Mechanical stretch decreases migration of alveolar epithelial cells through mechanisms involving Rac1 and Tiam1

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 295, Issue 5, 2008, Pages

  Desai, Leena P ^a   Chapman, Kenneth E ^a   Waters, Christopher M ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Cyclic strain; GTP Rac1; Guanine nucleotide exchange factor; Mechanotransduction

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN TIAM1; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; LUNG ALVEOLUS EPITHELIUM; MECHANICAL STIMULATION; NONHUMAN; POSITIVE END EXPIRATORY PRESSURE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; WOUND CLOSURE;

ANIMALS; CELL MEMBRANE; CELL MOVEMENT; CYTOSOL; DOWN-REGULATION; ENZYME ACTIVATION; EPITHELIAL CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MALE; NEOPLASM PROTEINS; PROTEIN TRANSPORT; PSEUDOPODIA; PULMONARY ALVEOLI; RAC1 GTP-BINDING PROTEIN; RATS; RATS, SPRAGUE-DAWLEY; STRESS, MECHANICAL;

EID: 57049153613     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.90218.2008     Document Type: Article

References (67)

1. 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. N Engl J Med 342: 1301-1308, 2000.
2. Atabai K, Ishigaki M, Geiser T, Ueki I, Matthay MA, Ware LB. Keratinocyte growth factor can enhance alveolar epithelial repair by nonmitogenic mechanisms. Am J Physiol Lung Cell Mol Physiol 283: L163-L169, 2002.
3. Cavanaugh KJ Jr, Margulies SS. Measurement of stretch-induced loss of alveolar epithelial barrier integrity with a novel in vitro method. Am J Physiol Cell Physiol 283: C1801-C1808, 2002.
4. Cavanaugh KJ Jr, Oswari J, Margulies SS. Role of stretch on tight junction structure in alveolar epithelial cells. Am J Respir Cell Mol Biol 25: 584-591, 2001.
5. Cerione RA, Zheng Y. The Dbl family of oncogenes. Curr Opin Cell Biol 8: 216-222, 1996.
6. Chapman KE, Sinclair SE, Zhuang D, Hassid A, Desai LP, Waters CM. Cyclic mechanical strain increases reactive oxygen species production in pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 289: L834-L841, 2005.
7. Chaturvedi LS, Marsh HM, Shang X, Zheng Y, Basson MD. Repetitive deformation activates focal adhesion kinase and ERK mitogenic signals in human Caco-2 intestinal epithelial cells through Src and Rac1. J Biol Chem 282: 14-28, 2007.
8. Cheng KC, Zhang H, Lin CY, Slutsky AS. Ventilation with negative airway pressure induces a cytokine response in isolated mouse lung. Anesth Analg 94: 1577-1582, 2002.
9. Connolly BA, Rice J, Feig LA, Buchsbaum RJ. Tiam1-IRSp53 complex formation directs specificity of rac-mediated actin cytoskeleton regulation. Mol Cell Biol 25: 4602-4614, 2005.
10. Corbridge TC, Wood LD, Crawford GP, Chudoba MJ, Yanos J, Sznajder JI. Adverse effects of large tidal volume and low PEEP in canine acid aspiration. Am Rev Respir Dis 142: 311-315, 1990.
11. Cox EA, Sastry SK, Huttenlocher A. Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol Biol Cell 12: 265-277, 2001.
12. Desai LP, Aryal AM, Ceacareanu B, Hassid A, Waters CM. RhoA and Rac1 are both required for efficient wound closure of airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 287: L1134-L1144, 2004.
13. Desai LP, Sinclair SE, Chapman KE, Hassid A, Waters CM. High tidal volume mechanical ventilation with hyperoxia alters alveolar type II cell adhesion. Am J Physiol Lung Cell Mol Physiol 293: L769-L778, 2007.
14. Dobbs LG. Isolation and culture of alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 258: L134-L147, 1990.
15. Dreyfuss D, Saumon G. Role of tidal volume, FRC, and end-inspiratory volume in the development of pulmonary edema following mechanical ventilation. Am Rev Respir Dis 148: 1194-1203, 1993.
16. Dreyfuss D, Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 157: 294-323, 1998.
17. Frank JA, Gutierrez JA, Jones KD, Allen L, Dobbs L, Matthay MA. Low tidal volume reduces epithelial and endothelial injury in acid-injured rat lungs. Am J Respir Crit Care Med 165: 242-249, 2002.
18. Gajic O, Lee J, Doerr CH, Berrios JC, Myers JL, Hubmayr RD. Ventilator-induced cell wounding and repair in the intact Lung. Am J Respir Crit Care Med 167: 1057-1063, 2003.
19. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 101: 7618-7623, 2004.
