Stress-activated protein kinases mediate cell migration in human airway epithelial cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 32, Issue 4, 2005, Pages 301-310

  White, Steven R ^a   Tse, Roberta ^a   Marroquin, Bertha A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Airway epithelium; c Jun N terminal protein kinase; Migration; Mitogen activated protein kinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; COLLAGEN TYPE 4; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE;

ABRASION; ARTICLE; CELL CULTURE; CELL DAMAGE; CELL LINE; CELL MIGRATION; CELL REGENERATION; CELL SPREADING; CELL STRESS; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LUNG ALVEOLUS EPITHELIUM; PROTEIN PHOSPHORYLATION; RESPIRATORY TRACT MUCOSA; STRESS; WOUND; WOUND CLOSURE; WOUND HEALING;

CELL LINE; CELL MOVEMENT; CELLS, CULTURED; ENZYME ACTIVATION; ENZYME INHIBITORS; EPITHELIAL CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RESPIRATORY SYSTEM; WOUND HEALING;

EID: 16444367966     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2004-0118OC     Document Type: Article

References (60)

1. Laitinen LA, Heino M, Laitinen A, Kava T, Haahtela T. Damage of the airway epithelium and bronchial reactivity in patients with asthma. Am Rev Respir Dis 1985;131:599-606.
2. Beasley R, Roche WR, Roberts JA, Holgate ST. Cellular events in the bronchi in mild asthma and after bronchial provocation. Am Rev Respir Dis 1989;139:806-817.
3. Erjefält JS, Erjefält I, Sundler F, Persson CGA. In vivo restitution of airway epithelium. Cell Tissue Res 1995;281:305-316.
4. Erjefält J, Persson C, Sundler F. Epithelial barrier formation by airway basal cells. Thorax 1997;52:213-217.
5. Keenan K, Combs JW, McDowell EM. Regeneration of hamster tracheal epithelium after mechanical injury: II. Multifocal lesions: stathmokinetic and autoradiographic studies of cell proliferation. Virchows Arch [Cell Pathol] 1982;41:215-229.
6. Keenan K, Combs JW, McDowell EM. Regeneration of hamster tracheal epithelium after mechanical injury: III. Large and small lesions: comparative stathmokinetic and single pulse and continuous thymidine labeling autoradiographic studies. Virchows Arch [Cell Pathol] 1982;41:231-252.
7. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-1745.
8. Jeffery PK, Wardlaw AJ, Nelson FC, Collins JV, Kay AB. Bronchial biopsies in asthma - an ultrastructural, quantitative study and correlation with hyperreactivity. Am Rev Respir Dis 1989;140:1745-1753.
9. Vignola AM, Chanez P, Campbell AM, Fouques F, Lebel B, Enander I, Bousquet J. Airway inflammation in mild intermittent and in persistent asthma. Am J Respir Crit Care Med 1998;157:403-409.
10. Vuong H, Patterson T, Adiseshaiah P, Shapiro P, Kalvakolanu DV, Reddy SP. JNK1 and AP-1 regulate PMA-inducible squamous differentiation marker expression in Clara-like H441 cells. Am J Physiol 2002;282:L215-L225.
11. Witt O, Schulze S, Kanbach K, Roth C, Pekrun A. Tumor cell differentiation by butyrate and environmental stress. Cancer Lett 2001;171:173-182.
12. Gerthoffer WT, Yamboliev I, Shearer M, Pohl J, Haynes R, Dang S, Sato K, Sellers JR. Activation of MAP kinases and phosphorylation of caldesmon in colonic smooth muscle. J Physiol (Lond) 1996;495:597-609.
13. Lee JC, Young PR. Role of CSB/p38/RK stress response kinase in LPS and cytokine signaling mechanisms. J Leukoc Biol 1996;59:152-157.
14. Hedges JC, Dechert MA, Yamboliev I, Martin JL, Hickey E, Weber LA, Gerthoffer WT. p38 mitogen-activated protein kinase mediates cell migration in smooth muscle cells. J Biol Chem 1999;274:24211-24219.
15. Okada Y, Saika S, Hashizume N, Kobata S, Yamanaka O, Ohnishi Y, Senba E. Expression of fos family and jun family protooncogenes during corneal epithelial wound healing. Curr Eye Res 1996;15:824-832.
16. Malliri A, Symons M, Hennigan RF, Huristone AFL, Lamb RF, Wheeler T, Ozanne BW. The transcription factor AP-1 is required for EGF-induced activation of Rho-like GTPases, cytoskeletal rearrangements, motility, and in vitro invasion of A431 cells. J Cell Biol 1998;143:1087-1099.
