Fibrinogen binding to ICAM-1 promotes EGFR-dependent mucin production in human airway epithelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 297, Issue 1, 2009, Pages

  Kim, Suil ^a,b   Nadel, Jay A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell differentiation; Cell surface molecules; Innate immunity; Mucous hypersecretion

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRINOGEN; FIBRINOGEN (117-133) PEPTIDE; INTERCELLULAR ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1 (8-22) PEPTIDE; INTERCELLULAR ADHESION MOLECULE 1 ANTIBODY; METALLOPROTEINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUCIN; NEUTRALIZING ANTIBODY; PEPTIDE DERIVATIVE; PHOSPHOLIPASE C INHIBITOR; PHOSPHOTYROSINE; PROTEIN KINASE C ALPHA INHIBITOR; PROTEIN KINASE C BETA INHIBITOR; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RESPIRATORY EPITHELIUM;

ANTIBODIES; CELL LINE, TUMOR; ENZYME ACTIVATION; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBRINOGEN; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LUNG; METALLOPROTEASES; MODELS, BIOLOGICAL; MUCINS; NEUTRALIZATION TESTS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN KINASE C; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; TYPE C PHOSPHOLIPASES;

EID: 67650088184     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00032.2009     Document Type: Article

References (70)

1. Agazie YM, Hayman MJ. Molecular mechanism for a role of SHP2 in epidermal growth factor receptor signaling. Mol Cell Biol 23: 7875-7886, 2003.
2. Avadhanula V, Rodriguez CA, Ulett GC, Bakaletz LO, Adderson EE. Nontypeable Haemophilus influenzae adheres to intercellular adhesion molecule 1 (ICAM-1) on respiratory epithelial cells and upregulates ICAM-1 expression. Infect Immun 74: 830-838, 2006.
3. Baselga J, Mendelsohn J, Kim YM, Pandiella A. Autocrine regulation of membrane transforming growth factor-alpha cleavage. J Biol Chem 271: 3279-3284, 1996.
4. Bentley AM, Durham SR, Robinson DS, Menz G, Storz C, Cromwell O, Kay AB, Wardlaw AJ. Expression of endothelial and leukocyte adhesion molecules intercellular adhesion molecule-1, E-selectin, and vascular cell adhesion molecule-1 in the bronchial mucosa in steady-state and allergen-induced asthma. J Allergy Clin Immunol 92: 857-868, 1993.
5. Bianco A, Sethi SK, Allen JT, Knight RA, Spiteri MA. Th2 cytokines exert a dominant influence on epithelial cell expression of the major group human rhinovirus receptor, ICAM-1. Eur Respir J 12: 619-626, 1998.
6. Bloemen PG, van den Tweel MC, Henricks PA, Engels F, Wagenaar SS, Rutten AA, Nijkamp FP. Expression and modulation of adhesion molecules on human bronchial epithelial cells. Am J Respir Cell Mol Biol 9: 586-593, 1993.
7. Böhmer FD, Böhmer A, Obermeier A, Ullrich A. Use of selective tyrosine kinase blockers to monitor growth factor receptor dephosphorylation in intact cells. Anal Biochem 228: 267-273, 1995.
8. Burgel PR, Lazarus SC, Tam DC, Ueki IF, Atabai K, Birch M, Nadel JA. Human eosinophils induce mucin production in airway epithelial cells via epidermal growth factor receptor activation. J Immunol 167: 5948-5954, 2001.
9. Burgel PR, Montani D, Danel C, Dusser DJ, Nadel JA. A morphometric study of mucins and small airway plugging in cystic fibrosis. Thorax 62: 153-161, 2007.
10. Champagne B, Tremblay P, Cantin A, St Pierre Y. Proteolytic cleavage of ICAM-1 by human neutrophil elastase. J Immunol 161: 6398-6405, 1998.
11. Chen P, Xie H, Wells A. Mitogenic signaling from the egf receptor is attenuated by a phospholipase C-gamma/protein kinase C feedback mechanism. Mol Biol Cell 7: 871-881, 1996.
12. Chirathaworn C, Kohlmeier JE, Tibbetts SA, Rumsey LM, Chan MA, Benedict SH. Stimulation through intercellular adhesion molecule-1 provides a second signal for T cell activation. J Immunol 168: 5530-5537, 2002.
