The RhoA/Rho kinase pathway regulates nuclear localization of serum response factor

American Journal of Respiratory Cell and Molecular Biology

Volumn 29, Issue 1, 2003, Pages 39-47

  Liu, Hong Wei ^b   Halayko, Andrew J ^b   Fernandes, Darren J ^b   Harmon, Gregory S ^b   McCauley, Joel A ^b   Kocieniewski, Pawel ^b   McConville, John ^b   Fu, Yiping ^b   Forsythe, Sean M ^b   Kogut, Paul ^b   Bellam, Shashi ^b   Dowell, Maria ^b   Churchill, Jason ^b   Lesso, Heinte ^b   Kassiri, Kamrouz ^b   Mitchell, Richard W ^b   Hershenson, Marc B ^b   Camoretti Mercado, Blanca ^b   Solway, Julian ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CLOSTRIDIUM TOXIN; LATRUNCULIN B; MYOSIN HEAVY CHAIN; PHOSPHOTRANSFERASE INHIBITOR; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR AP 2;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BREATHING MUSCLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DOG; ENZYME INHIBITION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PROMOTER REGION; PROTEIN CONTENT; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; SKELETAL MUSCLE; SMOOTH MUSCLE; SMOOTH MUSCLE CONTRACTILITY; TRANSCRIPTION REGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; AMIDES; ANIMALS; BACTERIAL TOXINS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL NUCLEUS; CELLS, CULTURED; DOGS; ENZYME INHIBITORS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUSCLE CELLS; MUSCLE, SMOOTH; MYOSIN HEAVY CHAINS; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; PYRIDINES; RHOA GTP-BINDING PROTEIN; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; THIAZOLES; THIAZOLIDINES; TRACHEA; TRANSCRIPTION, GENETIC;

ANIMALIA; CANIS FAMILIARIS; CLOSTRIDIUM; MAIZE STREAK VIRUS;

EID: 0012265697     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2002-0206OC     Document Type: Article

References (58)

