Respiratory epithelial cells regulate lung inflammation in response to inhaled endotoxin

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 287, Issue 1 31-1, 2004, Pages

  Skerrett, Shawn J ^a,b   Liggitt, H Denny ^a   Hajjar, Adeline M ^a   Ernst, Robert K ^a   Miller, Samuel I ^a   Wilson, Christopher B ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cytokines; Lipopolysaccharide; Nuclear factor B; Transgenic mice

Indexed keywords

APOPROTEIN; CYTOKINE; DOMINANT NEGATIVE I KAPPA B; ENDOTOXIN; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 2; SURFACTANT PROTEIN C; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALVEOLAR BONE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHIOLE; BRONCHUS MUCOSA; CELL NUCLEUS; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; INFLAMMATION; INHALATION; INTRACELLULAR TRANSPORT; KILLER CELL; LUNG HOMOGENATE; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN TRANSPORT; RESPIRATORY EPITHELIUM; TRANSGENE; TRANSGENIC MOUSE;

ADMINISTRATION, INHALATION; ANIMALS; BRONCHI; BRONCHITIS; CELL LINE; CYTOKINES; GENES, DOMINANT; HUMANS; I-KAPPA B PROTEINS; INTERLEUKIN-8; LIPOPOLYSACCHARIDES; LUNG; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NF-KAPPA B; PEROXIDASE; PNEUMONIA; PROMOTER REGIONS (GENETICS); PULMONARY ALVEOLI; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; RESPIRATORY MUCOSA;

EID: 2942755996     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00030.2004     Document Type: Article

References (62)