13. Chokki M, Yamamura S, Eguchi H, Masegi T, Horiuchi H, Tanabe H, Kamimura T, Yasuoka S. Human airway trypsin-like protease increases mucin gene expression in airway epithelial cells. Am J Respir Cell Mol Biol 30: 470-478, 2004.
14. Cook SJ, McCormick F. Inhibition by cAMP of Ras-dependent activation of Raf. Science 262: 1069-1072, 1993.
15. D'Souza SE, Byers-Ward VJ, Gardiner EE, Wang H, Sung SS. Identification of an active sequence within the first immunoglobulin domain of intercellular cell adhesion molecule-1 (ICAM-1) that interacts with fibrinogen. J Biol Chem 271: 24270-24277, 1996.
16. Davies JR, Hovenberg HW, Linden CJ, Howard R, Richardson PS, Sheehan JK, Carlstedt I. Mucins in airway secretions from healthy and chronic bronchitic subjects. Biochem J 313: 431-439, 1996.
17. Di Stefano A, Maestrelli P, Roggeri A, Turato G, Calabro S, Potena A, Mapp CE, Ciaccia A, Covacev L, Fabbri LM. Upregulation of adhesion molecules in the bronchial mucosa of subjects with chronic obstructive bronchitis. Am J Respir Crit Care Med 149: 803-810, 1994.
18. Erjefalt JS, Korsgren M, Nilsson MC, Sundler F, Persson CG. Association between inflammation and epithelial damage-restitution processes in allergic airways in vivo. Clin Exp Allergy 27: 1344-1355, 1997.
19. Fan H, Derynck R. Ectodomain shedding of TGF-alpha and other transmembrane proteins is induced by receptor tyrosine kinase activation and MAP kinase signaling cascades. EMBO J 18: 6962-6972, 1999.
20. Fiore E, Fusco C, Romero P, Stamenkovic I. Matrix metalloproteinase 9 (MMP-9/gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cell-mediated cytotoxicity. Oncogene 21: 5213-5223, 2002.
21. Gaglia JL, Greenfield EA, Mattoo A, Sharpe AH, Freeman GJ, Kuchroo VK. Intercellular adhesion molecule 1 is critical for activation of CD28-deficient T cells. J Immunol 165: 6091-6098, 2000.
22. Gardiner EE, D'Souza SE. Sequences within fibrinogen and intercellular adhesion molecule-1 (ICAM-1) modulate signals required for mitogenesis. J Biol Chem 274: 11930-11936, 1999.
23. Groneberg DA, Eynott PR, Lim S, Oates T, Wu R, Carlstedt I, Roberts P, McCann B, Nicholson AG, Harrison BD, Chung KF. Expression of respiratory mucins in fatal status asthmaticus and mild asthma. Histopathology 40: 367-373, 2002.
24. Groneberg DA, Eynott PR, Oates T, Lim S, Wu R, Carlstedt I, Nicholson AG, Chung KF. Expression of MUC5AC and MUC5B mucins in normal and cystic fibrosis lung. Respir Med 96: 81-86, 2002.
25. Haidaris PJ. Induction of fibrinogen biosynthesis and secretion from cultured pulmonary epithelial cells. Blood 89: 873-882, 1997.
26. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, Pare PD. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 350: 2645-2653, 2004.
27. Hubeau C, Lorenzato M, Couetil JP, Hubert D, Dusser D, Puchelle E, Gaillard D. Quantitative analysis of inflammatory cells infiltrating the cystic fibrosis airway mucosa. Clin Exp Immunol 124: 69-76, 2001.
28. Kim S, Schein AJ, Nadel JA. E-cadherin promotes EGFR-mediated cell differentiation and MUC5AC mucin expression in cultured human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 289: L1049-L1060, 2005.
29. Kohri K, Ueki IF, Nadel JA. Neutrophil elastase induces mucin production by ligand-dependent epidermal growth factor receptor activation. Am J Physiol Lung Cell Mol Physiol 283: L531-L540, 2002.
30. Kuyper LM, Pare PD, Hogg JC, Lambert RK, Ionescu D, Woods R, Bai TR. Characterization of airway plugging in fatal asthma. Am J Med 115: 6-11, 2003.
