Rho kinase signaling pathways during stretch in primary alveolar epithelia

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 10, 2012, Pages

  DiPaolo, Brian C ^a   Margulies, Susan S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Epithelial; Lung injury; Mechanical ventilation; Myosin regulatory light chain; Perijunctional actomyosin ring; RhoA

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BLEBBISTATIN; CALYCULIN A; F ACTIN; MYOSIN LIGHT CHAIN 2; RHO KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ACTINS; AMIDES; ANIMALS; AZEPINES; CARDIAC MYOSINS; CELLS, CULTURED; ENDOTHELIAL CELLS; ENZYME INHIBITORS; EPITHELIAL CELLS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; MALE; MECHANICAL PROCESSES; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; MYOSIN LIGHT CHAINS; NAPHTHALENES; PHOSPHORYLATION; PULMONARY ALVEOLI; PYRIDINES; RATS, SPRAGUE-DAWLEY; RESPIRATION, ARTIFICIAL; RESPIRATORY MUCOSA; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN;

EID: 84861137986     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00175.2011     Document Type: Article

References (96)

1. Albinsson S, Nordstrom I, Hellstrand P. Stretch of the vascular wall induces smooth muscle differentiation by promoting actin polymerization. J Biol Chem 279: 34849-34855, 2004.
2. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271: 20246-20249, 1996.
3. An SS, Fabry B, Mellema M, Bursac P, Gerthoffer WT, Kayyali US, Gaestel M, Shore SA, Fredberg JJ. Role of heat shock protein 27 in cytoskeletal remodeling of the airway smooth muscle cell. J Appl Physiol 96: 1701-1713, 2004.
4. Aspenstrom P. Effectors for the Rho GTPases. Curr Opin Cell Biol 11: 95-102, 1999.
5. Bhadriraju K, Elliott JT, Nguyen M, Plant AL. Quantifying myosin light chain phosphorylation in single adherent cells with automated fluorescence microscopy. BMC Cell Biol 8: 43, 2007.
6. Bhadriraju K, Yang M, Alom Ruiz S, Pirone D, Tan J, Chen CS. Activation of ROCK by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension. Exp Cell Res 313: 3616-3623, 2007.
7. Birukov KG, Birukova AA, Dudek SM, Verin AD, Crow MT, Zhan X, DePaola N, Garcia JG. Shear stress-mediated cytoskeletal remodeling and cortactin translocation in pulmonary endothelial cells. Am J Respir Cell Mol Biol 26: 453-464, 2002.
8. Birukov KG, Jacobson JR, Flores AA, Ye SQ, Birukova AA, Verin AD, Garcia JG. Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am J Physiol Lung Cell Mol Physiol 285: L785-L797, 2003.
9. Birukova AA, Fu P, Xing J, Cokic I, Birukov KG. Lung endothelial barrier protection by iloprost in the 2-hit models of ventilator-induced lung injury (VILI) involves inhibition of Rho signaling. Transl Res 155: 44-54, 2010.
10. Birukova AA, Rios A, Birukov KG. Long-term cyclic stretch controls pulmonary endothelial permeability at translational and post-translational levels. Exp Cell Res 314: 3466-3477, 2008.
11. Birukova AA, Smurova K, Birukov KG, Kaibuchi K, Garcia JG, Verin AD. Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc Res 67: 64-77, 2004.
12. Borok Z, Danto SI, Zabski SM, Crandall ED. Defined medium for primary culture de novo of adult rat alveolar epithelial cells. In Vitro Cell Dev Biol Anim 30A: 99-104, 1994.
13. Bruewer M, Hopkins AM, Hobert ME, Nusrat A, Madara JL. RhoA, Rac1, and Cdc42 exert distinct effects on epithelial barrier via selective structural and biochemical modulation of junctional proteins and F-actin. Am J Physiol Cell Physiol 287: C327-C335, 2004.
14. Bursac P, Fabry B, Trepat X, Lenormand G, Butler JP, Wang N, Fredberg JJ, An SS. Cytoskeleton dynamics: fluctuations within the network. Biochem Biophys Res Commun 355: 324-330, 2007.