1. Van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
2. Uehata, M., T. Ishizaki, H. Satoh, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya. 1997. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389:990-994.
3. Lamb, R. F., C. Roy, T. J. Diefenbach, H. V. Vinters, M. W. Johnson, D. G. Jay, and A. Hall. 2000. The TSC1 tumour suppressor hamartin regulates cell adhesion through ERM proteins and the GTPase Rho. Nat. Cell Biol. 2:281-287.
4. Nobes, C. D., and A. Hall. 1999. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144:1235-1244.
5. Togashi, H., C. W. Emala, I. P. Hall, and C. A. Hirshman. 1998. Carbachol-induced actin reorganization involves Gi activation of Rho in human airway smooth muscle cells. Am. J. Physiol. 274:L803-L809.
6. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
7. Hotchin, N. A., and A. Hall. 1995. The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J. Cell Biol. 131:1857-1865.
8. Nobes, C. D., and A. Hall. 1995. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
9. Hill, C. S., J. Wynne, and R. Treisman. 1994. Serum-regulated transcription by serum response factor (SRF): a novel role for the DNA binding domain. EMBO J. 13:5421-5432.
10. Price, M. A., C. Hill, and R. Treisman. 1996. Integration of growth factor signals at the c-fos serum response element. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351:551-559.
11. Zohar, M., H. Teramoto, B. Z. Katz, K. M. Yamada, and J. S. Gutkind. 1998. Effector domain mutants of Rho dissociate cytoskeletal changes from nuclear signaling and cellular transformation. Oncogene 17:991-998.
12. Hill, C. S., J. Wynne, and R. Treisman. 1995. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81:1159-1170.
13. Wei, L., W. Zhou, J. D. Croissant, F. E. Johansen, R. Prywes, A. Balasubramanyam, and R. J. Schwartz. 1998. RhoA signaling via serum response factor plays an obligatory role in myogenic differentiation. J. Biol. Chem. 273:30287-30294.
14. Mack, C. P., A. V. Somlyo, M. Hautmann, A. P. Somlyo, and G. K. Owens. 2001. Smooth muscle differentiation marker gene expression is regulated by RhoA-mediated actin polymerization. J. Biol. Chem. 276:341-347.
15. Camoretti-Mercado, B., H. W. Liu, A. J. Halayko, S. M. Forsythe, J. W. Kyle, B. Li, Y. Fu, J. McConville, P. Kogut, J. E. Vieira, N. M. Patel, M. B. Hershenson, E. Fuchs, S. Sinha, J. M. Miano, M. S. Parmacek, J. K. Burkhardt, and J. Solway. 2000. Physiological control of smooth muscle-specific gene expression through regulated nuclear translocation of serum response factor. J. Biol. Chem. 275:30387-30393.
16. Rech, J., I. Barlat, J. L. Veyrune, A. Vie, and J. M. Blanchard. 1994. Nuclear import of serum response factor (SRF) requires a short amino-terminal nuclear localization sequence and is independent of the casein kinase II phosphorylation site. J. Cell Sci. 107:3029-3036.
17. Gauthier-Rouviere, C., M. Vandromme, N. Lautredou, Q. Q. Cai, F. Girard, A. Fernandez, and N. Lamb. 1995. The serum response factor nuclear localization signal: general implications for cyclic AMP-dependent protein kinase activity in control of nuclear translocation. Mol. Cell. Biol. 15:433-444.
18. Ding, W., M. M. Witte, and R. E. Scott. 1999. Transformation blocks differentiation-induced inhibition of serum response factor interactions with serum response elements. Cancer Res. 59:3795-3802.
19. Chihara, K., M. Amano, N. Nakamura, T. Yano, M. Shibata, T. Tokui, H. Ichikawa, R. Ikebe, M. Ikebe, and K. Kaibuchi. 1997. Cytoskeletal rearrangements and transcriptional activation of c-fos serum response element by Rho-kinase. J. Biol. Chem. 272:25121-25127.
20. Alberts, A. S., O. Geneste, and R. Treisman. 1998. Activation of SRF-regulated chromosomal templates by Rho-family GTPases requires a signal that also induces H4 hyperacetylation. Cell 92:475-487.
21. Sahai, E., A. S. Alberts, and R. Treisman. 1998. RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. EMBO J. 17:1350-1361.
