Hyperosmotic stress regulates the distribution and stability of myocardin-related transcription factor, a key modulator of the cytoskeleton

American Journal of Physiology - Cell Physiology

Volumn 304, Issue 2, 2013, Pages

  Ly, Donald L ^a   Waheed, Faiza ^a   Lodyga, Monika ^a   Speight, Pam ^a   Masszi, András ^a   Nakano, Hiroyasu ^b   Hersom, Maria ^a,c   Pedersen, Stine F ^c   Szászi, Katalin ^a   Kapus, András ^a  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cell volume; GEF H1; Hypertonicity; Osmoprotection; RhoA

Indexed keywords

CIS ACTING ELEMENT; CIS ACTING ELEMENT CARG BOX; GEF H1; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOCARDIN; MYOCARDIN RELATED TRANSCRIPTION FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL DEATH; CELL NUCLEUS; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; HYPEROSMOTIC STRESS; KIDNEY TUBULE CELL; MEDIATOR; MYOFIBROBLAST; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APOPTOSIS; CELL LINE; CYTOSKELETON; GENE EXPRESSION REGULATION; GENE SILENCING; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HYPERTONIC SOLUTIONS; KIDNEY TUBULES; MAP KINASE SIGNALING SYSTEM; NUCLEAR PROTEINS; OSMOTIC PRESSURE; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; RHO-ASSOCIATED KINASES; STRESS, PHYSIOLOGICAL; SWINE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 84872408839     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00290.2012     Document Type: Article

References (76)

