Modulation of Rho guanine exchange factor Lfc activity by protein kinase A-mediated phosphorylation

Molecular and Cellular Biology

Volumn 29, Issue 21, 2009, Pages 5963-5973

  Meiri, David ^a   Greeve, Melissa A ^a   Brunet, Andrea ^a   Finan, Dina ^a   Wells, Clark D ^b   LaRose, Jose ^a   Rottapel, Robert ^a,b,c  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; DYNEIN ADENOSINE TRIPHOSPHATASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN 14 3 3; PROTEIN LFC; PROTEIN TCTEX 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

14-3-3 PROTEINS; A KINASE ANCHOR PROTEINS; ANIMALS; CELL LINE; CONSENSUS SEQUENCE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; RATS; RHOA GTP-BINDING PROTEIN; STRESS FIBERS;

EID: 70350553837     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01268-08     Document Type: Article

References (61)

1. Aghazadeh, B., W. E. Lowry, X. Y. Huang, and M. K. Rosen. 2000. Structural basis for relief of autoinhibition of the Dbl homology domain of proto-oncogene Vav by tyrosine phosphorylation. Cell 102:625-633.
2. 1/S phase transition. Dev. Cell 8:777-786.
3. Alam, M. R., R. C. Johnson, D. N. Darlington, T. A. Hand, R. E. Mains, and B. A. Eipper. 1997. Kalirin, a cytosolic protein with spectrin-like and GDP/GTP exchange factor-like domains that interacts with peptidylglycine alpha-amidating monooxygenase, an integral membrane peptide-processing enzyme. J. Biol. Chem. 272:12667-12675.
4. Baisamy, L., N. Jurisch, and D. Diviani. 2005. Leucine zipper-mediated homo-oligomerization regulates the Rho-GEF activity of AKAP-Lbc. J. Biol. Chem. 280:15405-15412.
5. Bakal, C. J., D. Finan, J. LaRose, C. D. Wells, G. Gish, S. Kulkarni, P. DeSepulveda, A. Wilde, and R. Rottapel. 2005. The Rho GTP exchange factor Lfc promotes spindle assembly in early mitosis. Proc. Natl. Acad. Sci. USA 102:9529-9534.
6. Bateman, J., and D. Van Vactor. 2001. The Trio family of guanine-nucleotide-exchange factors: regulators of axon guidance. J. Cell Sci. 114:1973-1980. (Pubitemid 32586623)
7. Benais-Pont, G., A. Punn, C. Flores-Maldonado, J. Eckert, G. Raposo, T. P. Fleming, M. Cereijido, M. S. Balda, and K. Matter. 2003. Identification of a tight junction-associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability. J. Cell Biol. 160:729-740. (Pubitemid 36298268)
8. Birkenfeld, J., P. Nalbant, B. P. Bohl, O. Pertz, K. M. Hahn, and G. M. Bokoch. 2007. GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev. Cell 12:699-712. (Pubitemid 46671149)
9. Birukova, A. A., D. Adyshev, B. Gorshkov, G. M. Bokoch, K. G. Birukov, and A. D. Verin. 2006. GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am. J. Physiol. Lung Cell. Mol. Physiol. 290:L540-L548.
10. Callow, M. G., S. Zozulya, M. L. Gishizky, B. Jallal, and T. Smeal. 2005. PAK4 mediates morphological changes through the regulation of GEF-H1. J. Cell Sci. 118:1861-1872.
11. 1Pix guanine nucleotide exchange factor activity through 14-3-3β binding. Mol. Cell. Biol. 28:1679-1687.
12. Chardin, P., J. H. Camonis, N. W. Gale, L. van Aelst, J. Schlessinger, M. H. Wigler, and D. Bar-Sagi. 1993. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260:1338-1343. (Pubitemid 23231980)
