Bench-to-bedside review: Acute respiratory distress syndrome - How neutrophils migrate into the lung

Critical Care

Volumn 8, Issue 6, 2004, Pages 453-461

  Reutershan, Jörg ^a,b   Ley, Klaus ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Acute respiratory distress syndrome; Adhesion molecules; Chemokines; Neutrophil recruitment

Indexed keywords

ACTIN; ANTIBIOTIC AGENT; BACTERIUM LIPOPOLYSACCHARIDE; BETA2 INTEGRIN; CD18 ANTIGEN; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CXCR2; COBROTOXIN; COMPLEMENT COMPONENT C5A; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; HYDROCHLORIC ACID; IMMUNOGLOBULIN G; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; SELECTIN; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; VASCULAR CELL ADHESION MOLECULE 1;

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; ARTIFICIAL VENTILATION; CELL TRANSPORT; CRITICAL ILLNESS; CYTOSKELETON; DISEASE SEVERITY; ESCHERICHIA COLI; EXPERIMENTAL MODEL; FLUID THERAPY; HUMAN; LEUKOCYTE ACTIVATION; LEUKOCYTE MIGRATION; LUNG ALVEOLUS; LUNG BLOOD VESSEL; LUNG INTERSTITIUM; LUNG PARENCHYMA; MOLECULAR MECHANICS; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; RESUSCITATION; REVIEW; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PNEUMONIAE;

CELL ADHESION MOLECULES; CRITICAL ILLNESS; CYTOKINES; HUMANS; NEUTROPHILS; RESPIRATORY DISTRESS SYNDROME, ADULT;

EID: 11344289641     PISSN: 13648535     EISSN: None     Source Type: Journal    
DOI: 10.1186/cc2881     Document Type: Review

References (92)

1. Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med 2000, 342:1334-1349.
2. Abraham E: Neutrophils and acute lung injury. Crit Care Med 2003, Suppl:S195-S199.
3. Abraham E, Carmody A, Shenkar R, Arcaroli J: Neutrophils as early immunologic effectors in hemorrhage- or endotoxemia-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 2000, 279:L1137-L1145.
4. Azoulay E, Darmon M, Delclaux C, Fieux F, Bornstain C, Moreau D, Attalah H, Le Gall JR, Schlemmer B: Deterioration of previous acute lung injury during neutropenia recovery. Crit Care Med 2002, 30:781-786.
5. Doerschuk CM, Beyers N, Coxson HO, Wiggs B, Hogg JG: Comparison of neutrophil and capillary diameters and their relation to neutrophil sequestration in the lung. J Appl Physiol 1993, 74:3040-3045.
6. Doerschuk CM, Allard MF, Martin BA, MacKenzie A, Autor AP, Hogg JC: Marginated pool of neutrophils in rabbit lungs. J Appl Physiol 1987, 63:1806-1815.
7. Butcher EC: Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 1991, 67: 033-1036.
8. Springer TA: Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994, 76: 301-314.
9. Ley K: Integration of inflammatory signals by rolling neutrophils. Immunol Rev 2002, 186:8-18.
10. Li Q, Park PW, Wilson CL, Parks WC: Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002, 111:635-646.
11. Wagner JG, Harkema JR, Roth RA: Pulmonary leukostasis and the inhibition of airway neutrophil recruitment are early events in the endotoxemic rat. Shock 2002, 17:151-158.
12. Drost EM, MacNee W: Potential role of IL-8, platelet-activating factor and TNF-alpha in the sequestration of neutrophils in the lung: effects on neutrophil deformability, adhesion receptor expression, and chemotaxis. Eur J Immunol 2002, 32: 93-403.
13. Tanaka H, Nishino M, Dahms TE: Physiologic responses to small emboli and hemodynamic effects of changes in deformability of polymorphonuclear leukocytes in isolated rabbit lung. Microvasc Res 2002, 63:81-90.