15. Bursac P, Lenormand G, Fabry B, Oliver M, Weitz DA, Viasnoff V, Butler JP, Fredberg JJ. Cytoskeletal remodelling and slow dynamics in the living cell. Nat Mater 4: 557-561, 2005.
16. Cavanaugh KJ, Cohen TS, Margulies SS. Stretch increases alveolar epithelial permeability to uncharged micromolecules. Am J Physiol Cell Physiol 290: C1179-C1188, 2006.
17. 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.
18. 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.
19. Cheek JM, Evans MJ, Crandall ED. Type I cell-like morphology in tight alveolar epithelial monolayers. Exp Cell Res 184: 375-387, 1989.
20. Chen X, Pavlish K, Benoit JN. Myosin phosphorylation triggers actin polymerization in vascular smooth muscle. Am J Physiol Heart Circ Physiol 295: H2172-H2177, 2008.
21. Chicurel ME, Chen CS, Ingber DE. Cellular control lies in the balance of forces. Curr Opin Cell Biol 10: 232-239, 1998.
22. Chihara K, Amano M, Nakamura N, Yano T, Shibata M, Tokui T, Ichikawa H, Ikebe R, Ikebe M, Kaibuchi K. Cytoskeletal rearrangements and transcriptional activation of c-fos serum response element by Rho-kinase. J Biol Chem 272: 25121-25127, 1997.
23. Cohen P, Klumpp S, Schelling DL. An improved procedure for identifying and quantitating protein phosphatases in mammalian tissues. FEBS Lett 250: 596-600, 1989.
24. Cohen TS, Cavanaugh KJ, Margulies SS. Frequency and peak stretch magnitude affect alveolar epithelial permeability. Eur Respir J 32: 854-861, 2008.
25. Collins NT, Cummins PM, Colgan OC, Ferguson G, Birney YA, Murphy RP, Meade G, Cahill PA. Cyclic strain-mediated regulation of vascular endothelial occludin and ZO-1: influence on intercellular tight junction assembly and function. Arterioscler Thromb Vasc Biol 26: 62-68, 2006.
26. Craig R, Smith R, Kendrick-Jones J. Light-chain phosphorylation controls the conformation of vertebrate non-muscle and smooth muscle myosin molecules. Nature 302: 436-439, 1983.
27. Danto SI, Zabski SM, Crandall ED. Reactivity of alveolar epithelial cells in primary culture with type I cell monoclonal antibodies. Am J Respir Cell Mol Biol 6: 296-306, 1992.
28. 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.
29. DiPaolo BC, Lenormand G, Fredberg JJ, Margulies SS. Stretch magnitude and frequency-dependent actin cytoskeleton remodeling in alveolar epithelia. Am J Physiol Cell Physiol 299: C345-C353, 2010.
30. Dittmer A, Dittmer J. -Actin is not a reliable loading control in Western blot analysis. Electrophoresis 27: 2844-2845, 2006.
31. Dobbs LG, Gonzalez R, Williams MC. An improved method for isolating type II cells in high yield and purity. Am Rev Respir Dis 134: 141-145, 1986.
32. Eddinger TJ, Meer DP. Myosin II isoforms in smooth muscle: heterogeneity and function. Am J Physiol Cell Physiol 293: C493-C508, 2007.
33. Egan EA. Lung inflation, lung solute permeability, and alveolar edema. J Appl Physiol 53: 121-125, 1982.
34. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273: 29745-29753, 1998.
35. Feng J, Ito M, Ichikawa K, Isaka N, Nishikawa M, Hartshorne DJ, Nakano T. Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J Biol Chem 274: 37385-37390, 1999.
36. Fujiwara K, Pollard TD. Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J Cell Biol 71: 848-875, 1976.
37. Gassmann M, Grenacher B, Rohde B, Vogel J. Quantifying Western blots: pitfalls of densitometry. Electrophoresis 30: 1845-1855, 2009.