13. Chikumi, H., A. Barac, B. Behbahani, Y. Gao, H. Teramoto, Y. Zheng, and J. S. Gutkind. 2004. Homo- and hetero-oligomerization of PDZ-RhoGEF, LARG and p115RhoGEF by their C-terminal region regulates their in vivo Rho GEF activity and transforming potential. Oncogene 23:233-240. (Pubitemid 38142257)
14. Chuang, J. Z., T. Y. Yeh, F. Bollati, C. Conde, F. Canavosio, A. Caceres, and C. H. Sung. 2005. The dynein light chain Tctex-1 has a dynein-independent role in actin remodeling during neurite outgrowth. Dev. Cell 9:75-86.
15. Colomer, V., S. Engelender, A. H. Sharp, K. Duan, J. K. Cooper, A. Lanahan, G. Lyford, P. Worley, and C. A. Ross. 1997. Huntingtin-associated protein 1 (HAP1) binds to a Trio-like polypeptide, with a rac1 guanine nucleotide exchange factor domain. Hum. Mol. Genet. 6:1519-1525.
16. Debant, A., C. Serra-Pages, K. Seipel, S. O'Brien, M. Tang, S. H. Park, and M. Streuli. 1996. The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains. Proc. Natl. Acad. Sci. USA 93:5466-5471.
17. De Sepulveda, P., K. Okkenhaug, J. L. Rose, R. G. Hawley, P. Dubreuil, and R. Rottapel. 1999. Socs1 binds to multiple signalling proteins and suppresses steel factor-dependent proliferation. EMBO J. 18:904-915. (Pubitemid 29082270)
18. Diviani, D., L. Abuin, S. Cotecchia, and L. Pansier. 2004. Anchoring of both PKA and 14-3-3 inhibits the Rho-GEF activity of the AKAP-Lbc signaling complex. EMBO J. 23:2811-2820. (Pubitemid 39013553)
19. Diviani, D., L. Baisamy, and A. Appert-Collin. 2006. AKAP-Lbc: a molecular scaffold for the integration of cyclic AMP and Rho transduction pathways. Eur. J. Cell Biol. 85:603-610.
20. Diviani, D., J. Soderling, and J. D. Scott. 2001. AKAP-Lbc anchors protein kinase A and nucleates Gα 12-selective Rho-mediated stress fiber formation. J. Biol. Chem. 276:44247-44257.
21. Eisenhaure, T. M., S. A. Francis, L. D. Willison, S. R. Coughlin, and D. J. Lerner. 2003. The Rho guanine nucleotide exchange factor Lsc homo-oligomerizes and is negatively regulated through domains in its carboxyl terminus that are absent in novel splenic isoforms. J. Biol. Chem. 278:30975-30984.
22. Ellerbroek, S. M., K. Wennerberg, and K. Burridge. 2003. Serine phosphorylation negatively regulates RhoA in vivo. J. Biol. Chem. 278:19023-19031.
23. Feng, Q., D. Baird, and R. A. Cerione. 2004. Novel regulatory mechanisms for the Dbl family guanine nucleotide exchange factor Cool-2/alpha-Pix. EMBO J. 23:3492-3504. (Pubitemid 39265539)
24. Fujishiro, S. H., S. Tanimura, S. Mure, Y. Kashimoto, K. Watanabe, and M. Kohno. 2008. ERK1/2 phosphorylate GEF-H1 to enhance its guanine nucleotide exchange activity toward RhoA. Biochem. Biophys. Res. Commun. 368:162-167.
25. Fukuhara, S., C. Murga, M. Zohar, T. Igishi, and J. S. Gutkind. 1999. A novel PDZ domain containing guanine nucleotide exchange factor links heterotrimeric G proteins to Rho. J. Biol. Chem. 274:5868-5879.
26. García-Mata, R., and K. Burridge. 2007. Catching a GEF by its tail. Trends Cell Biol. 17:36-43.
27. Gauthier-Fisher, A., D. C. Lin, M. Greeve, D. R. Kaplan, R. Rottapel, and F. D. Miller. 17 May 2009, posting date. Lfc and Tctex-1 regulate the genesis of neurons from cortical precursor cells. Nat. Neurosci. doi:10.1038/nn.2339.
28. Glaven, J. A., I. P. Whitehead, T. Nomanbhoy, R. Kay, and R. A. Cerione. 1996. Lfc and Lsc oncoproteins represent two new guanine nucleotide exchange factors for the Rho GTP-binding protein. J. Biol. Chem. 271:27374-27381.