14. Doerschuk CM: The role of CD18-mediated adhesion in neutrophil sequestration induced by infusion of activated plasma in rabbits. Am J Respir Cell Mol Biol 1992, 7:140-148.
15. Worthen GS, Schwab B, III, Elson EL, Downey GP: Mechanics of stimulated neutrophils: cell stiffening induces retention in capillaries. Science 1989, 245:183-186.
16. Skoutelis AT, Kaleridis V, Athanassiou GM, Kokkinis KI, Missirlis YF, Bassaris HP: Neutrophil deformability in patients with sepsis, septic shock, and adult respiratory distress syndrome. Crit Care Med 2000, 28:2355-2359.
17. Doyle NA, Bhagwan SD, Meek BB, Kutkoski GJ, Steeber DA, Tedder TF, Doerschuk CM: Neutrophil margination, sequestration, and emigration in the lungs of L-selectin-deficient mice. J Clin Invest 1997, 99:526-533.
18. Olson TS, Singbartl K, Ley K: L-selectin is required for fMLP- but not C5a-induced margination of neutrophils in pulmonary circulation. Am J Physiol Regul Integr Comp Physiol 2002, 282: R1245-R1252.
19. Carraway MS, Welty-Wolf KE, Kantrow SP, Huang YC, Simonson SG, Que LG, Kishimoto TK, Piantadosi CA: Antibody to E- and L-selectin does not prevent lung injury or mortality in septic baboons. Am J Respir Crit Care Med 1998, 157:938-949.
20. Andonegui G, Bonder CS, Green F, Mullaly SC, Zbytnuik L, Raharjo E, Kubes P: Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 2003, 111:1011-1020.
21. Burns JA, Issekutz TB, Yagita H, Issekutz AC: The beta2, alpha4, alpha5 integrins and selectins mediate chemotactic factor and endotoxin-enhanced neutrophil sequestration in the lung. Am J Pathol 2001, 158:1809-1819.
22. Burns AR, Smith CW, Walker DC: Unique structural features that influence neutrophil emigration into the lung. Physiol Rev 2003, 83:309-336.
23. Furuse M, Itoh M, Hirase T, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S: Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J Cell Biol 1994, 127:1617-1626.
24. Su WH, Chen HI, Jen CJ: Differential movements of VE-cadherin and PECAM-1 during transmigration of polymorphonuclear leukocytes through human umbilical vein endothelium. Blood 2002, 100:3597-3603.
25. Mackarel AJ, Cottell DC, Russell KJ, FitzGerald MX, O'Connor CM: Migration of neutrophils across human pulmonary endothelial cells is not blocked by matrix metalloproteinase or serine protease inhibitors. Am J Respir Cell Mol Biol 1999, 20:1209-1219.
26. Betsuyaku T, Shipley JM, Liu Z, Senior RM: Neutrophil emigration in the lungs, peritoneum, and skin does not require gelatinase B. Am J Respir Cell Mol Biol 1999, 20:1303-1309.
27. Patel KD, Cuvelier SL, Wiehler S: Selectins: critical mediators of leukocyte recruitment. Semin Immunol 2002, 14: 3-81.
28. Diamond MS, Springer TA: The dynamic regulation of integrin adhesiveness. Curr Biol 1994, 4:506-517.
29. Motosugi H, Quinlan WM, Bree M, Doerschuk CM: Role of CD11b in focal acid-induced pneumonia and contralateral lung injury in rats. Am J Respir Crit Care Med 1998, 157:192-198.
30. Mizgerd JP, Horwitz BH, Quillen HC, Scott ML, Doerschuk CM: Effects of CD18 deficiency on the emigration of murine neutrophils during pneumonia. J Immunol 1999, 163:995-999.
31. Wagner JG, Driscoll KE, Roth RA: Inhibition of pulmonary neutrophil trafficking during endotoxemia is dependent on the stimulus for migration. Am J Respir Cell Mol Biol 1999, 20: 769-776.
