Zyxin is involved in thrombin signaling via interaction with PAR-1 receptor

FASEB Journal

Volumn 23, Issue 12, 2009, Pages 4193-4206

  Han, Jingyan ^a   Liu, Guoquan ^a   Profirovic, Jasmina ^a   Niu, Jiaxin ^a   Voyno Yasenetskaya, Tatyana ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Actin cytoskeleton; Endothelium; G protein coupled receptors; Heterotrimeric G proteins

Indexed keywords

INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEINASE ACTIVATED RECEPTOR 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; THROMBIN; VASODILATOR STIMULATED PHOSPHOPROTEIN; ZYXIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS7; CHO CELL; DOWN REGULATION; ENDOTHELIUM CELL; FEMALE; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SERUM RESPONSIVE ELEMENT; SIGNAL TRANSDUCTION; STRESS FIBER;

ANIMALS; CELL ADHESION MOLECULES; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETAL PROTEINS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GLYCOPROTEINS; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; MICROFILAMENT PROTEINS; PHOSPHOPROTEINS; PROTEIN TRANSPORT; RECEPTOR, PAR-1; SIGNAL TRANSDUCTION; THROMBIN;

EID: 72749107915     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-131862     Document Type: Article

References (60)

1. Narayanan, S. (1999) Multifunctional roles of thrombin. Ann. Clin. Lab. Sci. 29, 275-280
2. Minami, T., Sugiyama, A., Wu, S. Q., Abid, R., Kodama, T., and Aird, W. C. (2004) Thrombin and phenotypic modulation of the endothelium. Arterscler. Thromb. Vasc. Biol. 24, 41-53
3. Coughlin, S. R. (1999) How the protease thrombin talks to cells. Proc. Natl. Acad. Sci. U. S. A. 96, 11023-11027
4. O'Brien, P. J., Prevost, N., Molino, M., Hollinger, M. K., Woolkalis, M. J., Woulfe, D. S., and Brass, L. F. (2000) Thrombin responses in human endothelial cells. contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J. Biol. Chem. 275, 13502-13509 (Pubitemid 30257415)
5. Rahman, A., True, A. L., Anwar, K. N., Ye, R. D., Voyno-Yasenetskaya, T. A., and Malik, A. B. (2002) Galpha(q) and gbetagamma regulate PAR-1 signaling of thrombin-induced NF-kappaB activation and ICAM-1 transcription in endothelial cells. Circ. Res. 91, 398-405 (Pubitemid 35034207)
6. Vanhauwe, J. F., Thomas, T. O., Minshall, R. D., Tiruppathi, C., Li, A., Gilchrist, A., Yoon, E. J., Malik, A. B., and Hamm, H. E. (2002) Thrombin receptors activate G(o) proteins in endothelial cells to regulate intracellular calcium and cell shape changes. J. Biol. Chem. 277, 34143-34149 (Pubitemid 35056234)
7. Martin, C. B., Mahon, G. M., Klinger, M. B., Kay, R. J., Symons, M., Der, C. J., and Whitehead, I. P. (2001) The thrombin receptor, PAR-1, causes transformation by activation of rho-mediated signaling pathways. Oncogene 20, 1953-1963 (Pubitemid 32458027)
8. McLaughlin, J. N., Shen, L., Holinstat, M., Brooks, J. D., Dibenedetto, E., and Hamm, H. E. (2005) Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J. Biol. Chem. 280, 25048-25059 (Pubitemid 40934596)
9. Chikumi, H., Fukuhara, S., and Gutkind, J. S. (2002) Regulation of G protein-linked guanine nucleotide exchange factors for rho, PDZ-RhoGEF, and LARG by tyrosine phosphorylation: evidence of a role for focal adhesion kinase. J. Biol. Chem. 277, 12463-12473 (Pubitemid 34952821)
10. Buhl, A. M., Johnson, N. L., Dhanasekaran, N., and Johnson, G. L. (1995) G alpha 12 and G alpha 13 stimulate rhodependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270, 24631-24634