29. Guillemot, L., E. Hammar, C. Kaister, J. Ritz, D. Caille, L. Jond, C. Bauer, P. Meda, and S. Citi. 2004. Disruption of the cingulin gene does not prevent tight junction formation but alters gene expression. J. Cell Sci. 117:5245-5256. (Pubitemid 39562487)
30. Hu, C. D., Y. Chinenov, and T. K. Kerppola. 2002. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9:789-798.
31. Hu, C. D., and T. K. Kerppola. 2003. Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol. 21:539-545.
32. Itoh, R. E., K. Kurokawa, Y. Ohba, H. Yoshizaki, N. Mochizuki, and M. Matsuda. 2002. Activation of Rac and Cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell. Biol. 22:6582-6591.
33. Jin, J., F. D. Smith, C. Stark, C. D. Wells, J. P. Fawcett, S. Kulkarni, P. Metalnikov, P. O'Donnell, P. Taylor, L. Taylor, A. Zougman, J. R. Woodgett, L. K. Langeberg, J. D. Scott, and T. Pawson. 2004. Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 14:1436-1450.
34. Katzav, S., D. Martin-Zanca, and M. Barbacid. 1989. vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells. EMBO J. 8:2283-2290. (Pubitemid 19273306)
35. Kozasa, T., X. Jiang, M. J. Hart, P. M. Sternweis, W. D. Singer, A. G. Gilman, G. Bollag, and P. C. Sternweis. 1998. p115 RhoGEF, a GTPase activating protein for Gα12 and Gα13. Science 280:2109-2111.
36. Kranewitter, W. J., and M. Gimona. 1999. N-terminally truncated Vav induces the formation of depolymerization-resistant actin filaments in NIH 3T3 cells. FEBS Lett. 455:123-129.
37. Krendel, M., F. T. Zenke, and G. M. Bokoch. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4:294-301.
38. Lang, P., F. Gesbert, M. Delespine-Carmagnat, R. Stancou, M. Pouchelet, and J. Bertoglio. 1996. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15:510-519. (Pubitemid 26044564)
39. Machado, R. D., N. Rudarakanchana, C. Atkinson, J. A. Flanagan, R. Harrison, N. W. Morrell, and R. C. Trembath. 2003. Functional interaction between BMPR-II and Tctex-1, a light chain of dynein, is isoform-specific and disrupted by mutations underlying primary pulmonary hypertension. Hum. Mol. Genet. 12:3277-3286.
40. Manganello, J. M., J. S. Huang, T. Kozasa, T. A. Voyno-Yasenetskaya, and G. C. Le Breton. 2003. Protein kinase A-mediated phosphorylation of the Galpha13 switch I region alters the Galphabetagamma13-G protein-coupled receptor complex and inhibits Rho activation. J. Biol. Chem. 278:124-130.
41. Meek, S. E., W. S. Lane, and H. Piwnica-Worms. 2004. Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J. Biol. Chem. 279:32046-32054.
42. Nimnual, A. S., B. A. Yatsula, and D. Bar-Sagi. 1998. Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science 279:560-563.
43. Okamoto, P. M., C. Gamby, D. Wells, J. Fallon, and R. B. Vallee. 2001. Dynamin isoform-specific interaction with the shank/ProSAP scaffolding proteins of the postsynaptic density and actin cytoskeleton. J. Biol. Chem. 276:48458-48465.
44. Ren, Y., R. Li, Y. Zheng, and H. Busch. 1998. Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J. Biol. Chem. 273:34954-34960.
45. Rossman, K. L., C. J. Der, and J. Sondek. 2005. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6:167-180.
46. Ryan, X. P., J. Alldritt, P. Svenningsson, P. B. Allen, G. Y. Wu, A. C. Nairn, and P. Greengard. 2005. The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47:85-100.