1. Aijaz S, D'Atri F, Citi S, Balda MS, Matter K. Binding of GEF-H1 to the tight junction-associated adaptor cingulin results in inhibition of Rho signaling and G1/S phase transition. Dev Cell 8: 777-786, 2005.
2. Arthur WT, Petch LA, Burridge K. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr Biol 10: 719-722, 2000.
3. Badid C, Desmouliere A, McGregor B, Costa AM, Fouque D, Hadj Aissa A, Laville M. Interstitial alpha-smooth muscle actin: a prognostic marker in membranous nephropathy. Clin Nephrol 52: 210-217, 1999.
4. Benais-Pont G, Punn A, Flores-Maldonado C, Eckert J, Raposo G, Fleming TP, Cereijido M, Balda MS, Matter K. Identification of a tight junction-associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability. J Cell Biol 160: 729-740, 2003.
5. Bertolotto C, Ricci JE, Luciano F, Mari B, Chambard JC, Auberger P. Cleavage of the serum response factor during death receptor-induced apoptosis results in an inhibition of the c-FOS promoter transcriptional activity. J Biol Chem 275: 12941-12947, 2000.
6. Birukova AA, Fu P, Xing J, Yakubov B, Cokic I, Birukov KG. Mechanotransduction by GEF-H1 as a novel mechanism of ventilatorinduced vascular endothelial permeability. Am J Physiol Lung Cell Mol Physiol 298: L837-L848, 2010.
7. Buchwalter G, Gross C, Wasylyk B. Ets ternary complex transcription factors. Gene 324: 1-14, 2004.
8. Burg MB, Ferraris JD. Salt, skeletons, and suicide. Focus on "Hyperosmotic stress regulates the distribution and stability of myocardin-related transcription factor, a key modulator of the cytoskeleton. Am J Physiol Cell Physiol (October 24, 2012). doi:10.1152/ajpcell.00319.2012.
9. Burg MB, Ferraris JD, Dmitrieva NI. Cellular response to hyperosmotic stresses. Physiol Rev 87: 1441-1474, 2007.
10. Busche S, Descot A, Julien S, Genth H, Posern G. Epithelial cell-cell contacts regulate SRF-mediated transcription via Rac-actin-MAL signalling. J Cell Sci 121: 1025-1035, 2008.
11. Callow MG, Zozulya S, Gishizky ML, Jallal B, Smeal T. PAK4 mediates morphological changes through the regulation of GEF-H1. J Cell Sci 118: 1861-1872, 2005.
12. Cantore M, Reinehr R, Sommerfeld A, Becker M, Haussinger D. TheSrc family kinase Fyn mediates hyperosmolarity-induced Mrp2 and Bsep retrieval from canalicular membrane. J Biol Chem 286: 45014-45029, 2011.
13. Chang YC, Nalbant P, Birkenfeld J, Chang ZF, Bokoch GM. GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell 19: 2147-2153, 2008.
14. Chapman HA. Epithelial-mesenchymal interactions in pulmonary fibrosis. Annu Rev Physiol 73: 413-435, 2011.
15. Charbonney E, Speight P, Masszi A, Nakano H, Kapus A. Beta-cateninand Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblast transition. Mol Biol Cell 22: 4472-4485, 2011.
16. - cotransporter? Am J Physiol Cell Physiol 289: C68-C81, 2005.
17. Di Ciano-Oliveira C, Sirokmany G, Szaszi K, Arthur WT, Masszi A, Peterson M, Rotstein OD, Kapus A. Hyperosmotic stress activates Rho: differential involvement in Rho kinase-dependent MLC phosphorylation and NKCC activation. Am J Physiol Cell Physiol 285: C555-C566, 2003.
18. Di Ciano-Oliveira C, Thirone AC, Szaszi K, Kapus A. Osmotic stress and the cytoskeleton: the R(h)ole of Rho GTPases. Acta Physiol (Oxf) 187: 257-272, 2006.
19. Di Ciano C, Nie Z, Szaszi K, Lewis A, Uruno T, Zhan X, Rotstein OD, Mak A, Kapus A. Osmotic stress-induced remodeling of the cortical cytoskeleton. Am J Physiol Cell Physiol 283: C850-C865, 2002.
20. Drewett V, Devitt A, Saxton J, Portman N, Greaney P, Cheong NE, Alnemri TF, Alnemri E, Shaw PE. Serum response factor cleavage by caspases 3 and 7 linked to apoptosis in human BJAB cells. J Biol Chem 276: 33444-33451, 2001.
21. Evelyn CR, Wade SM, Wang Q, Wu M, Iniguez-Lluhi JA, Merajver SD, Neubig RR. CCG-1423: a small-molecule inhibitor of RhoA transcriptional signaling. Mol Cancer Ther 6: 2249-2260, 2007.
22. Fan L, Sebe A, Peterfi Z, Masszi A, Thirone AC, Rotstein OD, Nakano H, McCulloch CA, Szaszi K, Mucsi I, Kapus A. Cell contact-dependent regulation of epithelial-myofibroblast transition via the rho-rho kinasephospho-myosin pathway. Mol Biol Cell 18: 1083-1097, 2007.
23. Fujishiro SH, Tanimura S, Mure S, Kashimoto Y, Watanabe K, Kohno M. ERK1/2 phosphorylate GEF-H1 to enhance its guanine nucleotide exchange activity toward RhoA. Biochem Biophys Res Commun 368: 162-167, 2008.
24. Garcia-Mata R, Wennerberg K, Arthur WT, Noren NK, Ellerbroek SM, Burridge K. Analysis of activated GAPs and GEFs in cell lysates. Methods Enzymol 406: 425-437, 2006.
25. Gorbatenko A, Wiwel M, Klingberg H, Nielsen AB, Kapus A, Pedersen SF. Hyperosmotic stress strongly potentiates serum response factor (SRF)-dependent transcriptional activity in Ehrlich Lettre Ascites cells through a mechanism involving p38 mitogen-activated protein kinase. J Cell Physiol 226: 2857-2868, 2011.