11. Pai, K. S., Mahajan, V. B., Lau, A., and Cunningham, D. D. (2001) Thrombin receptor signaling to cytoskeleton requires Hsp90. J. Biol. Chem. 276, 32642-32647 (Pubitemid 37384705)
12. Vaiskunaite, R., Kozasa, T., and Voyno-Yasenetskaya, T. A. (2001) Interaction between the G alpha subunit of heterotrimeric G (12) protein and Hsp90 is required for G alpha(12) signaling. J. Biol. Chem. 276, 46088-46093 (Pubitemid 37370857)
13. Macalma, T., Otte, J., Hensler, M. E., Bockholt, S. M., Louis, H. A., Kalff-Suske, M., Grzeschik, K. H., von der Ahe, D., and Beckerle, M. C. (1996) Molecular characterization of human zyxin. J. Biol. Chem. 271, 31470-31478
14. Beckerle, M. C. (1997) Zyxin: zinc fingers at sites of cell adhesion. BioEssays 19, 949-957
15. Drees, B., Friederich, E., Fradelizi, J., Louvard, D., Beckerle, M. C., and Golsteyn, R. M. (2000) Characterization of the interaction between zyxin and members of the Ena/vasodilator-stimulated phosphoprotein family of proteins. J. Biol. Chem. 275, 22503-22511 (Pubitemid 30621839)
16. Li, B., and Trueb, B. (2001) Analysis of the alpha-actinin/zyxin interaction. J. Biol. Chem. 276, 33328-33335
17. Fradelizi, J., Noireaux, V., Plastino, J., Menichi, B., Louvard, D., Sykes, C., Golsteyn, R. M., and Friederich, E. (2001) ActA and human zyxin harbour Arp2/3-independent actin-polymerization activity. Nat. Cell Biol. 3, 699-707 (Pubitemid 32734247)
18. Hobert, O., Schilling, J. W., Beckerle, M. C., Ullrich, A., and Jallal, B. (1996) SH3 domain-dependent interaction of the proto-oncogene product vav with the focal contact protein zyxin. Oncogene 12, 1577-1581 (Pubitemid 26132045)
19. Dawid, I. B., Toyama, R., and Taira, M. (1995) LIM domain proteins. Compt. Rendus Acad. Sci. III Sci. Vie. 318, 295-306
20. Schmeichel, K. L., and Beckerle, M. C. (1998) LIM domains of cysteine-rich protein 1 (CRP1) are essential for its zyxin-binding function. Biochem. J. 331(Pt. 3), 885-892
21. Yi, J., Kloeker, S., Jensen, C. C., Bockholt, S., Honda, H., Hirai, H., and Beckerle, M. C. (2002) Members of the zyxin family of LIM proteins interact with members of the p130Cas family of signal transducers. J. Biol. Chem. 277, 9580-9589 (Pubitemid 34953047)
22. Hirota, T., Morisaki, T., Nishiyama, Y., Marumoto, T., Tada, K., Hara, T., Masuko, N., Inagaki, M., Hatakeyama, K., and Saya, H. (2000) Zyxin, a regulator of actin filament assembly, targets the mitotic apparatus by interacting with h-warts/LATS1 tumor suppressor. J. Cell Biol. 149, 1073-1086 (Pubitemid 30354257)
23. Nix, D. A., Fradelizi, J., Bockholt, S., Menichi, B., Louvard, D., Friederich, E., and Beckerle, M. C. (2001) Targeting of zyxin to sites of actin membrane interaction and to the nucleus. J. Biol. Chem. 276, 34759-34767 (Pubitemid 37384475)
24. Kato, T., Muraski, J., Chen, Y., Tsujita, Y., Wall, J., Glembotski, C. C., Schaefer, E., Beckerle, M., and Sussman, M. A. (2005) Atrial natriuretic peptide promotes cardiomyocyte survival by cGMP-dependent nuclear accumulation of zyxin and akt. J. Clin. Invest. 115, 2716-2730 (Pubitemid 41434399)
25. Yoshigi, M., Hoffman, L. M., Jensen, C. C., Yost, H. J., and Beckerle, M. C. (2005) Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J. Cell Biol. 171, 209-215 (Pubitemid 41540014)
26. Xu, J., Lai, Y. J., Lin, W. C., and Lin, F. T. (2004) TRIP6 enhances lysophosphatidic acid-induced cell migration by interacting with the lysophosphatidic acid 2 receptor. J. Biol. Chem. 279, 10459-10468 (Pubitemid 38372655)