1. Aderem A and Ulevitch R.J. Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787, 2000.
2. Akira S. Mammalian Toll-like receptors. Curr Opin Immunol 15: 5-11, 2003.
3. Alcamo E, Mizgerd JP, Horwitz BH, Bronson R, Beg AA, Scott M, Doerschuk CM, Hynes RO, and Baltimore D. Targeted mutation of of TNF receptor I rescues the RelA-deficient mouse and reveals a critical role for NF-κB in leukocyte recruitment. J Immunol 167: 1592-1600, 2001.
4. Beck-Schimmer B, Madjdpour C, Kneller S, Ziegler U, Pasch T, Wuthrich RP, Ward PA, and Schimmer RC. Role of alveolar epithelial ICAM-1 in lipopolysaccharide-induced lung inflammation. Eur Respir J 19: 1142-1150, 2002.
5. Beck-Schimmer B, Schimmer RC, Warner RL, Schmal H, Nordblom G, Flory CM, Lesch ME, Friedl HP, Schrier DJ, and Ward PA. Expression of lung vascular and airway ICAM-1 after exposure to bacterial lipopolysaccharide. Am J Respir Cell Mol Biol 17: 344-352, 1997.
6. Becker MN, Diamond G, Verghese MW, and Randell SH. CD14-dependent lipopolysaccharide-induced β-defensin-2 expression in human tracheobronchial epithelium. J Biol Chem 275: 29731-29736, 2000.
7. Berg JT, Lee ST, Thepen T, Lee CY, and Tsan MF. Depletion of alveolar macrophages by liposome-encapsulated dichloromethylene diphosphonate. J Appl Physiol 74: 2812-2819, 1993.
8. Blackwell TS, Lancaster LH, Blackwell TR, Venkatakrishnan A, and Christman JW. Differential NF-κB activation after intratracheal endotoxin. Am J Physiol Lung Cell Mol Physiol 277: L823-L830, 1999.
9. Burns AR, Takei F, and Doerschuk CM. Quantitation of ICAM-1 expression in mouse lung during pneumonia. J Immunol 153: 3189-3198, 1994.
10. 2 (CD11/CD18) integrin-independent neutrophil recruitment to endotoxin-induced lung inflammation. J Immunol 166: 4644-4649, 2001.
11. Chen SC, Mehrad B, Deng JC, Vassileva G, Manfra DJ, Cook DN, Wiekowski MT, Zlotnik A, Standiford TJ, and Lira SA. Impaired pulmonary host defense in mice lacking expression of the CXC chemokine lungkine. J Immunol 166: 3362-3368, 2001.
12. Cooper P, Potter S, Mueck B, Yousefi S, and Jarai G. Identification of genes induced by inflammatory cytokines in airway epithelium. Am J Physiol Lung Cell Mol Physiol 280: L841-L852, 2001.
13. Cromwell O, Hamid Q, Corrigan CJ, Barkans J, Meng Q, Collins PD, and Kay AB. Expression and generation of interleukin-8, IL-6 and granulocyte-macrophage colony-stimulating factor by bronchial epithelial cells and enhancement by IL-1β and tumour necrosis factor-α. Immunol. 77: 330-337, 1992.
14. Darveau RP and Hancock RE. Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains. J Bacteriol 155: 831-838, 1983.
15. Diamond G, Legarda D, and Ryan LK. The innate immune response of the respiratory epithelium. Immunol Rev 173: 27-38, 2000.
16. DiDonato J, Mercurio F, Rosette C, Wu-Li J, Suyang H, Ghosh S, and Karin M. Mapping of the inducible IκB phosphorylation sites that signal its ubiquitination and degradation. Mol Cell Biol 16: 1295-1304, 1996.
17. DiMango E, Zar HJ, Bryan R, and Prince A. Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J Clin Invest 96: 2204-2210, 1995.
18. Doerschuk CM, Winn RK, Coxson HO, and Harlan JM. CD18-dependent and -independent mechanisms of neutrophil emigration in the pulmonary and systemic microcirculation of rabbits. J Immunol 144: 2327-2333, 1990.
19. Ernst RK, Yi EC, Guo L, Lim KB, Burns JL, Hackett M, and Miller SI. Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286: 1561-1565, 1999.
20. Frevert CW, Huang S, Danaee H, Paulauskis JD, and Kobzik L. Functional characterization of the rat chemokine KC and its importance in neutrophil recruitment in a rat model of pulmonary inflammation. J Immunol 154: 335-344, 1995.
21. Hajjar AM, Ernst RK, Tsai JH, Wilson CB, and Miller SI. Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat Immun 3: 354-359, 2002.
22. Hubbard AK, Timblin CR, Shukla A, Rincon M, and Mossman BT. Activation of NF-κB-dependent gene expression by silica in lungs of luciferase reporter mice. Am J Physiol Lung Cell Mol Physiol 282: L968-L975, 2002.
23. Khair OA, Devalia JL, Abdelaziz MM, Sapsford RJ, Tarraf H, and Davies RJ. Effect of Haemophilus influenzae endotoxin on the synthesis of IL-6, IL-8. TNF-α and expression of ICAM-1 in cultured Iranian bronchial epithelial cells. Eur Respir J 7: 2109-2116, 1994.