32. Burns AR, Takei F, Doerschuk CM: Quantitation of ICAM-1 expression in mouse lung during pneumonia. J Immunol 1994, 153:3189-3198.
33. Moreland JG, Fuhrman RM, Pruessner JA, Schwartz DA: 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.
34. Ohno S, Malik AB: Polymorphonuclear leucocyte (PMN) inhibitory factor prevents PMN-dependent endothelial cell injury by an anti-adhesive mechanism. J Cell Physiol 1997, 171:212-216.
35. Vaporciyan AA, DeLisser HM, Yan HC, Mendiguren II, Thom SR, Jones ML, Ward PA, Albelda SM: Involvement of platelet-endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science 1993, 262:1580-1582.
36. Muller AM, Cronen C, Muller KM, Kirkpatrick CJ: Heterogeneous expression of cell adhesion molecules by endothelial cells in ARDS. J Pathol 2002, 198:270-275.
37. Eppihimer MJ, Russell J, Langley R, Vallien G, Anderson DC, Granger DN: Differential expression of platelet-endothelial cell adhesion molecule-1 (PECAM-1) in murine tissues. Microcirculation 1998, 5:179-188.
38. Tasaka S, Qin L, Saijo A, Albelda SM, DeLisser HM, Doerschuk CM: Platelet endothelial cell adhesion molecule-1 in neutrophil emigration during acute bacterial pneumonia in mice and rats. Am J Respir Crit Care Med 2003, 167:164-170.
39. Burns JA, Issekutz TB, Yagita H, Issekutz AC: The alpha 4 beta 1 (very late antigen (VLA)-4, CD49d/CD29) and alpha 5 beta 1 (VLA-5, CD49e/CD29) integrins mediate beta 2 (CD11/CD18) integrin-independent neutrophil recruitment to endotoxin-induced lung inflammation. J Immunol 2001, 166:4644-4649.
40. Mizgerd JP, Meek BB, Kutkoski GJ, Bullard DC, Beaudet AL, Doerschuk CM: Selectins and neutrophil traffic: margination and Streptococcus pneumoniae-induced emigration in murine lungs. J Exp Med 1996, 184:639-645.
41. Mulligan MS, Miyasaka M, Ward PA: Protective effects of combined adhesion molecule blockade in models of acute lung injury. Proc Assoc Am Physicians 1996, 108:198-208.
42. Hayashi H, Koike H, Kurata Y, Imanishi N, Tojo SJ: Protective effects of sialyl Lewis X and anti-P-selectin antibody against lipopolysaccharide-induced acute lung injury in rabbits. Eur J Pharmacol 1999, 370:47-56.
43. Kubo H, Doyle NA, Graham L, Bhagwan SD, Quinlan WM, Doerschuk CM: L- and P-selectin and CD11/CD18 in intracapillary neutrophil sequestration in rabbit lungs. Am J Respir Crit Care Med 1999, 159:267-274.
44. Zhang H, Downey GP, Suter PM, Slutsky AS, Ranieri VM: Conventional mechanical ventilation is associated with bronchoalveolar lavage-induced activation of polymorphonuclear leukocytes: a possible mechanism to explain the systemic consequences of ventilator-induced lung injury in patients with ARDS. Anesthesiology 2002, 97: 426-1433.
45. The Acute Respiratory Distress Syndrome Network: Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 2000, 342:1301-1308.
46. Olson TS, Ley K: Chemokines and chemokine receptors in leukocyte trafficking. Am J Physiol Regul Integr Comp Physiol 2002, 283:R7-R28.
47. Ley K: Arrest chemokines. Microcirculation 2003, 10:289-295.
48. Rollins BJ: Chemokines. Blood 1997, 90: 09-928.
49. Rot A, Von Andrian UH: Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 2004, 22:891-928.
50. Nieto M, Frade JM, Sancho D, Mellado M, Martinez A, Sanchez-Madrid F: Polarization of chemokine receptors to the leading edge during lymphocyte chemotaxis. J Exp Med 1997, 186: 153-158.