27. Gorovoy, M., Niu, J., Bernard, O., Profirovic, J., Minshall, R., Neamu, R., and Voyno-Yasenetskaya, T. (2005) LIM kinase 1 coordinates microtubule stability and actin polymerization in human endothelial cells. J. Biol. Chem. 280, 26533-26542 (Pubitemid 41022251)
28. Andreeva, A. V., Kutuzov, M. A., Vaiskunaite, R., Profirovic, J., Meigs, T. E., Predescu, S., Malik, A. B., and Voyno-Yasenetskaya, T. (2005) G alpha12 interaction with alphaSNAP induces VE-cadherin localization at endothelial junctions and regulates barrier function. J. Biol. Chem. 280, 30376-30383 (Pubitemid 41216220)
29. Vaiskunaite, R., Adarichev, V., Furthmayr, H., Kozasa, T., Gudkov, A., and Voyno-Yasenetskaya, T. A. (2000) Conformational activation of radixin by G13 protein alpha subunit. J. Biol. Chem. 275, 26206-26212 (Pubitemid 30676667)
30. Voyno-Yasenetskaya, T., Conklin, B. R., Gilbert, R. L., Hooley, R., Bourne, H. R., and Barber, D. L. (1994) G alpha 13 stimulates na-H exchange. J. Biol. Chem. 269, 4721-4724
31. Schaphorst, K. L., Pavalko, F. M., Patterson, C. E., and Garcia, J. G. (1997) Thrombin-mediated focal adhesion plaque reorganization in endothelium: Role of protein phosphorylation. Am. J. Resp. Cell Mol. Biol. 17, 443-455
32. Lum, H., and Malik, A. B. (1996) Mechanisms of increased endothelial permeability. Canad. J. Physiol. Pharmacol. 74, 787-800
33. Mao, J., Yuan, H., Xie, W., Simon, M. I., and Wu, D. (1998) Specific involvement of G proteins in regulation of serum response factor-mediated gene transcription by different receptors. J. Biol. Chem. 273, 27118-27123 (Pubitemid 28500418)
34. Dudek, S. M., and Garcia, J. G. (2001) Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol. 91, 1487-1500
35. Wojciak-Stothard, B., Potempa, S., Eichholtz, T., and Ridley, A. J. (2001) Rho and rac but not Cdc42 regulate endothelial cell permeability. J. Cell Sci. 114, 1343-1355 (Pubitemid 32409470)
36. Baumer, Y., Drenckhahn, D., and Waschke, J. (2008) cAMP induced rac 1-mediated cytoskeletal reorganization in microvascular endothelium. Histochem. Cell Biol. 129, 765-778
37. Mehta, D., and Malik, A. B. (2006) Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86, 279-367
38. Waschke, J., Baumgartner, W., Adamson, R. H., Zeng, M., Aktories, K., Barth, H., Wilde, C., Curry, F. E., and Drenckhahn, D. (2004) Requirement of rac activity for maintenance of capillary endothelial barrier properties. Am. J. Physiol. Heart Circ. Physiol. 286, H394-401 (Pubitemid 38049505)
39. Hirata, H., Tatsumi, H., and Sokabe, M. (2008) Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J. Cell Sci. 121, 2795-2804
40. Lele, T. P., Pendse, J., Kumar, S., Salanga, M., Karavitis, J., and Ingber, D. E. (2006) Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. J. Cell Physiol. 207, 187-194
41. Yi, J., and Beckerle, M. C. (1998) The human TRIP6 gene encodes a LIM domain protein and maps to chromosome 7q22, a region associated with tumorigenesis. Genomics 49, 314-316 (Pubitemid 28240700)
42. Sahai, E., Alberts, A. S., and Treisman, R. (1998) RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. EMBO J. 17, 1350-1361 (Pubitemid 28105514)
43. Hill, C. S., Wynne, J., and Treisman, R. (1995) The rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81, 1159-1170
44. Gohla, A., Offermanns, S., Wilkie, T. M., and Schultz, G. (1999) Differential involvement of Galpha12 and Galpha13 in receptor-mediated stress fiber formation. J. Biol. Chem. 274, 17901-17907