26. Guilluy C, Swaminathan V, Garcia-Mata R, O'Brien ET, Superfine R, Burridge K. The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat Cell Biol 13: 722-727, 2011.
27. Hallows KR, Packman CH, Knauf PA. Acute cell volume changes in anisotonic media affect F-actin content of HL-60 cells. Am J Physiol Cell Physiol 261: C1154-C1161, 1991.
28. Heck JN, Ponik SM, Garcia-Mendoza MG, Pehlke CA, Inman DR, Eliceiri KW, Keely PJ. Microtubules regulate GEF-H1 in response to extracellular matrix stiffness. Mol Biol Cell 23: 2583-2592, 2012.
29. Heidenreich O, Neininger A, Schratt G, Zinck R, Cahill MA, Engel K, Kotlyarov A, Kraft R, Kostka S, Gaestel M, Nordheim A. MAPKAP kinase 2 phosphorylates serum response factor in vitro and in vivo. J Biol Chem 274: 14434-14443, 1999.
30. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev 89: 193-277, 2009.
31. Jeon US, Kim JA, Sheen MR, Kwon HM. How tonicity regulates genes: story of TonEBP transcriptional activator. Acta Physiol (Oxf) 187: 241-247, 2006.
32. Jurmeister S, Baumann M, Balwierz A, Keklikoglou I, Ward A, Uhlmann S, Zhang JD, Wiemann S, Sahin O. MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actinregulatory proteins FHOD1 and PPM1F. Mol Cell Biol 32: 633-651, 2012.
33. Kakiashvili E, Speight P, Waheed F, Seth R, Lodyga M, Tanimura S, Kohno M, Rotstein OD, Kapus A, Szaszi K. GEF-H1 mediates tumor necrosis factor-alpha-induced Rho activation and myosin phosphorylation: role in the regulation of tubular paracellular permeability. J Biol Chem 284: 11454-11466, 2009.
34. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428, 2009.
35. Kapus A, Di Ciano C, Sun J, Zhan X, Kim L, Wong TW, Rotstein OD. Cell volume-dependent phosphorylation of proteins of the cortical cytoskeleton and cell-cell contact sites. The role of Fyn and FER kinases. J Biol Chem 275: 32289-32298, 2000.
36. Kapus A, Szaszi K, Sun J, Rizoli S, Rotstein OD. Cell shrinkageregulates Src kinases and induces tyrosine phosphorylation of cortactin, independent of the osmotic regulation of Na+/H+ exchangers. J Biol Chem 274: 8093-8102, 1999.
37. Kuwayama H, Ecke M, Gerisch G, Van Haastert PJ. Protection against osmotic stress by cGMP-mediated myosin phosphorylation. Science 271: 207-209, 1996.
38. Lewis A, Di Ciano C, Rotstein OD, Kapus A. Osmotic stress activates Rac and Cdc42 in neutrophils: role in hypertonicity-induced actin polymerization. Am J Physiol Cell Physiol 282: C271-C279, 2002.
39. Malek AM, Xu C, Kim ES, Alper SL. Hypertonicity triggers RhoAdependent assembly of myosin-containing striated polygonal actin networks in endothelial cells. Am J Physiol Cell Physiol 292: C1645-C1659, 2007.
40. Masszi A, Fan L, Rosivall L, McCulloch CA, Rotstein OD, Mucsi I, Kapus A. Integrity of cell-cell contacts is a critical regulator of TGF-beta 1-induced epithelial-to-myofibroblast transition: role for beta-catenin. Am J Pathol 165: 1955-1967, 2004.
41. Masszi A, Speight P, Charbonney E, Lodyga M, Nakano H, Szaszi K, Kapus A. Fate-determining mechanisms in epithelial-myofibroblast transition: major inhibitory role for Smad3. J Cell Biol 188: 383-399, 2010.
42. Miano JM. Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol 35: 577-593, 2003.
43. Mihira H, Suzuki HI, Akatsu Y, Yoshimatsu Y, Igarashi T, Miyazono K, Watabe T. TGF-beta-induced mesenchymal transition of MS-1 endothelial cells requires Smad-dependent cooperative activation of Rho signals and MRTF-A. J Biochem 151: 145-156, 2012.
44. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113: 329-342, 2003.
45. Morita T, Mayanagi T, Sobue K. Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J Cell Biol 179: 1027-1042, 2007.
46. Mouilleron S, Guettler S, Langer CA, Treisman R, McDonald NQ. Molecular basis for G-actin binding to RPEL motifs from the serum response factor coactivator MAL. EMBO J 27: 3198-3208, 2008.
47. Muehlich S, Wang R, Lee SM, Lewis TC, Dai C, Prywes R. Seruminduced phosphorylation of the serum response factor coactivator MKL1 by the extracellular signal-regulated kinase 1/2 pathway inhibits its nuclear localization. Mol Cell Biol 28: 6302-6313, 2008.
48. Nie M, Balda MS, Matter K. Stress- and Rho-activated ZO-1-associated nucleic acid binding protein binding to p21 mRNA mediates stabilization, translation, and cell survival. Proc Natl Acad Sci USA 109: 10897-10902, 2012.
49. Nieto MA. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 27: 347-376, 2011.
50. Olson EN, Nordheim A. Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11: 353-365, 2010.
51. Parmacek MS. Myocardin-related transcription factors: critical coactivators regulating cardiovascular development and adaptation. Circ Res 100: 633-644, 2007.
52. Pedersen SF, Hoffmann EK. Possible interrelationship between changes in F-actin and myosin II, protein phosphorylation, and cell volume regulation in Ehrlich ascites tumor cells. Exp Cell Res 277: 57-73, 2002.