51. Takai Y, Sasaki T, Matozaki T: Small GTP-binding proteins. Physiol Rev 2001, 81:153-208.
52. Ambruso DR, Knall C, Abell AN, Panepinto J, Kurkchubasche A, Thurman G, Gonzalez-Aller C, Hiester A, deBoer M, Harbeck RJ, Oyer R, Johnson GL, Roos D: Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. Proc Natl Acad Sci USA 2000, 97:4654-4659.
53. Miller EJ, Cohen AB, Nagao S, Griffith D, Maunder RJ, Martin TR, Weiner-Kronish JP, Sticherling M, Christophers E, Matthay MA: Elevated levels of NAP-1/interleukin-8 are present in the airspaces of patients with the adult respiratory distress syndrome and are associated with increased mortality. Am Rev Respir Dis 1992, 146: 27-432.
54. Folkesson HG, Matthay MA, Hebert CA, Broaddus VC: Acid aspiration-induced lung injury in rabbits is mediated by interleukin-8-dependent mechanisms. J Clin Invest 1995, 96: 07-116.
55. Osman MO, Kristensen JU, Jacobsen NO, Lausten SB, Deleuran B, Deleuran M, Gesser B, Matsushima K, Larsen CG, Jensen SL: A monoclonal anti-interleukin 8 antibody (WS-4) inhibits cytokine response and acute lung injury in experimental severe acute necrotising pancreatitis in rabbits. Gut 1998, 43: 232-239.
56. Sekido N, Mukaida N, Harada A, Nakanishi I, Watanabe Y, Matsushima K: Prevention of lung reperfusion injury in rabbits by a monoclonal antibody against interleukin-8. Nature 1993, 365: 654-657.
57. Krupa A, Kato H, Matthay MA, Kurdowska AK: Proinflammatory activity of anti-IL-8 autoantibody:IL-8 complexes in alveolar edema fluid from patients with Acute Lung Injury. Am J Physiol Lung Cell Mol Physiol 2004, 286:L1105-L1113.
58. Kurdowska A, Noble JM, Steinberg KP, Ruzinski JT, Hudson LD, Martin TR: Anti-interleukin 8 autoantibody: interleukin 8 complexes in the acute respiratory distress syndrome. Relationship between the complexes and clinical disease activity. Am J Respir Crit Care Med 2001, 163:463-468.
59. Kurdowska A, Noble JM, Grant IS, Robertson CR, Haslett C, Donnelly SC: Anti-interleukin-8 autoantibodies in patients at risk for acute respiratory distress syndrome. Crit Care Med 2002, 30: 335-2337.
60. Lomas JL, Chung CS, Grutkoski PS, LeBlanc BW, Lavigne L, Reichner J, Gregory SH, Doughty LA, Cioffi WG, Ayala A: Differential effects of macrophage inflammatory chemokine-2 and keratinocyte-derived chemokine on hemorrhage-induced neutrophil priming for lung inflammation: assessment by adoptive cells transfer in mice. Shock 2003, 19:358-365.
61. Quinton LJ, Nelson S, Zhang P, Boe DM, Happel KI, Pan W, Bagby GJ: Selective transport of cytokine-induced neutrophil chemoattractant from the lung to the blood facilitates pulmonary neutrophil recruitment. Am J Physiol Lung Cell Mol Physiol 2004, 286:L465-L472.
62. Aoki K, Ishida Y, Kikuta N, Kawai H, Kuroiwa M, Sato H: Role of CXC chemokines in the enhancement of LPS-induced neutrophil accumulation in the lung of mice by dexamethasone. Biochem Biophys Res Commun 2002, 294:1101-1108.
63. Bless NM, Warner RL, Padgaonkar VA, Lentsch AB, Czermak BJ, Schmal H, Fried HP, Ward PA: Roles for C-X-C chemokines and C5a in lung injury after hindlimb ischemia-reperfusion. Am J Physiol 1999, 276:L57-L63.