22. Treisman, R., A. S. Alberts, and E. Sahai. 1998. Regulation of SRF activity by Rho family GTPases. Cold Spring Harb. Syrup. Quant. Biol. 63:643-651.
23. Sotiropoulos, A., D. Gineitis, J. Copeland, and R. Treisman. 1999. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98:159-169.
24. Geneste, O., J. W. Copeland, and R. Treisman. 2002. LIM kinase and Diaphanous cooperate to regulate serum response factor and actin dynamics. J. Cell Biol. 157:831-838.
25. Mitchell, R. W., A. J. Halayko, S. Kahraman, J. Solway, and M. E. Wylam. 2000. Selective restoration of calcium coupling to muscarinic M(3) receptors in contractile cultured airway myocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:L1091-L1100.
26. Ishizaki, T., M. Uehata, I. Tamechika, J. Keel, K. Nonomura, M. Maekawa, and S. Narumiya. 2000. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol. Pharmacol. 57:976-983.
27. Fujisawa, K., P. Madaule, T. Ishizaki, G. Watanabe, H. Bito, Y. Saito, A. Hall, and S. Narumiya. 1998. Different regions of Rho determine Rho-selective binding of different classes of Rho target molecules. J. Biol. Chem. 273:18943-18949.
28. Solway, J., J. Seltzer, F. F. Samaha, S. Kim, L. E. Alger, Q. Niu, E. E. Morrisey, H. S. Ip, and M. S. Parmacek. 1995. Structure and expression of a smooth muscle cell-specific gene. SM22 alpha. J. Biol. Chem. 270: 13460-13469.
29. Camoretti-Mercado, B., S. M. Forsythe, M. M. LeBeau, R. Espinosa iii, J. E. Vieira, A. J. Halayko, S. Willadsen, B. Kurtz, C. Ober, G. A. Evans, R. Thweatt, S. Shapiro, Q. Niu, Y. Qin, P. A. Padrid, and J. Solway. 1998. Expression and cytogenetic localization of the human SM22 gene (TAGLN). Genomics 49:452-457.
30. Lamarche, N., N. Tapon, L. Stowers, P. D. Burbelo, P. Aspenstrom, T. Bridges, J. Chant, and A. Hall. 1996. Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell 87:519-529.
31. Halayko, A. J., B. Camoretti-Mercado, S. M. Forsythe, J. E. Vieira, R. W. Mitchell, M. E. Wylam, M. B. Hershenson, and J. Solway. 1999. Divergent differentiation paths in airway smooth muscle culture: induction of functionally contractile myocytes. Am. J. Physiol. 276:L197-L206.
32. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
33. Li, L., Z. Liu, B. Mercer, P. Overbeek, and E. N. Olson. 1997. Evidence for serum response factor-mediated regulatory networks governing SM22alpha transcription in smooth, skeletal, and cardiac muscle cells. Dev. Biol. 187:311-321.
34. Li, L., J. M. Miano, P. Cserjesi, and E. N. Olson. 1996. SM22 alpha, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ. Res. 78:188-195.
35. Li, L., J. M. Miano, B. Mercer, and E. N. Olson. 1996. Expression of the SM22alpha promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J. Cell Biol. 132:849-859.
36. Kim, S., H. S. Ip, M. M. Lu, C. Clendenin, and M. S. Parmacek. 1997. A serum response factor-dependent transcriptional regulatory program identifies distinct smooth muscle cell sublineages. Mol. Cell. Biol. 17:2266-2278.
37. Madsen, C. S., C. P. Regan, and G. K. Owens. 1997. Interaction of CArG elements and a GC-rich repressor element in transcriptional regulation of the smooth muscle myosin heavy chain gene in vascular smooth muscle cells. J. Biol. Chem. 272:29842-29851.
38. Madsen, C. S., J. C. Hershey, M. B. Hautmann, S. L. White, and G. K. Owens. 1997. Expression of the smooth muscle myosin heavy chain gene is regulated by a negative-acting GC-rich element located between two positive-acting serum response factor-binding elements. J. Biol. Chem. 272:6332-6340.
39. Katoh, Y., E. Loukianov, E. Kopras, A. Zilberman, and M. Periasamy. 1994. Identification of functional promoter elements in the rabbit smooth muscle myosin heavy chain gene. J. Biol. Chem. 269:30538-30545.
40. Zilberman, A., V. Dave, J. Miano, E. N. Olson, and M. Periasamy. 1998. Evolutionarily conserved promoter region containing CArG*-like elements is crucial for smooth muscle myosin heavy chain gene expression. Circ. Res. 82:566-575.