20. Garat C, Kheradmand F, Albertine KH, Folkesson HG, Matthay MA. Soluble and insoluble fibronectin increases alveolar epithelial wound healing in vitro. Am J Physiol Lung Cell Mol Physiol 271: L844-L853, 1996.
21. Gattinoni L, Caironi P, Carlesso E. How to ventilate patients with acute lung injury and acute respiratory distress syndrome. Curr Opin Crit Care 11: 69-76, 2005.
22. Geiser T, Jarreau PH, Atabai K, Matthay MA. Interleukin-1β augments in vitro alveolar epithelial repair. Am J Physiol Lung Cell Mol Physiol 279: L1184-L1190, 2000.
23. Habets GG, Scholtes EH, Zuydgeest D, van der Kammen RA, Stam JC, Berns A, Collard JG. Identification of an invasion-inducing gene, Tiam-1, that encodes a protein with homology to GDP-GTP exchangers for Rho-like proteins. Cell 77: 537-549, 1994.
24. Hall A. Rho GTPases and the actin cytoskeleton. Science 279: 509-514, 1998.
25. Hamelers IH, Olivo C, Mertens AE, Pegtel DM, van der Kammen RA, Sonnenberg A, Collard JG. The Rac activator Tiam1 is required for (alpha)3(beta)1-mediated laminin-5 deposition, cell spreading, and cell migration. J Cell Biol 171: 871-881, 2005.
26. Hordijk PL, ten Klooster JP, van der Kammen RA, Michiels F, Oomen LC, Collard JG. Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 278: 1464-1466, 1997.
27. Huh D, Fujioka H, Tung YC, Futai N, Paine R 3rd, Grotberg JB, Takayama S. Acoustically detectable cellular-level lung injury induced by fluid mechanical stresses in microfluidic airway systems. Proc Natl Acad Sci USA 104: 18886-18891, 2007.
28. Jafari B, Ouyang B, Li LF, Hales CA, Quinn DA. Intracellular glutathione in stretch-induced cytokine release from alveolar type-2 like cells. Respirology 9: 43-53, 2004.
29. Katsumi A, Milanini J, Kiosses WB, del Pozo MA, Kaunas R, Chien S, Hahn KM, Schwartz MA. Effects of cell tension on the small GTPase Rac. J Cell Biol 158: 153-164, 2002.
30. Kawamura S, Miyamoto S, Brown JH. Initiation and transduction of stretch-induced RhoA and Rac1 activation through caveolae: cytoskeletal regulation of ERK translocation. J Biol Chem 278: 31111-31117, 2003.
31. Kay SS, Bilek AM, Dee KC, Gaver DP 3rd. Pressure gradient, not exposure duration, determines the extent of epithelial cell damage in a model of pulmonary airway reopening. J Appl Physiol 97: 269-276, 2004.
32. Kheradmand F, Folkesson HG, Shum L, Derynk R, Pytela R, Matthay MA. Transforming growth factor-α enhances alveolar epithelial cell repair in a new in vitro model. Am J Physiol Lung Cell Mol Physiol 267: L728-L738, 1994.
33. Kraemer A, Goodwin M, Verma S, Yap AS, Ali RG. Rac is a dominant regulator of cadherin-directed actin assembly that is activated by adhesive ligation independently of Tiam1. Am J Physiol Cell Physiol 292: C1061-C1069, 2007.
34. Kumar A, Murphy R, Robinson P, Wei L, Boriek AM. Cyclic mechanical strain inhibits skeletal myogenesis through activation of focal adhesion kinase, Rac-1 GTPase, and NF-kappaB transcription factor. FASEB J 18: 1524-1535, 2004.
35. Lee SH, Kunz J, Lin SH, Yu-Lee LY. 16-kDa prolactin inhibits endothelial cell migration by down-regulating the Ras-Tiam1-Rac1-Pak1 signaling pathway. Cancer Res 67: 11045-11053, 2007.
36. Malhotra A. Low-tidal-volume ventilation in the acute respiratory distress syndrome. N Engl J Med 357: 1113-1120, 2007.
37. Malliri A, van Es S, Huveneers S, Collard JG. The Rac exchange factor Tiam1 is required for the establishment and maintenance of cadherin-based adhesions. J Biol Chem 279: 30092-30098, 2004.
38. Matthay MA, Zimmerman GA. Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogenesis and rational management. Am J Respir Cell Mol Biol 33: 319-327, 2005.
39. Mendez JL, Hubmayr RD. New insights into the pathology of acute respiratory failure. Curr Opin Crit Care 11: 29-36, 2005.
40. Michiels F, Habets GG, Stam JC, van der Kammen RA, Collard JG. A role for Rac in Tiam1-induced membrane ruffling and invasion. Nature 375: 338-340, 1995.
41. Minard ME, Ellis LM, Gallick GE. Tiam1 regulates cell adhesion, migration and apoptosis in colon tumor cells. Clin Exp Metastasis 23: 301-313, 2006.
42. Minard ME, Kim LS, Price JE, Gallick GE. The role of the guanine nucleotide exchange factor Tiam1 in cellular migration, invasion, adhesion and tumor progression. Breast Cancer Res 84: 21-32, 2004.