47. Sachdev, P., S. Menon, D. B. Kastner, J. Z. Chuang, T. Y. Yeh, C. Conde, A. Caceres, C. H. Sung, and T. P. Sakmar. 2007. G protein beta gamma subunit interaction with the dynein light-chain component Tctex-1 regulates neurite outgrowth. EMBO J. 26:2621-2632. (Pubitemid 46884283)
48. Samarin, S. N., A. I. Ivanov, G. Flatau, C. A. Parkos, and A. Nusrat. 2007. Rho/Rho-associated kinase-II signaling mediates disassembly of epithelial apical junctions. Mol. Biol. Cell 18:3429-3439.
49. Sugai, M., M. Saito, I. Sukegawa, Y. Katsushima, Y. Kinouchi, N. Nakahata, T. Shimosegawa, T. Yanagisawa, and J. Sukegawa. 2003. PTH/PTH-related protein receptor interacts directly with Tctex-1 through its COOH terminus. Biochem. Biophys. Res. Commun. 311:24-31.
50. Suzuki, N., S. Nakamura, H. Mano, and T. Kozasa. 2003. Gα 12 activates Rho GTPase through tyrosine-phosphorylated leukemia-associated RhoGEF. Proc. Natl. Acad. Sci. USA 100:733-738.
51. Takesono, A., M. J. Cismowski, C. Ribas, M. Bernard, P. Chung, S. Hazard III, E. Duzic, and S. M. Lanier. 1999. Receptor-independent activators of heterotrimeric G-protein signaling pathways. J. Biol. Chem. 274:33202-33205.
52. Takizawa, N., T. C. Smith, T. Nebl, J. L. Crowley, S. J. Palmieri, L. M. Lifshitz, A. G. Ehrhardt, L. M. Hoffman, M. C. Beckerle, and E. J. Luna. 2006. Supervillin modulation of focal adhesions involving TRIP6/ZRP-1. J. Cell Biol. 174:447-458. (Pubitemid 44156774)
53. Toksoz, D., and D. A. Williams. 1994. Novel human oncogene lbc detected by transfection with distinct homology regions to signal transduction products. Oncogene 9:621-628. (Pubitemid 24041542)
54. Westwick, J. K., R. J. Lee, Q. T. Lambert, M. Symons, R. G. Pestell, C. J. Der, and I. P. Whitehead. 1998. Transforming potential of Dbl family proteins correlates with transcription from the cyclin D1 promoter but not with activation of Jun NH2-terminal kinase, p38/Mpk2, serum response factor, or c-Jun. J. Biol. Chem. 273:16739-16747.
55. Whitehead, I., H. Kirk, C. Tognon, G. Trigo-Gonzalez, and R. Kay. 1995. Expression cloning of lfc, a novel oncogene with structural similarities to guanine nucleotide exchange factors and to the regulatory region of protein kinase C. J. Biol. Chem. 270:18388-18395.
56. Wong, W., and J. D. Scott. 2004. AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell Biol. 5:959-970.
57. Wu, J., J. Zhai, H. Lin, Z. Nie, W. W. Ge, L. Garcia-Bermejo, R. J. Muschel, W. W. Schlaepfer, and R. Canete-Soler. 2003. Cytoplasmic retention sites in p190RhoGEF confer anti-apoptotic activity to an EGFP-tagged protein. Brain Res. Mol. Brain Res. 117:27-38.
58. Yano, H., and M. V. Chao. 2005. Biochemical characterization of intracellular membranes bearing Trk neurotrophin receptors. Neurochem. Res. 30:767-777.
59. Zenke, F. T., M. Krendel, C. DerMardirossian, C. C. King, B. P. Bohl, and G. M. Bokoch. 2004. 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.
60. Zhai, J., H. Lin, M. Shamim, W. W. Schlaepfer, and R. Canete-Soler. 2001. Identification of a novel interaction of 14-3-3 with p190RhoGEF. J. Biol. Chem. 276:41318-41324.
61. Zhu, K., B. Debreceni, F. Bi, and Y. Zheng. 2001. Oligomerization of DH domain is essential for Dbl-induced transformation. Mol. Cell. Biol. 21:425-437.