24. Koay MA, Gao X, Washington MK, Parman KS, Sadikot RT, Blackwell TS, and Christman JW. Macrophages are necessary for maximal nuclear factor-κB activation in response to endotoxin. Am J Respir Cell Mol Biol 26: 572-578, 2002.
25. Korfhagen TR, Glasser SW, Wert SE, Bruno MD, Daugherty CC, McNeish JD, Stock JL, Potter SS, and Whitsett JA. Cis-acting sequences from a human surfactant protein gene confer pulmonary-specific gene expression in transgenic mice. Proc Natl Acad Sci USA 87: 6122-6126, 1990.
26. Koyama S, Rennard SI, Leikauf GD, Shoji S, Von Essen S, Claassen L, and Robbins RA. Endotoxin stimulates bronchial epithelial cells to release chemotactic factors for neutrophils. A potential mechanism for neutrophil recruitment, cytotoxicity, and inhibition of proliferation in bronchial inflammation. J Immunol 147: 4293-4301, 1991.
27. Koyama S, Sato E, Nomura H, Kubo K, Miura M, Yamashita T, Nagai S, and Izumi T. The potential of various lipopolysaccharides to release IL-8 and G-CSF. Am J Physiol Lung Cell Mol Physiol 278: L658-L666, 2000.
28. Kumasaka T, Quinlan WM, Doyle NA, Condon TP, Sligh I, Takei F, Beaudet AL, Bennett CF, and Doerschuk CM. Role of the intercellular adhesion molecule-1 (ICAM-1) in endotoxin-induced pneumonia evaluated using ICAM-1 antisense oligonucleotides, anti-ICAM-1 monoclonal antibodies, and ICAM-1 mutant mice. J Clin Invest 97: 2362-2369, 1996.
29. Kwon OJ, Au BT, Collins PD, Adeoek IM, Mak JC, Robbins RR, Chung KF, and Barnes PJ. Tumor necrosis factor-induced interleukin-8 expression in cultured human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 267: L398-L405, 1994.
30. Li Q and Verma IM. NF-κB regulation in the immune system. Nat Rev Immunol 2: 725-734, 2002.
31. Li XC, Miyasaka M, and Issekutz TB. Blood monocyte migration to acute lung inflammation involves both CD11/CD18 and very late activation antigen-4-dependent and independent pathways. J Immunol 161: 6258-6264, 1998.
32. Lieber A, He CY, Meuse L, Himeda C, Wilson C, and Kay MA, Inhibition of NF-κB activation in combination with bcl-2 expression allows for persistence of first-generation adenovirus vectors in the mouse liver. J Virol 72: 9267-9277, 1998.
33. Lieber M, Smith B, Szakal A, Nelson-Rees W, and Todaro G. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int J Cancer 17: 62-70, 1976.
34. Lorenz E,Jones M, Wohlford-Lenane C, Meyer N, Frees KL, Arbour NC, and Schwartz DA. Genes other than TLR4 are involved in the response to inhaled LPS. Am J Physiol Lung Cell Mol Physiol 281: L1106-L1114, 2001.
35. Martin TR. Recognition of bacterial endotoxin in the lungs. Am J Respir Cell Mol Biol 23: 128-132, 2000.
36. Martin TR, Mathison JC, Tobias P, Letureq DJ, Moriarty AM, Maunder R.J. and Ulevitch R.J. Lipopolysaccharide binding protein enhances the responsiveness of alveolar macrophages to bacterial lipopolysaccharide. Implications for cytokine production in normal and injured lungs. J Clin Invest 90: 2209-2219, 1992.
37. Massion PP, Inoue H, Richman-Eisenstat J, Grunberger D, Jorens PG, Housset B, Pittet JF, Wiener-Kronish JP, and Nadel JA. Novel Pseudomonas product stimulates interleukin-8 production in airway epithelial cells in vitro. J Clin Invest 93: 26-32, 1994.
38. McCormack FX and Whitsett JA. The pulmonary collectins. SP-A and SP-D, orchestrate innate immunity in the lung. J Clin Invest 109: 707-712, 2002.
39. Mizgerd JP. Molecular mechanisms of neutrophil recruitment elicited by bacteria in the lungs. Semin Immunol 14: 123-132, 2002.
40. Mizgerd JP, Scott ML, Spieker MR, and Doerschuk CM. Functions of IκB proteins in inflammatory responses to Escherichia coli LPS in mouse lungs. Am J Respir Cell Mol Biol 27: 575-582, 2002.
41. Nakamura H, Yoshimura K, Jaffe HA, and Crystal RG. Interleukin-8 gene expression in human bronchial epithelial cells. J Biol Chem 266: 19611-19617, 1991.
42. Paine R III, Rolfe MW, Standiford TJ, Burdick MD, Rollins BJ, and Strieter RM. MCP-1 expression by rat type II alveolar epithelial cells in primary culture. J Immunol 150: 4561-4570, 1993.