31. Laprise P, Langlois MJ, Boucher MJ, Jobin C, Rivard N. Down-regulation of MEK/ERK signaling by E-cadherin-dependent PI3K/Akt pathway in differentiating intestinal epithelial cells. J Cell Physiol 199: 32-39, 2004.
32. Lemjabbar H, Basbaum C. Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells. Nat Med 8: 41-46, 2002.
33. Li Y, Bharti A, Chen D, Gong J, Kufe D. Interaction of glycogen synthase kinase 3beta with the DF3/MUC1 carcinoma-associated antigen and beta-catenin. Mol Cell Biol 18: 7216-7224, 1998.
34. Lominadze D, Tsakadze N, Sen U, Falcone JC, D'Souza SE. Fibrinogen and fragment D-induced vascular constriction. Am J Physiol Heart Circ Physiol 288: H1257-H1264, 2005.
35. Look DC, Rapp SR, Keller BT, Holtzman MJ. Selective induction of intercellular adhesion molecule-1 by interferon-gamma in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 263: L79-L87, 1992.
36. Marlin SD, Springer TA. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell 51: 813-819, 1987.
37. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179-185, 1995.
38. McCourt PA, Ek B, Forsberg N, Gustafson S. Intercellular adhesion molecule-1 is a cell surface receptor for hyaluronan. J Biol Chem 269: 30081-30084, 1994.
39. Moghal N, Neel BG. Integration of growth factor, extracellular matrix, and retinoid signals during bronchial epithelial cell differentiation. Mol Cell Biol 18: 6666-6678, 1998.
40. Montero JC, Yuste L, Diaz-Rodriguez E, Esparis-Ogando A, Pandiella A. Mitogen-activated protein kinase-dependent and -independent routes control shedding of transmembrane growth factors through multiple secretases. Biochem J 363: 211-221, 2002.
41. Nadel JA. Innate immune mucin production via epithelial cell surface signaling: relationship to allergic disease. Curr Opin Allergy Clin Immunol 7: 57-62, 2007.
42. Neff SB, Z'Graggen BR, Neff TA, Jamnicki-Abegg M, Suter D, Schimmer RC, Booy C, Joch H, Pasch T, Ward PA, Beck-Schimmer B. Inflammatory response of tracheobronchial epithelial cells to endotoxin. Am J Physiol Lung Cell Mol Physiol 290: L86-L96, 2006.
43. Pandey P, Kharbanda S, Kufe D. Association of the DF3/MUC1 breast cancer antigen with Grb2 and the Sos/Ras exchange protein. Cancer Res 55: 4000-4003, 1995.
44. Pece S, Chiariello M, Murga C, Gutkind JS. Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J Biol Chem 274: 19347-19351, 1999.
45. Pizzichini E, Pizzichini MM, Efthimiadis A, Evans S, Morris MM, Squillace D, Gleich GJ, Dolovich J, Hargreave FE. Indices of airway inflammation in induced sputum: reproducibility and validity of cell and fluid-phase measurements. Am J Respir Crit Care Med 154: 308-317, 1996.
46. Pluskota E, Chen Y, D'Souza SE. Src homology domain 2-containing tyrosine phosphatase 2 associates with intercellular adhesion molecule 1 to regulate cell survival. J Biol Chem 275: 30029-30036, 2000.
47. Pluskota E, D'Souza SE. Fibrinogen interactions with ICAM-1 (CD54) regulate endothelial cell survival. Eur J Biochem 267: 4693-4704, 2000.
48. Polosa R, Prosperini G, Leir SH, Holgate ST, Lackie PM, Davies DE. Expression of c-erbB receptors and ligands in human bronchial mucosa. Am J Respir Cell Mol Biol 20: 914-923, 1999.
49. Regimbald LH, Pilarski LM, Longenecker BM, Reddish MA, Zimmermann G, Hugh JC. The breast mucin MUCI as a novel adhesion ligand for endothelial intercellular adhesion molecule 1 in breast cancer. Cancer Res 56: 4244-4249, 1996.
50. Roovers K, Assoian RK. Integrating the MAP kinase signal into the G1 phase cell cycle machinery. Bioessays 22: 818-826, 2000.