53. Pedersen SF, Mills JW, Hoffmann EK. Role of the F-actin cytoskeleton in the RVD and RVI processes in Ehrlich ascites tumor cells. Exp Cell Res 252: 63-74, 1999.
54. Posern G, Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 16: 588-596, 2006.
55. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB, Myofibroblasts I. Paracrine cells important in health and disease. Am J Physiol Cell Physiol 277: C1-C9, 1999.
56. Quaggin SE, Kapus A. Scar wars: mapping the fate of epithelialmesenchymal- myofibroblast transition. Kidney Int 80: 41-50, 2011.
57. Rasmussen M, Alexander RT, Darborg BV, Mobjerg N, Hoffmann EK, Kapus A, Pedersen SF. Osmotic cell shrinkage activates ezrin/radixin/moesin (ERM) proteins: activation mechanisms and physiological implications. Am J Physiol Cell Physiol 294: C197-C212, 2008.
58. Rizoli SB, Rotstein OD, Parodo J, Phillips MJ, Kapus A. Hypertonic inhibition of exocytosis in neutrophils: central role for osmotic actin skeleton remodeling. Am J Physiol Cell Physiol 279: C619-C633, 2000.
59. Ronkina N, Menon MB, Schwermann J, Arthur JS, Legault H, Telliez JB, Kayyali US, Nebreda AR, Kotlyarov A, Gaestel M. Stress induced gene expression: a direct role for MAPKAP kinases in transcriptional activation of immediate early genes. Nucleic Acids Res 39: 2503-2518, 2011.
60. Sasazuki T, Sawada T, Sakon S, Kitamura T, Kishi T, Okazaki T, Katano M, Tanaka M, Watanabe M, Yagita H, Okumura K, Nakano H. Identification of a novel transcriptional activator, BSAC, by a functional cloning to inhibit tumor necrosis factor-induced cell death. J Biol Chem 277: 28853-28860, 2002.
61. Schliess F, Haussinger D. Osmosensing by integrins in rat liver. Methods Enzymol 428: 129-144, 2007.
62. Sebe A, Masszi A, Zulys M, Yeung T, Speight P, Rotstein OD, Nakano H, Mucsi I, Szaszi K, Kapus A. Rac, PAK and p38 regulate cell contact-dependent nuclear translocation of myocardin-related transcription factor. FEBS Lett 582: 291-298, 2008.
63. Shaposhnikov D, Descot A, Schilling J, Posern G. Myocardin-related transcription factor A regulates expression of Bok and Noxa and is involved in apoptotic signalling. Cell Cycle 11: 141-150, 2012.
64. Small EM, Thatcher JE, Sutherland LB, Kinoshita H, Gerard RD, Richardson JA, Dimaio JM, Sadek H, Kuwahara K, Olson EN. Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ Res 107: 294-304,2010.
65. Sotiropoulos A, Gineitis D, Copeland J, Treisman R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98: 159-169, 1999.
66. Takahashi K, Sasaki T, Mammoto A, Takaishi K, Kameyama T, Tsukita S, Takai Y. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J Biol Chem 272: 23371-23375, 1997.
67. Thirone AC, Speight P, Zulys M, Rotstein OD, Szaszi K, Pedersen SF, Kapus A. Hyperosmotic stress induces Rho/Rho kinase/LIM kinasemediated cofilin phosphorylation in tubular cells: key role in the osmotically triggered F-actin response. Am J Physiol Cell Physiol 296: C463-C475, 2009.
68. Tsapara A, Luthert P, Greenwood J, Hill CS, Matter K, Balda MS. The RhoA activator GEF-H1/Lfc is a transforming growth factor-beta target gene and effector that regulates alpha-smooth muscle actin expression and cell migration. Mol Biol Cell 21: 860-870, 2010.
69. Uhlik MT, Abell AN, Johnson NL, Sun W, Cuevas BD, Lobel-Rice KE, Horne EA, Dell'Acqua ML, Johnson GL. Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat Cell Biol 5: 1104-1110, 2003.
70. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316: 1749-1752, 2007.
71. Waheed F, Speight P, Dan Q, Garcia-Mata R, Szaszi K. Affinity precipitation of active Rho-GEFs using a GST-tagged mutant Rho protein (GST-RhoA(G17A)) from epithelial cell lysates. J Vis Exp 61: 3932, 2012.
72. Waheed F, Speight P, Kawai G, Dan Q, Kapus A, Szaszi K. Extracellular signal-regulated kinase and GEF-H1 mediate depolarization-induced Rho activation and paracellular permeability increase. Am J Physiol Cell Physiol 298: C1376-C1387, 2010.
73. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A, Olson EN. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci USA 99: 14855-14860, 2002.
74. Zenke FT, Krendel M, DerMardirossian C, King CC, Bohl BP, Bokoch GM. p21-activated kinase 1 phosphorylates and regulates 14-3-3 binding to GEF-H1, a microtubule-localized Rho exchange factor. J Biol Chem 279: 18392-18400, 2004.
75. Zhou X, Ferraris JD, Dmitrieva NI, Liu Y, Burg MB. MKP-1 inhibits high NaCl-induced activation of p38 but does not inhibit the activation of TonEBP/OREBP: opposite roles of p38alpha and p38delta. Proc Natl Acad Sci USA 105: 5620-5625, 2008.
76. Zhou X, Izumi Y, Burg MB, Ferraris JD. Rac1/osmosensing scaffold for MEKK3 contributes via phospholipase C-gamma1 to activation of the osmoprotective transcription factor NFAT5. Proc Natl Acad Sci USA 108: 12155-12160, 2011.