43. Peralta FM and Casale TB. Orientation and presence of epithelium are key to endotoxin-induced neutrophil migration. Eur Respir J 11: 1053-1059, 1998.
44. Poynter ME, Irvin CG, and Janssen-Heininger YM. A prominent role for airway epithelial NF-κB activation in lipopolysaccharide-induced airway inflammation. J Immunol 170: 6257-6265, 2003.
45. Pugin J, Schurer-Maly CC, Letureq D, Moriarty A, Ulevitch RJ, and Tohias PS. Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc Natl Acad Sci USA 90: 2744-2748, 1993.
46. Ridger VC, Wagner BE, Wallace WA, and Hellewell PG. Differential effects of CD18, CD29, and CD49 integrin subunit inhibition on neutrophil migration in pulmonary inflammation. J Immunol 166: 3484-3490, 2001.
47. Rose F, Guthmann B, Tenenhaum T, Fink L, Ghofrani A, Weissmann N, Konig P, Ermert L, Dahlem G, Haenze J, Kummer W, Seeger W, and Grimminger F. Apical, but not basolateral, endotoxin preincubation protects alveolar epithelial cells against hydrogen peroxide-induced loss of barrier function: the role of nitric oxide synthesis. J Immunol 169: 1474-1481, 2002.
48. Sadikot RT, Han W, Everhart MB, Zoia O, Peebles RS, Jansen ED, Yull FE, Christman JW, and Blackwell TS. Selective IκB kinase expression in airway epithelium generates neutrophilic lung inflammation. J Immunol 170: 1091-1098, 2003.
49. Sadikot RT, Jansen ED, Blackwell TR, Zoia O, Yull F, Christman JW, and Blackwell TS. High-dose dexamethasone accentuates nuclear factor-κB activation in endotoxin-treated mice. Am J Respir Crit Care Med 164: 873-878, 2001.
50. Schmal H, Shanley TP, Jones ML, Friedl and Ward PA. Role for macrophage inflammatory protein-2 in lipopolysaccharide-induced lung injury in rats. J Immunol 156: 1963-1972, 1996.
51. Schulz C, Farkas L, Wolf K, Kratzel K, Eissner G, and Pfeifer M. Differences in LPS-induced activation of bronchial epithelial cells (BEAS-2B) and type II-like pneumocytes (A-549). Scand J Immunol 56: 294-302, 2002.
52. Skerrett SJ, Martin TR, Chi EY, Peschon JJ, Mohler KM, and Wilson CB. Role of the type I TNF receptor in lung inflammation after inhalation of endotoxin of Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol 276: L715-L727, 1999.
53. Smart SJ and Casale TB. Pulmonary epithelial cells facilitate TNF-α-induced neutrophil chemotaxis. A role for cytokine networking. J Immunol 152: 4087-4094, 1994.
54. Smith S, Liggitt D, Jeromsky E, Tan X, Skerrett SJ, and Wilson CB. Local role for tumor necrosis factor α in the pulmonary inflammatory response to Mycobacterium tuberculosis infection. Infect Immun 70: 2082-2089, 2002.
55. Smith S, Skerrett SJ, Chi EY, Jonas M, Mohler K, and Wilson CB. The locus of tumor necrosis factor-α action in lung inflammation. Am J Respir Cell Mol Biol 19: 881-891, 1998.
56. Standiford TJ, Kunkel SL, Basha MA, Chensue SW, Lynch JP III, Toews GB, Westwick J, and Strieter RM. Interleukin-8 gene expression by a pulmonary epithelial cell line. A model for cytokine networks in the lung. J Clin Invest 86: 1945-1953, 1990.
57. Strieter RM, Belperio JA, and Keane MP. Cytokines in innate host defense in the lung. J Clin Invest 109: 699-705, 2002.
58. Stripp BR, Sawaya PL, Luse DS, Wikenheiser KA, Wert SE, Huffman JA, Lattier DL, Singh G, Katyal SL, and Whitsett JA. Cis-acting elements that confer lung epithelial cell expression of the CC10 gene. J Biol Chem 267: 14703-14712, 1992.
59. Tsai WC, Strieter RM, Wilkowski JM, Bueknell KA, Burdiek MD, Lira SA, and Standiford TJ. Lung-specific transgenic expression of KC enhances resistance to Klebsiella pneumoniae in mice. J Immunol 161: 2435-2440, 1998.
60. Tsutsumi-Ishii Y and Nagaoka I. Modulation of human β-defensin-2 transcription in pulmonary epithelial cells by lipopolysaccharide-stimulated mononuclear phagocytes via proinflammatory cytokine production. J Immunol 170: 4226-4236, 2003.
61. Wang X, Moser C, Louboutin JP, Lysenko ES, Weiner DJ, Weiser JN, and Wilson JM. Toll-like receptor 4 mediates innate immune responses to Haemophilus influenzae infection in mouse lung. J Immunol 168: 810-815, 2002.
62. Wert SE, Glasser SW, Korfhagen TR, and Whitsett JA. Transcriptional elements from the human SP-C gene direct expression in the primordial respiratory epithelium of transgenic mice. Dev Biol 156: 426-443, 1993.