51. Schachtrup C, Lu P, Jones LL, Lee JK, Lu J, Sachs BD, Zheng B, Akassoglou K. Fibrinogen inhibits neurite outgrowth via beta3 integrin-mediated phosphorylation of the EGF receptor. Proc Natl Acad Sci USA 104: 11814-11819, 2007.
52. Schroeder JA, Thompson MC, Gardner MM, Gendler SJ. Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J Biol Chem 276: 13057-13064, 2001.
53. Seeger W, Elssner A, Gunther A, Kramer HJ, Kalinowski HO. Lung surfactant phospholipids associate with polymerizing fibrin: loss of surface activity. Am J Respir Cell Mol Biol 9: 213-220, 1993.
54. Shao MX, Nadel JA. Dual oxidase 1-dependent MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci USA 102: 767-772, 2005.
55. Shao MX, Nakanaga T, Nadel JA. Cigarette smoke induces MUC5AC mucin overproduction via tumor necrosis factor-alpha-converting enzyme in human airway epithelial (NCI-H292) cells. Am J Physiol Lung Cell Mol Physiol 287: L420-L427, 2004.
56. Shao MX, Ueki IF, Nadel JA. Tumor necrosis factor alpha-converting enzyme mediates MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci USA 100: 11618-11623, 2003.
57. Simpson-Haidaris PJ, Courtney MA, Wright TW, Goss R, Harmsen A, Gigliotti F. Induction of fibrinogen expression in the lung epithelium during Pneumocystis carinii pneumonia. Infect Immun 66: 4431-4439, 1998.
58. Sorby M, Ostman A. Protein-tyrosine phosphatase-mediated decrease of epidermal growth factor and platelet-derived growth factor receptor tyrosine phosphorylation in high cell density cultures. J Biol Chem 271: 10963-10966, 1996.
59. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314, 1994.
60. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56: 849-853, 1989.
61. Sunnarborg SW, Hinkle CL, Stevenson M, Russell WE, Raska CS, Peschon JJ, Castner BJ, Gerhart MJ, Paxton RJ, Black RA, Lee DC. Tumor necrosis factor-alpha converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J Biol Chem 277: 12838-12845, 2002.
62. Takeyama K, Dabbagh K, Lee HM, Agusti C, Lausier JA, Ueki IF, Grattan KM, Nadel JA. Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci USA 96: 3081-3086, 1999.
63. Togashi Y, Yamaki K, Sakai T, Watanabe-Kobayashi M, Mue S, Ohuchi K. Analysis of the expression of intercellular adhesion molecule-1 in cells of the human bronchial epithelial cell line NCI-H292. Eur J Pharmacol 345: 199-206, 1998.
64. Tomashefski JF Jr, Abramowsky CR, Chung-Park M, Wisniewska J, Bruce MC. Immunofluorescence studies of lung tissue in cystic fibrosis. Pediatr Pathol 12: 313-324, 1992.
65. Tosi MF, Stark JM, Smith CW, Hamedani A, Gruenert DC, Infeld MD. Induction of ICAM-1 expression on human airway epithelial cells by inflammatory cytokines: effects on neutrophil-epithelial cell adhesion. Am J Respir Cell Mol Biol 7: 214-221, 1992.
66. Tsakadze NL, Sithu SD, Sen U, English WR, Murphy G, D'Souza SE. Tumor necrosis factor-alpha-converting enzyme (TACE/ADAM-17) mediates the ectodomain cleavage of intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 281: 3157-3164, 2006.
67. Wagers SS, Norton RJ, Rinaldi LM, Bates JH, Sobel BE, Irvin CG. Extravascular fibrin, plasminogen activator, plasminogen activator inhibitors, and airway hyperresponsiveness. J Clin Invest 114: 104-111, 2004.
68. Wang Q, Pfeiffer GR 2nd, Gaarde WA. Activation of SRC tyrosine kinases in response to ICAM-1 ligation in pulmonary microvascular endothelial cells. J Biol Chem 278: 47731-47743, 2003.
69. Woods D, Parry D, Cherwinski H, Bosch E, Lees E, McMahon M. Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol Cell Biol 17: 5598-5611, 1997.
70. Wu J, Dent P, Jelinek T, Wolfman A, Weber MJ, Sturgill TW. Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3,5-monophosphate. Science 262: 1065-1069, 1993.