45. Holinstat, M., Mehta, D., Kozasa, T., Minshall, R. D., and Malik, A. B. (2003) Protein kinase calpha-induced p115RhoGEF phosphorylation signals endothelial cytoskeletal rearrangement. J. Biol. Chem. 278, 28793-28798 (Pubitemid 36935789)
46. Kozasa, T., Jiang, X., Hart, M. J., Sternweis, P. M., Singer, W. D., Gilman, A. G., Bollag, G., and Sternweis, P. C. (1998) p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13. Science 280, 2109-2111
47. Conklin, B. R., Chabre, O., Wong, Y. H., Federman, A. D., and Bourne, H. R. (1992) Recombinant gq alpha. mutational activation and coupling to receptors and phospholipase C. J. Biol. Chem. 267, 31-34
48. Katada, T., Northup, J. K., Bokoch, G. M., Ui, M., and Gilman, A. G. (1984) The inhibitory guanine nucleotide-binding regulatory component of adenylate cyclase. Subunit dissociation and guanine nucleotide-dependent hormonal inhibition. J. Biol. Chem. 259, 3578-3585 (Pubitemid 14170087)
49. Laurent, V., Loisel, T. P., Harbeck, B., Wehman, A., Grobe, L., Jockusch, B. M., Wehland, J., Gertler, F. B., and Carlier, M. F. (1999) Role of proteins of the Ena/VASP family in actin-based motility of listeria monocytogenes. J. Cell Biol. 144, 1245-1258 (Pubitemid 29157302)
50. Han, Y. H., Chung, C. Y., Wessels, D., Stephens, S., Titus, M. A., Soll, D. R., and Firtel, R. A. (2002) Requirement of a vasodilator-stimulated phosphoprotein family member for cell adhesion, the formation of filopodia, and chemotaxis in dictyostelium. J. Biol. Chem. 277, 49877-49887 (Pubitemid 36014436)
51. Garcia, J. G., and Schaphorst, K. L. (1995) Regulation of endothelial cell gap formation and paracellular permeability. J. Invest. Med. 43, 117-126
52. Hoffman, L. M., Jensen, C. C., Kloeker, S., Wang, C. L., Yoshigi, M., and Beckerle, M. C. (2006) Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling. J. Cell Biol. 172, 771-782 (Pubitemid 43306232)
53. Copeland, J. W., and Treisman, R. (2002) The diaphanous-related formin mDia1 controls serum response factor activity through its effects on actin polymerization. Mol. Biol. Cell 13, 4088-4099
54. Geneste, O., Copeland, J. W., and Treisman, R. (2002) LIM kinase and diaphanous cooperate to regulate serum response factor and actin dynamics. J. Cell Biol. 157, 831-838 (Pubitemid 34847820)
55. Grosse, R., Copeland, J. W., Newsome, T. P., Way, M., and Treisman, R. (2003) A role for VASP in RhoA-diaphanous signalling to actin dynamics and SRF activity. EMBO J. 22, 3050-3061 (Pubitemid 36758625)
56. Posern, G., Sotiropoulos, A., and Treisman, R. (2002) Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol. Biol. Cell. 13, 4167-4178 (Pubitemid 35471176)
57. Sotiropoulos, A., Gineitis, D., Copeland, J., and Treisman, R. (1999) Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159-169 (Pubitemid 29344904)
58. Mahajan, V. B., Pai, K. S., Lau, A., and Cunningham, D. D. (2000) Creatine kinase, an ATP-generating enzyme, is required for thrombin receptor signaling to the cytoskeleton. Proc. Natl. Acad. Sci. U. S. A. 97, 12062-12067 (Pubitemid 30815138)
59. Rajagopal, K., Lefkowitz, R. J., and Rockman, H. A. (2005) When 7 transmembrane receptors are not G protein-coupled receptors. J. Clin. Invest. 115, 2971-2974 (Pubitemid 41567561)
60. Zhai, P., Yamamoto, M., Galeotti, J., Liu, J., Masurekar, M., Thaisz, J., Irie, K., Holle, E., Yu, X., Kupershmidt, S., Roden, D. M., Wagner, T., Yatani, A., Vatner, D. E., Vatner, S. F., and Sadoshima, J. (2005) Cardiac-specific overexpression of AT1 receptor mutant lacking G alpha q/G alpha i coupling causes hypertrophy and bradycardia in transgenic mice. J. Clin. Invest. 115, 3045-3056