17. Ioroi T, Yamamori M, Yagi K, Hirai M, Zhan Y, Kim S, Iwao H. Dominant negative c-Jun inhibits platelet-derived growth factor directed migration by vascular smooth muscle cells. J Pharmacol Sci 2003;91:145-148.
18. Yates S, Rayner TE. Transcription factor activation in response to cutaneous injury: role of AP-1 in reepithelialization. Wound Repair Regen 2002;10:5-15.
19. Holgate ST, Davies DE, Lackie PM, Wilson SJ, Puddicombe SM, Lordan JL. Epithelial-mesenchymal interactions in the pathogenesis of asthma. J Allergy Clin Immunol 2000;105:193-204.
20. Abe MK, Chao TS, Solway J, Rosner MR, Hershenson MB. Hydrogen peroxide stimulates mitogen-activated protein kinase in bovine tracheal myocytes: implications for human airway disease. Am J Respir Cell Mol Biol 1994;11:577-585.
21. Page K, Li J, Hershenson MB. p38 MAP kinase negatively regulates cyclin D1 expression in airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2001;280:L955-L964.
22. Gruenert DC, Finkbeiner WE, Widdicombe JH. Culture and transformation of human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 1995;268:L347-L360.
23. Dorscheid DR, Conforti A, Hamann KJ, Rabe KF, White SR. Characterization of cell surface lectin-binding patterns of human airway epithelium. Histochem J 1999;31:145-151.
24. Sanghavi J, Rabe KF, Kim JS, Magnusson H, Leff AR, White SR Sr. Migration of human and guinea pig airway epithelial cells in response to calcitonin gene-related peptide. Am J Respir Cell Mol Biol 1994;11:181-187.
25. Kim JS, McKinnis VS, Nawrocki A, White SR. Stimulation of migration and wound repair of guinea pig airway epithelial cells in response to epidermal growth factor. Am J Respir Cell Mol Biol 1998;18:66-74.
26. Dorscheid DR, Wojcik KR, Sun S, Marroquin BA, White SR. Apoptosis of airway epithelial cells induced by corticosteroids. Am J Respir Crit Care Med 2001;164:1939-1947.
27. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 1995;364:229-233.
28. Saklatvala J, Rawlinson L, Waller RJ, Sarsfield S, Lee JC, Morton LF, Barnes MJ, Farndale RW. Role for p38 mitogen-activated protein kinase in platelet aggregation caused by collagen or a thromboxane analogue. J Biol Chem 1996;271:6586-6589.
29. White SR, Dorscheid DR, Rabe KF, Wojcik K, Hamann KJ. Regulation of epithelial monolayer wound repair by extracel lular matrix and integrin interactions. Am J Respir Cell Mol Biol 1999;20:787-796.
30. Singh-Kaw P, Zarnegar R, Siegfried JM. Stimulatory effects of hepatocyte growth factor on normal and neoplastic human bronchial epithelial cells. Am J Physiol 1995;268:L1012-L1020.
31. Zahm JM, Debordeaux C, Raby B, Klossek JM, Bonnet N, Puchelle E. Motogenic effect of recombinant HGF on airway epithelial cells during the in vitro wound repair of the respiratory epithelium. J Cell Physiol 2000;185:447-453.
32. Yu R, Mandlekar S, Lei W, Fahl WE, Tan TH, Kong AT. p38 mitogen-activated protein kinase negatively regulates the induction of phase II drug-metabolizing enzymes that detoxify carcinogens. J Biol Chem 2000;275:2322-2327.
33. Han Z, Boyle DL, Chang L, Bennett B, Karin M, Yang L, Manning AM, Firestein GS. c-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J Clin Invest 2001;108:73-81.
34. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 2001;98:13681-13686.
35. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci USA 1995;92:7686-7689.
36. Duncia JV, Santella JB III, Higley CA, Pitts WJ, Wityak J, Frietze WE, Rankin FW, Sun JH, Earl RA, Tabaka AC, et al. MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg Med Chem Lett 1998;8:2839-2844.
37. Ciocca DR, Oesterreich S, Chamness GC, McGuire WL, Fuqua SA. Biological and clinical implications of heat shock protein 27,000 (Hsp27): a review. J Natl Cancer Inst 1993;85:1558-1570.