64. Greenberger MJ, Strieter RM, Kunkel SL, Danforth JM, Laichalk LL, McGillicuddy DC, Standiford TJ: Neutralization of macrophage inflammatory protein-2 attenuates neutrophil recruitment and bacterial clearance in murine Klebsiella pneumonia. J Infect Dis 1996, 173:159-165.
65. Goncalves AS, Appelberg R: The involvement of the chemokine receptor CXCR2 in neutrophil recruitment in LPS-induced inflammation and in Mycobacterium avium infection. Scand J Immunol 2002, 55:585-591.
66. Belperio JA, Keane MP, Burdick MD, Londhe V, Xue YY, Li K, Phillips RJ, Strieter RM: Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J Clin Invest 2002, 110:1703-1716.
67. Johnson MC, Kajikawa O, Goodman RB, Wong VA, Mongovin SM, Wong WB, Fox-Dewhurst R, Martin TR: Molecular expression of the alpha-chemokine rabbit GRO in Escherichia coli and characterization of its production by lung cells in vitro and in vivo. J Biol Chem 1996, 271:10853-10858.
68. Vanderbilt JN, Mager EM, Allen L, Sawa T, Wiener-Kronish J, Gonzalez R, Dobbs LG: CXC chemokines and their receptors are expressed in type II cells and upregulated following lung injury. Am J Respir Cell Mol Biol 2003, 29:661-668.
69. Nick JA, Young SK, Brown KK, Avdi NJ, Arndt PG, Suratt BT, Janes MS, Henson PM, Worthen GS: Role of p38 mitogen-activated protein kinase in a murine model of pulmonary inflammation. J Immunol 2000, 164:2151-2159.
70. Goodman RB, Strieter RM, Martin DP, Steinberg KP, Milberg JA, Maunder RJ, Kunkel SL, Walz A, Hudson LD, Martin TR: Inflammatory cytokines in patients with persistence of the acute respiratory distress syndrome. Am J Respir Crit Care Med 1996, 154:602-611.
71. Wiedermann FJ, Mayr AJ, Kaneider NC, Fuchs D, Mutz NJ, Schobersberger W: Alveolar granulocyte colony-stimulating factor and alpha-chemokines in relation to serum levels, pulmonary neutrophilia, and severity of lung injury in ARDS. Chest 2004, 125:212-219.
72. Colletti LM, Green M: Lung and liver injury following hepatic ischemia/reperfusion in the rat is increased by exogenous lipopolysaccharide which also increases hepatic TNF production in vivo and in vitro. Shock 2001, 16:312-319.
73. Neumann B, Zantl N, Veihelmann A, Emmanuilidis K, Pfeffer K, Heidecke CD, Holzmann B: Mechanisms of acute inflammatory lung injury induced by abdominal sepsis. Int Immunol 1999, 11:217-227.
74. Chen SC, Mehrad B, Deng JC, Vassileva G, Manfra DJ, Cook DN, Wiekowski MT, Zlotnik A, Standiford TJ, Lira SA: Impaired pulmonary host defense in mice lacking expression of the CXC chemokine lungkine. J Immunol 2001, 166:3362-3368.
75. Miller WS: A study of the factors underlying the formation of alveolar pores in pneumonia. J Exp Med 1923, 38: 07-711.
76. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, Fisher CJ Jr; Recombinant human protein C Worldwide Evaluation in Severe Sepsis (PROWESS) study group: Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 2001, 344:699-709.
77. Welty-Wolf KE, Carraway MS, Ortel TL, Piantadosi CA: Coagulation and inflammation in acute lung injury. Thromb Haemost 2002, 88:17-25.
78. Erlich J, Fearns C, Mathison J, Ulevitch RJ, Mackman N: Lipopolysaccharide induction of tissue factor expression in rabbits. Infect Immun 1999, 67:2540-2546.