38. Grant JW, Taubman MB, Church SL, Johnson RL, Nadal-Ginard B. Mammalian nonsarcomeric myosin regulatory light chains are encoded by two differentially regulated and linked genes. J Cell Biol 111: 1127-1135, 1990.
39. Hecht G, Pestic L, Nikcevic G, Koutsouris A, Tripuraneni J, Lorimer DD, Nowak G, Guerriero V Jr, Elson EL, Lanerolle PD. Expression of the catalytic domain of myosin light chain kinase increases paracellular permeability. Am J Physiol Cell Physiol 271: C1678-C1684, 1996.
40. Ikebe M, Hartshorne DJ. Phosphorylation of smooth muscle myosin at two distinct sites by myosin light chain kinase. J Biol Chem 260: 10027-10031, 1985.
41. Ikebe M, Hartshorne DJ, Elzinga M. Phosphorylation of the 20,000- dalton light chain of smooth muscle myosin by the calcium-activated, phospholipid-dependent protein kinase. Phosphorylation sites and effects of phosphorylation. J Biol Chem 262: 9569-9573, 1987.
42. Ishihara H, Martin BL, Brautigan DL, Karaki H, Ozaki H, Kato Y, Fusetani N, Watabe S, Hashimoto K, Uemura D, et al. Calyculin A and okadaic acid: inhibitors of protein phosphatase activity. Biochem Biophys Res Commun 159: 871-877, 1989.
43. Ishizaki T, Maekawa M, Fujisawa K, Okawa K, Iwamatsu A, Fujita A, Watanabe N, Saito Y, Kakizuka A, Morii N, Narumiya S. The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J 15: 1885-1893, 1996.
44. Jewell EA, Shamraj OI, Lingrel JB. Isoforms of thesubunit of Na,K-ATPase and their significance. Acta Physiol Scand Suppl 607: 161-169, 1992.
45. Kamm KE, Stull JT. Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem 276: 4527-4530, 2001.
46. Kano Y, Katoh K, Masuda M, Fujiwara K. Macromolecular composition of stress fiber-plasma membrane attachment sites in endothelial cells in situ. Circ Res 79: 1000-1006, 1996.
47. Kaunas R, Nguyen P, Usami S, Chien S. Cooperative effects of Rho and mechanical stretch on stress fiber organization. Proc Natl Acad Sci USA 102: 15895-15900, 2005.
48. Kim KJ, Crandall ED. Effects of lung inflation on alveolar epithelial solute and water transport properties. J Appl Physiol 52: 1498-1505, 1982.
49. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273: 245-248, 1996.
50. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137: 481-492, 1997.
51. Kockskamper J, Khafaga M, Grimm M, Elgner A, Walther S, Kockskamper A, von Lewinski D, Post H, Grossmann M, Dorge H, Gottlieb PA, Sachs F, Eschenhagen T, Schondube FA, Pieske B. Angiotensin II and myosin light-chain phosphorylation contribute to the stretch-induced slow force response in human atrial myocardium. Cardiovasc Res 79: 642-651, 2008.
52. Krarup T, Jakobsen LD, Jensen BS, Hoffmann EK. Na -K -2Cl cotransport in Ehrlich cells: regulation by protein phosphatases and kinases. Am J Physiol Cell Physiol 275: C239-C250, 1998.
53. Krishnan R, Park CY, Lin YC, Mead J, Jaspers RT, Trepat X, Lenormand G, Tambe D, Smolensky AV, Knoll AH, Butler JP, Fredberg JJ. Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness. PLos One 4: e5486, 2009.
54. Li Z, Chang Z, Chiao LJ, Kang Y, Xia Q, Zhu C, Fleming JB, Evans DB, Chiao PJ. TrkBT1 induces liver metastasis of pancreatic cancer cells by sequestering Rho GDP dissociation inhibitor and promoting RhoA activation. Cancer Res 69: 7851-7859, 2009.
55. Liebler JM, Borok Z, Li X, Zhou B, Sandoval AJ, Kim KJ, Crandall ED. Alveolar epithelial type I cells express 2-adrenergic receptors and G-protein receptor kinase 2. J Histochem Cytochem 52: 759-767, 2004.
