferkol TW, Flotte TR, Virella-Lowell IL. IL-10 delivery by AAV5 vector attenuates inflammation in mice with Pseudomonas pneumonia. Gene Ther 2010;17:567-576.
29. Dewberry RM, King AR, Crossman DC, Francis SE. Interleukin-1 receptor antagonist (IL-1ra) modulates endothelial cell proliferation. FEBS Lett 2008;582:886-890.
30. Ortiz LA, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, Phinney DG. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 2007;104:11002-11007. (Pubitemid 47175216)
31. Abbate A, Salloum FN, Vecile E, Das A, Hoke NN, Straino S, Biondi-Zoccai GG, Houser JE, Qureshi IZ, Ownby ED, et al. Anakinra, a recombinant human interleukin-1 receptor antagonist, inhibits apoptosis in experimental acute myocardial infarction. Circulation 2008;117:2670-2683.
32. Cabanski M, Wilhelm J, Zaslona Z, Steinmuller M, Fink L, Seeger W, Lohmeyer J. Genome-wide transcriptional profiling of mononuclear phagocytes recruited to mouse lungs in response to alveolar challenge with the TLR2 agonist Pam3CSK4. Am J Physiol Lung Cell Mol Physiol 2009;297:L608-L618.
33. Lee WL, Downey GP. Neutrophil activation and acute lung injury. Curr Opin Crit Care 2001;7:1-7. (Pubitemid 32163422)
34. Matute-Bello G, Frevert CW, Liles WC, Nakamura M, Ruzinski JT, Ballman K, Wong VA, Vathanaprida C, Martin TR. Fas/Fas ligand system mediates epithelial injury, but not pulmonary host defenses, in response to inhaled bacteria. Infect Immun 2001;69:5768-5776. (Pubitemid 32786516)
35. Morty RE, Eickelberg O, Seeger W. Alveolar fluid clearance in acute lung injury: what have we learned from animal models and clinical studies? Intensive Care Med 2007;33:1229-1240.
36. Ruckdeschel K, Pfaffinger G, Haase R, Sing A, Weighardt H, Hacker G, Holzmann B, Heesemann J. Signaling of apoptosis through TLRS critically involves toll/IL-1 receptor domain-containing adapter inducing IFN-beta, but not MyD88, in bacteria-infected murine macrophages. J Immunol 2004;173:3320-3328. (Pubitemid 39142041)
37. Glavan BJ, Holden TD, Goss CH, Black RA, Neff MJ, Nathens AB, Martin TR, Wurfel MM. Genetic variation in the Fas gene and associations with acute lung injury. Am J Respir Crit Care Med 2011;183:356-363.
38. Ying B, Yang T, Song X, Hu X, Fan H, Lu X, Chen L, Cheng D, Wang T, Liu D, et al. Quercetin inhibits IL-1 beta-induced ICAM-1 expression in pulmonary epithelial cell line A549 through the MAPK pathways. Mol Biol Rep 2009;36:1825-1832.
39. Lappalainen U, Whitsett JA, Wert SE, Tichelaar JW, Bry K. Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. Am J Respir Cell Mol Biol 2005;32:311-318. (Pubitemid 40478306)
40. Roux J, Kawakatsu H, Gartland B, Pespeni M, Sheppard D, Matthay MA, Canessa CM, Pittet JF. Interleukin-1beta decreases expression of the epithelial sodium channel alpha-subunit in alveolar epithelial cells via a p38 MAPK-dependent signaling pathway. J Biol Chem 2005;280:18579-18589. (Pubitemid 41379556)
41. Lamacchia C, Palmer G, Bischoff L, Rodriguez E, Talabot-Ayer D, Gabay C. Distinct roles of hepatocyte- and myeloid cell-derived IL-1 receptor antagonist during endotoxemia and sterile inflammation in mice. J Immunol 2010;185:2516-2524.
42. Patwari PP, O'Cain P, Goodman DM, Smith M, Krushkal J, Liu C, Somes G, Quasney MW, Dahmer MK. Interleukin-1 receptor antagonist intron 2 variable number of tandem repeats polymorphism and respiratory failure in children with community-acquired pneumonia. Pediatr Crit Care Med 2008;9:553-559.
43. Fisher CJ Jr, Dhainaut JF, Opal SM, Pribble JP, Balk RA, Slotman GJ, Iberti TJ, Rackow EC, Shapiro MJ, Greenman RL, et al. Recombinant human interleukin 1 receptor antagonist in the treatment of patients with sepsis syndrome. Results from a randomized, double-blind, placebo-controlled trial. Phase III rhIL-1ra Sepsis Syndrome Study Group. JAMA 1994;271:1836-1843.
44. Opal SM, Fisher CJ Jr, Dhainaut JF, Vincent JL, Brase R, Lowry SF, Sadoff JC, Slotman GJ, Levy H, Balk RA, et al. Confirmatory interleukin-1 receptor antagonist trial in severe sepsis: a phase III, randomized, double-blind, placebo-controlled, multicenter trial. The interleukin-1 receptor antagonist sepsis investigator group. Crit Care Med 1997;25:1115-1124. (Pubitemid 27310249)
45. Parsons PE, Moss M, Vannice JL, Moore EE, Moore FA, Repine JE. Circulating IL-1ra and IL-10 levels are increased but do not predict the development of acute respiratory distress syndrome in at-risk patients. Am J Respir Crit Care Med 1997;155:1469-1473. (Pubitemid 27172800)
46. Geiser T, Jarreau PH, Atabai K, Matthay MA. Interleukin-1beta augments in vitro alveolar epithelial repair. Am J Physiol Lung Cell Mol Physiol 2000;279:L1184-L1190. (Pubitemid 32009504)
47. Geiser T, Atabai K, Jarreau PH, Ware LB, Pugin J, Matthay MA. Pulmonary edema fluid from patients with acute lung injury augments in vitro alveolar epithelial repair by an IL-1beta-dependent mechanism. Am J Respir Crit Care Med 2001;163:1384-1388. (Pubitemid 32506603)
48. Tanabe M, Matsumoto T, Shibuya K, Tateda K, Miyazaki S, Nakane A, Iwakura Y, Yamaguchi K. Compensatory response of IL-1 gene knockout mice after pulmonary infection with Klebsiella pneumoniae. J Med Microbiol 2005;54:7-13.
49. Gasse P, Mary C, Guenon I, Noulin N, Charron S, Schnyder-Candrian S, Schnyder B, Akira S, Quesniaux VF, Lagente V, et al. IL-1r1/MyD88 signaling and the inflammasome are essential in pulmonary inflammation and fibrosis in mice. J Clin Invest 2007;117:3786-3799. (Pubitemid 350224089)
50. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003;3:23-35. (Pubitemid 37328697)