38. Landry J, Huot J. Modulation of actin dynamics during stress and physiological stimulation by a signaling pathway involving p38 MAP kinase and heat-shock protein 27. Biochem Cell Biol 1995;73:703-707.
39. Piotrowicz RS, Levin EG. Basolateral membrane-associated 27-kDa heat shock protein and microfilament polymerization. J Biol Chem 1997;272:25920- 25927.
40. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 1995;15:505-516.
41. Lavoie JN, Hickey E, Weber LA, Landry J. Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 1993;268:24210-24214.
42. Piotrowicz RS, Hickey E, Levin EG. Heat shock protein 27 kDa expression and phosphorylation regulates endothelial cell migration. FASEB J 1998:12:1481-1490.
43. Rust W, Kingsley K, Petnicki T, Padmanabhan S, Carper SW, Plopper GE. Heat shock protein 27 plays two distinct roles in controlling human breast cancer cell migration on laminin-5. Mol Cell Biol Res Commun 1999;1:196-202.
44. Boehme SA, Sullivan SK, Crowe PD, Santos M, Conlon PJ, Sriramarao P, Bacon KB. Activation of mitogen-activated protein kinase regulates eotaxin-induced eosinophil migration. J Immunol 1999;163:1611-1618.
45. Graf K, Xi XP, Yang D, Fleck E, Hsueh WA, Law RE. Mitogen-activated protein kinase activation is involved in platelet-derived growth factor-directed migration by vascular smooth muscle cells. Hypertension 1997;29:334-339.
46. Kavurma MM, Khachigian LM. ERK, JNK, and p38 MAP kinases differentially regulate proliferation and migration of phenotypically distinct smooth muscle cell subtypes. J Cell Biochem 2003;89:289-300.
47. Huang C, Rajfur Z, Berchers C, Schaller MD, Jacobson K. JNK phosphorylates paxillin and regulates cell migration. Nature 2003;424:219-223.
48. Li J, Molkentin JD, Colbert MC. 2001. Retinoic acid inhibits cardiac neural crest migration by blocking c-Jun N-terminal kinase activation. Devel. Biol. 232:351-361.
49. Marin V, Farnarier C, Grés S, Kaplanski S, Su MS-S, Dinarello CA, Kaplanski G. The p38 mitogen-activated protein kinase pathway plays a critical role in thrombin-induced endothelial chemokine production and leukocyte recruitment. Blood 2001;98:667-673.
50. Rousseau S, Houle F, Landry J, Huot J. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 1997;15:2169-2177.
51. Raingeaud J, Gupta S, Rogers JS, Dickens H, Han J, Ulevitch RJ, Davis RJ. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem 1995;270:7420-7426.
52. Zervos AS, Faccio L, Gatto JP, Kyriakis JM, Brent R. Mxi2, a mitogen-activated protein kinase that recognizes and phosphorylates Max protein. Proc Natl Acad Sci USA 1995;92:10531-10534.
53. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Lla-mazares A, Zamanillo D, Hunt T, Nebreda AR. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 1994;78:1027-1037.
54. Huot J, Houle F, Spitz DR, Landry J. HSP27 phosphorylation-mediated resistance against actin fragmentation and cell death induced by oxidative stress. Cancer Res 1996;56:273-279.
55. Hedges JC, Dechert MA, Yamboliev IA, Martin JL, Hickey E, Weber LA, Gerthoffer WT. A role for p38(MAPK)/HSP27 pathway in smooth muscle cell migration. J Biol Chem 1999;274:24211-24219.
56. Hai T, Curran T. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci USA 1991;88:3720-3724.
57. Dignass AU, Tsunekawa S, Podolsky DK. Fibroblast growth factors modulate intestinal epithelial cell growth and migration. Gastroenterology 1994;106:1254-1262.
58. Dieckgraefe BK, Weems DM, Santoro SA, Alpers DH. ERK and p38 MAP kinase are mediators of intestinal epithelial wound-induced signal transduction. Biochem Biophys Res Commun 1997;233:389-394.
59. Derijard B, Hibi M, Wu IH, Barrett T, Su B, Deng T, Karin M, Davis RJ. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 1994;76:1025-1037.
60. Kito H, Chen EL, Wang X, Ikeda M, Azuma N, Nakajima N, Gahtan V, Sumpio BE. Role of mitogen-activated protein kinases in pulmonary endothelial cells exposed to cyclic strain. J Appl Physiol 2000;89:2391-2400.