56. Liu WF, Nelson CM, Tan JL, Chen CS. Cadherins, RhoA, and Rac1 are differentially required for stretch-mediated proliferation in endothelial versus smooth muscle cells. Circ Res 101: e44-e52, 2007.
57. Lum H, Podolski JL, Gurnack ME, Schulz IT, Huang F, Holian O. Protein phosphatase 2B inhibitor potentiates endothelial PKC activity and barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 281: L546-L555, 2001.
58. Madara JL. Intestinal absorptive cell tight junctions are linked to cytoskeleton. Am J Physiol Cell Physiol 253: C171-C175, 1987.
59. Madara JL, Pappenheimer JR. Structural basis for physiological regulation of paracellular pathways in intestinal epithelia. J Membr Biol 100: 149-164, 1987.
60. Messer NG, Kendrick-Jones J. Molecular cloning and sequencing of the chicken smooth muscle myosin regulatory light chain. FEBS Lett 234: 49-52, 1988.
61. Mizutani T, Haga H, Koyama Y, Takahashi M, Kawabata K. Diphosphorylation of the myosin regulatory light chain enhances the tension acting on stress fibers in fibroblasts. J Cell Physiol 209: 726-731, 2006.
62. Mizutani T, Kawabata K, Koyama Y, Takahashi M, Haga H. Regulation of cellular contractile force in response to mechanical stretch by diphosphorylation of myosin regulatory light chain via RhoA signaling cascade. Cell Motil Cytoskeleton 66: 389-397, 2009.
63. Mucha DR, Myers CL, Schaeffer RC Jr. Endothelial contraction and monolayer hyperpermeability are regulated by Src kinase. Am J Physiol Heart Circ Physiol 284: H994-H1002, 2003.
64. Nusrat A, Giry M, Turner JR, Colgan SP, Parkos CA, Carnes D, Lemichez E, Boquet P, Madara JL. Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc Natl Acad Sci USA 92: 10629-10633, 1995.
65. Nusrat A, Turner JR, Madara JL. Molecular physiology and patho-physiology of tight junctions. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am J Physiol Gastrointest Liver Physiol 279: G851-G857, 2000.
66. Ohashi K, Nagata K, Maekawa M, Ishizaki T, Narumiya S, Mizuno K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem 275: 3577-3582, 2000.
67. Oswari J, Matthay MA, Margulies SS. Keratinocyte growth factor reduces alveolar epithelial susceptibility to in vitro mechanical deformation. Am J Physiol Lung Cell Mol Physiol 281: L1068-L1077, 2001.
68. Petrache I, Verin AD, Crow MT, Birukova A, Liu F, Garcia JG. Differential effect of MLC kinase in TNF-induced endothelial cell apoptosis and barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 280: L1168-L1178, 2001.
69. Poley RN, Dosier CR, Speich JE, Miner AS, Ratz PH. Stimulated calcium entry and constitutive RhoA kinase activity cause stretch-induced detrusor contraction. Eur J Pharmacol 599: 137-145, 2008.
70. Qiao R, Zhou B, Liebler JM, Li X, Crandall ED, Borok Z. Identification of three genes of known function expressed by alveolar epithelial type I cells. Am J Respir Cell Mol Biol 29: 98-105, 2003.
71. Ridley AJ. Rho family proteins: coordinating cell responses. Trends Cell Biol 11: 471-477, 2001.
72. Riento K, Ridley AJ. Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4: 446-456, 2003.
73. Sahai E, Olson MF, Marshall CJ. Cross-talk between Ras and Rho signalling pathways in transformation favours proliferation and increased motility. EMBO J 20: 755-766, 2001.
74. Satterwhite LL, Lohka MJ, Wilson KL, Scherson TY, Cisek LJ, Corden JL, Pollard TD. Phosphorylation of myosin-II regulatory light chain by cyclin-p34cdc2: a mechanism for the timing of cytokinesis. J Cell Biol 118: 595-605, 1992.