41. Ishizaki, T., M. Naito, K. Fujisawa, M. Maekawa, N. Watanabe, Y. Saito, and S. Narumiya. 1997. p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett. 404:128-124.
42. Nakano, K., K. Takaishi, A. Kodama, A. Mammoto, H. Shiozaki, M. Monden, and Y. Takai. 1999. Distinct actions and cooperative roles of ROCK and mDia in Rho small G protein-induced reorganization of the actin cytoskeleton in Madin-Darby canine kidney cells. Mol. Biol. Cell 10:2481-2491.
43. Spencer, J. A., and R. P. Misra. 1999. Expression of the SRF gene occurs through a Ras/Sp/SRF-mediated mechanism in response to serum growth signals. Oncogene 18:7319-7327.
44. Spencer, J. A., and R. P. Misra. 1996. Expression of the serum response factor gene is regulated by serum response factor binding sites. J. Biol. Chem. 271:16535-16543.
45. Strassheim, D., L. G. May, K. A. Varker, H. L. Puhl, S. H. Phelps, R. A. Porter, R. S. Aronstam, J. D. Noti, and C. L. Williams. 1999. M3 muscarinic acetylcholine receptors regulate cytoplasmic myosin by a process involving RhoA and requiring conventional protein kinase C isoforms. J. Biol. Chem. 274:18675-18685.
46. Hippenstiel, S., T. Kratz, M. Krull, J. Seybold, C. von Eichel-Streiber, and N. Suttorp. 1998. Rho protein inhibition blocks protein kinase C translocation and activation. Biochem. Biophys. Res. Commun. 245:830-834.
47. Nozu, F., Y. Tsunoda, A. I. Ibitayo, K. N. Bitar, and C. Owyang. 1999. Involvement of RhoA and its interaction with protein kinase C and Src in CCK-stimulated pancreatic acini. Am. J. Physiol. 276:G915-G923.
48. Taggart, M. J., Y. H. Lee, and K. G. Morgan. 1999. Cellular redistribution of PKCalpha, rhoA, and ROKalpha following smooth muscle agonist stimulation. Exp. Cell Res. 251:92-101.
49. Soh, J. W., E. H. Lee, R. Prywes, and I. B. Weinstein. 1999. Novel roles of specific isoforms of protein kinase C in activation of the c-fos serum response element. Mol. Cell. Biol. 19:1313-1324.
50. Kim, H. J., J. H. Kim, and J. W. Lee. 1998. Steroid receptor coactivator-1 interacts with serum response factor and coactivates serum response element-mediated transactivations. J. Biol. Chem. 273:28564-28567.
51. Ramirez, S., S. Ait-Si-Ali, P. Robin, D. Trouche, A. Harel-Bellan, and S. Ait Si Ali. 1997. The CREB-binding protein (CBP) cooperates with the serum response factor for transactivation of the c-fos serum response element. J. Biol. Chem. 272:31016-31021.
52. Kallio, P. J., K. Okamoto, S. O'Brien, P. Carrero, Y. Makino, H. Tanaka, and L. Poellinger. 1998. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J. 17:6573-6586.
53. Blobel, G. A., T. Nakajima, R. Eckner, M. Montminy, and S. H. Orkin. 1998. CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc. Natl. Acad. Sci. USA 95:2061-2066.
54. Kakita, T., K. Hasegawa, T. Morimoto, S. Kaburagi, H. Wada, and S. Sasayama. 1999. p300 protein as a coactivator of GATA-5 in the transcription of cardiac-restricted atrial natriuretic factor gene. J. Biol. Chem. 274:34096-34102.
55. Wada, H., K. Hasegawa, T. Morimoto, T. Kakita, T. Yanazume, and S. Sasayama. 2000. A p300 protein as a coactivator of GATA-6 in the transcription of the smooth muscle-myosin heavy chain gene. J. Biol. Chem. 275:25330-25335.
56. Kumar, K. P., K. M. McBride, B. K. Weaver, C. Dingwall, and N. C. Reich. 2000. Regulated nuclear-cytoplasmic localization of interferon regulatory factor 3, a subunit of double-stranded RNA-activated factor 1. Mol. Cell. Biol. 20:4159-4168.
57. Lu, J., T. E. Landerholm, J. S. Wei, X. R. Dong, S. P. Wu, X. Liu, K. Nagata, M. Inagaki, and M. W. Majesky. 2001. Coronary smooth muscle differentiation from proepicardial cells requires rhoA-mediated actin reorganization and p160 rho-kinase activity. Dev. Biol. 240:404-418.
58. Beqaj, S., S. Jakkaraju, R. R. Mattingly, D. Pan, and L. Schuger. 2002. High RhoA activity maintains the undifferentiated mesenchymal cell phenotype, whereas RhoA down-regulation by laminin-2 induces smooth muscle myogenesis. J. Cell Biol. 156:893-903.