43. Moissoglu K, Slepchenko BM, Meller N, Horwitz AF, Schwartz MA. In vivo dynamics of Rac-membrane interactions. Mol Biol Cell 17: 2770-2779, 2006.
44. Muscedere JG, Mullen JB, Gan K, Slutsky AS. Tidal ventilation at low airway pressures can augment lung injury. Am J Respir Crit Care Med 149: 1327-1334, 1994.
45. Osada T, Watanabe S, Tanaka H, Hirose M, Miyazaki A, Sato N. Effect of mechanical strain on gastric cellular migration and proliferation during mucosal healing: role of Rho dependent and Rac dependent cytoskeletal reorganisation. Gut 45: 508-515, 1999.
46. Pelham RJ Jr, Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94: 13661-13665, 1997.
47. Perkins GD, Nathani N, McAuley DF, Gao F, Thickett DR. In vitro and in vivo effects of salbutamol on neutrophil function in acute lung injury. Thorax 62: 36-42, 2007.
48. Perlman CE, Bhattacharya J. Alveolar expansion imaged by optical sectioning microscopy. J Appl Physiol 103: 1037-1044, 2007.
49. Price LS, Leng J, Schwartz MA, Bokoch GM. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol Biol Cell 9: 1863-1871, 1998.
50. Ray RM, Vaidya RJ, Johnson LR. MEK/ERK regulates adherens junctions and migration through Rac1. Cell Motil Cytoskeleton 64: 143-156, 2007.
51. Roberts JR, Perkins GD, Fujisawa T, Pettigrew KA, Gao F, Ahmed A, Thickett DR. Vascular endothelial growth factor promotes physical wound repair and is anti-apoptotic in primary distal lung epithelial and A549 cells. Crit Care Med 35: 2164-2170, 2007.
52. Samuelsen JT, Schwarze PE, Huitfeldt HS, Thrane EV, Lag M, Refsnes M, Skarpen E, Becher R. Regulation of rat alveolar type 2 cell proliferation in vitro involves type II cAMP-dependent protein kinase. Am J Physiol Lung Cell Mol Physiol 292: L232-L239, 2007.
53. Savla U, Waters CM. Mechanical strain inhibits repair of airway epithelium in vitro. Am J Physiol Lung Cell Mol Physiol 274: L883-L892, 1998.
54. Schmidt A, Hall A. The Rho exchange factor Net1 is regulated by nuclear sequestration. J Biol Chem 277: 14581-14588, 2002.
55. Schwartz MA, Shattil SJ. Signaling networks linking integrins and rho family GTPases. Trends Biochem Sci 25: 388-391, 2000.
56. Sinclair SE, Molthen RC, Haworth ST, Dawson CA, Waters CM. Airway strain during mechanical ventilation in an intact animal model. Am J Respir Crit Care Med 176: 786-794, 2007.
57. Steinberg J, Schiller HJ, Halter JM, Gatto LA, Dasilva M, Amato M, McCann UG, Nieman GF. Tidal volume increases do not affect alveolar mechanics in normal lung but cause alveolar overdistension and exacerbate alveolar instability after surfactant deactivation. Crit Care Med 30: 2675-2683, 2002.
58. Suh GY, Koh Y, Chung MP, An CH, Kim H, Jang WY, Han J, Kwon OJ. Repeated derecruitments accentuate lung injury during mechanical ventilation. Crit Care Med 30: 1848-1853, 2002.
59. Taskar V, John J, Evander E, Robertson B, Jonson B. Surfactant dysfunction makes lungs vulnerable to repetitive collapse and reexpansion. Am J Respir Crit Care Med 155: 313-320, 1997.
60. Ten Klooster JP, Evers EE, Janssen L, Machesky LM, Michiels F, Hordijk P, Collard JG. Interaction between Tiam1 and the Arp2/3 complex links activation of Rac to actin polymerization. Biochem J 397: 39-45, 2006.
61. Tschumperlin DJ, Oswari J, Margulies AS. Deformation-induced injury of alveolar epithelial cells. Effect of frequency, duration, and amplitude. Am J Respir Crit Care Med 162: 357-362, 2000.
62. Van Aelst L, D'Souza-Schorey C. Rho GTPases and signaling networks. Genes Dev 11: 2295-2322, 1997.
63. Vlahakis NE, Schroeder MA, Pagano RE, Hubmayr RD. Deformation-induced lipid trafficking in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 280: L938-L946, 2001.
64. Vlahakis NE, Schroeder MA, Pagano RE, Hubmayr RD. Role of deformation-induced lipid trafficking in the prevention of plasma membrane stress failure. Am J Respir Crit Care Med 166: 1282-1289, 2002.
65. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349, 2000.
66. Yamauchi J, Miyamoto Y, Tanoue A, Shooter EM, Chan JR. Ras activation of a Rac1 exchange factor, Tiam1, mediates neurotrophin-3-induced Schwann cell migration. Proc Natl Acad Sci USA 102: 14889-14894, 2005.
67. Zheng Y. Dbl family guanine nucleotide exchange factors. Trends Biochem Sci 26: 724-732, 2001.