75. Shen L, Black ED, Witkowski ED, Lencer WI, Guerriero V, Schneeberger EE, Turner JR. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci 119: 2095-2106, 2006.
76. Shen L, Turner JR. Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 16: 3919-3936, 2005.
77. Shikata Y, Rios A, Kawkitinarong K, DePaola N, Garcia JG, Birukov KG. Differential effects of shear stress and cyclic stretch on focal adhesion remodeling, site-specific FAK phosphorylation, and small GTPases in human lung endothelial cells. Exp Cell Res 304: 40-49, 2005.
78. Simonovic I, Rosenberg J, Koutsouris A, Hecht G. Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol 2: 305-315, 2000.
79. 2 sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358, 2003.
80. Sumi T, Matsumoto K, Nakamura T. Specific activation of LIM kinase 2 via phosphorylation of threonine 505 by ROCK, a Rho-dependent protein kinase. J Biol Chem 276: 670-676, 2001.
81. Sun X, Shikata Y, Wang L, Ohmori K, Watanabe N, Wada J, Shikata K, Birukov KG, Makino H, Jacobson JR, Dudek SM, Garcia JG. Enhanced interaction between focal adhesion and adherens junction proteins: involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement. Microvasc Res 77: 304-313, 2009.
82. Sweadner KJ. Isozymes of the Na /K -ATPase. Biochim Biophys Acta 988: 185-220, 1989.
83. Totsukawa G, Yamakita Y, Yamashiro S, Hartshorne DJ, Sasaki Y, Matsumura F. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J Cell Biol 150: 797-806, 2000.
84. Trepat X, Deng L, An SS, Navajas D, Tschumperlin DJ, Gerthoffer WT, Butler JP, Fredberg JJ. Universal physical responses to stretch in the living cell. Nature 447: 592-595, 2007.
85. Tschumperlin DJ, Margulies SS. Equibiaxial deformation-induced injury of alveolar epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol 275: L1173-L1183, 1998.
86. 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.
87. Turner JR. "Putting the squeeze" on the tight junction: understanding cytoskeletal regulation. Semin Cell Dev Biol 11: 301-308, 2000.
88. Turner JR, Angle JM, Black ED, Joyal JL, Sacks DB, Madara JL. PKC-dependent regulation of transepithelial resistance: roles of MLC and MLC kinase. Am J Physiol Cell Physiol 277: C554-C562, 1999.
89. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am J Physiol Cell Physiol 273: C1378-C1385, 1997.
90. Walsh SV, Hopkins AM, Chen J, Narumiya S, Parkos CA, Nusrat A. Rho kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology 121: 566-579, 2001.
91. Wang JH, Goldschmidt-Clermont P, Wille J, Yin FC. Specificity of endothelial cell reorientation in response to cyclic mechanical stretching. J Biomech 34: 1563-1572, 2001.
92. Waters CM, Ridge KM, Sunio G, Venetsanou K, Sznajder JI. Mechanical stretching of alveolar epithelial cells increases Na -K -ATPase activity. J Appl Physiol 87: 715-721, 1999.
93. White GE, Gimbrone MA Jr, Fujiwara K. Factors influencing the expression of stress fibers in vascular endothelial cells in situ. J Cell Biol 97: 416-424, 1983.
94. Yanase M, Ikeda H, Ogata I, Matsui A, Noiri E, Tomiya T, Arai M, Inoue Y, Tejima K, Nagashima K, Nishikawa T, Shibata M, Ikebe M, Rojkind M, Fujiwara K. Functional diversity between Rho-kinase- and MLCK-mediated cytoskeletal actions in a myofibroblast-like hepatic stellate cell line. Biochem Biophys Res Commun 305: 223-228, 2003.
95. Zar H. Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall, 1999.
96. Zhang M, Rao PV. Blebbistatin, a novel inhibitor of myosin II ATPase activity, increases aqueous humor outflow facility in perfused enucleated porcine eyes. Invest Ophthalmol Vis Sci 46: 4130-4138, 2005.