79. Coughlin SR: Thrombin signalling and protease-activated receptors. Nature 2000, 407:258-264.
80. Taylor FB, Chang AC, Peer G, Li A, Ezban M, Hedner U: Active site inhibited factor VIIa (DEGR VIIa) attenuates the coagulant and interleukin-6 and -8, but not tumor necrosis factor, responses of the baboon to LD100 Escherichia coli. Blood 1998, 91: 609-1615.
81. Meduri GU, Kohler G, Headley S, Tolley E, Stentz F, Postlethwaite A: Inflammatory cytokines in the BAL of patients with ARDS. Persistent elevation over time predicts poor outcome. Chest 1995, 108:1303-1314.
82. Gando S, Kameue T, Matsuda N, Hayakawa M, Morimoto Y, Ishitani T, Kemmotsu O: Imbalances between the levels of tissue factor and tissue factor pathway inhibitor in ARDS patients. Thromb Res 2003, 109:119-124.
83. Abraham E, Reinhart K, Opal S, Demeyer I, Doig C, Rodriguez AL, Beale R, Svoboda P, Laterre PF, Simon S, Light B, Spapen H, Stone J, Seibert A, Peckelsen C, De Deyne C, Postier R, Pettila V, Artigas A, Percell SR, Shu V, Zwingelstein C, Tobias J, Poole L, Stolzenbach JC, Creasey AA; OPTIMIST Trial Study Group: Efficacy and safety of tifacogin (recombinant tissue factor pathway inhibitor) in severe sepsis: a randomized controlled trial. JAMA 2003, 290:238-247.
84. Hansen CB, Pyke C, Petersen LC, Rao LV: Tissue factor-mediated endocytosis, recycling, and degradation of factor VIIa by a clathrin-independent mechanism not requiring the cytoplasmic domain of tissue factor. Blood 2001, 97:1712-1720.
85. Doshi SN, Marmur JD: Evolving role of tissue factor and its pathway inhibitor. Crit Care Med 2002, Suppl: 241-S250.
86. Ruf W, Riewald M: Tissue factor-dependent coagulation protease signaling in acute lung injury. Crit Care Med 2003, Suppl:S231-S237.
87. Welty-Wolf KE, Carraway MS, Miller DL, Ortel TL, Ezban M, Ghio AJ, Idell S, Piantadosi CA: Coagulation blockade prevents sepsis-induced respiratory and renal failure in baboons. Am J Respir Crit Care Med 2001, 164:1988-1996.
88. Miller DL, Welty-Wolf K, Carraway MS, Ezban M, Ghio A, Suliman H, Piantadosi CA: Extrinsic coagulation blockade attenuates lung injury and proinflammatory cytokine release after intratracheal lipopolysaccharide. Am J Respir Cell Mol Biol 2002, 26: 50-658.
89. Carraway MS, Welty-Wolf KE, Miller DL, Ortel TL, Idell S, Ghio AJ, Petersen LC, Piantadosi CA: Blockade of tissue factor: treatment for organ injury in established sepsis. Am J Respir Crit Care Med 2003, 167:1200-1209.
90. Matthay MA, Zimmerman GA, Esmon C, Bhattacharya J, Coller B, Doerschuk CM, Floros J, Gimbrone MA Jr, Hoffman E, Hubmayr RD, Leppert M, Matalon S, Munford R, Parsons P, Slutsky AS, Tracey KJ, Ward P, Gail DB, Harabin AL: Future research directions in acute lung injury: summary of a National Heart, Lung, and Blood Institute working group. Am J Respir Crit Care Med 2003, 167:1027-1035.
91. Tateda K, Moore TA, Newstead MW, Tsai WC, Zeng X, Deng JC, Chen G, Reddy R, Yamaguchi K, Standiford TJ: Chemokine-dependent neutrophil recruitment in a murine model of Legionella pneumonia: potential role of neutrophils as immunoregulatory cells. Infect Immun 2001, 69:2017-2024.
92. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE, Bagby GJ, Nelson S, Charrier K, Peschon JJ, Kolls JK: Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001, 194:519-527.