The many faces of the guanine-nucleotide exchange factor trio

Cell Adhesion and Migration

Volumn 6, Issue 6, 2012, Pages 482-487

  Van Rijssel, Jos ^a   Van Buul, Jaap D ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Lamellipodia; Rac1; Rho GEF; RhoG; Trio

Indexed keywords

DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; F ACTIN; FILAMIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR TRIO; KALIRIN; PROTEIN; PROTEIN SH3; RAC1 PROTEIN; SPECTRIN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BLADDER CANCER; BREAST TUMOR; CANCER PATIENT; CARCINOGENESIS; CELL MIGRATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GLIOBLASTOMA; HUMAN; LEUKOCYTE; NERVE CELL DIFFERENTIATION; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SOFT TISSUE SARCOMA;

EID: 84872093495     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.21418     Document Type: Article

References (67)

1. Debant A, Serra-Pagès C, Seipel K, O 'Brien S, Tang M, Park SH, et al. 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 U S A 1996; 93:5466-71; PMID:8643598; http://dx.doi.org/10.1073/pnas.93.11.5466
2. Bellanger JM, Lazaro JB, Diriong S, Fernandez A, Lamb N, Debant A. The two guanine nucleotide exchange factor domains of Trio link the Rac1 and the RhoA pathways in vivo. Oncogene 1998; 16:147-52; PMID:9464532; http://dx.doi.org/10.1038/sj.onc.1201532
3. Blangy A, Vignal E, Schmidt S, Debant A, Gauthier-Rouvière C, Fort P. TrioGEF1 controls Rac- and Cdc42-dependent cell structures through the direct activation of rhoG. J Cell Sci 2000; 113:729-39; PMID:10652265
4. Seipel K, Medley QG, Kedersha NL, Zhang XA, O 'Brien SP, Serra-Pages C, et al. Trio amino-terminal guanine nucleotide exchange factor domain expression promotes actin cytoskeleton reorganization, cell migration and anchorage-independent cell growth. J Cell Sci 1999; 112:1825-34; PMID:10341202
5. Medley QG, Serra-Pagès C, Iannotti E, Seipel K, Tang M, O 'Brien SP, et al. The trio guanine nucleotide exchange factor is a RhoA target. Binding of RhoA to the trio immunoglobulin-like domain. J Biol Chem 2000; 275:36116-23; PMID:10948190; http://dx.doi.org/10.1074/jbc.M003775200
6. Medley QG, Buchbinder EG, Tachibana K, Ngo H, Serra-Pagès C, Streuli M. Signaling between focal adhesion kinase and trio. J Biol Chem 2003; 278: 13265-70; PMID:12551902; http://dx.doi.org/10.1074/jbc.M300277200
7. McPherson CE, Eipper BA, Mains RE. Multiple novel isoforms of Trio are expressed in the developing rat brain. Gene 2005; 347:125-35; PMID:15715966; http://dx.doi.org/10.1016/j.gene.2004.12.028
8. Saito K, Tautz L, Mustelin T. The lipid-binding SEC14 domain. Biochim Biophys Acta 2007; 1771: 719-26; PMID:17428729; http://dx.doi.org/10.1016/j. bbalip.2007.02.010
9. Alam MR, Caldwell BD, Johnson RC, Darlington DN, Mains RE, Eipper BA. Novel proteins that interact with the COOH-terminal cytosolic routing determinants of an integral membrane peptide-processing enzyme. J Biol Chem 1996; 271:28636-40; PMID: 8910496; http://dx.doi.org/10.1074/jbc.271.45.28636
10. Alam MR, Johnson RC, Darlington DN, Hand TA, Mains RE, Eipper BA. 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 1997; 272: 12667-75; PMID:9139723; http://dx.doi.org/10.1074/jbc.272.19.12667
11. Colomer V, Engelender S, Sharp AH, Duan K, Cooper JK, Lanahan A, et al. Huntingtin-associated protein 1 (HAP1) binds to a Trio-like polypeptide, with a rac1 guanine nucleotide exchange factor domain. Hum Mol Genet 1997; 6:1519-25; PMID:9285789; http://dx.doi.org/10.1093/hmg/6.9.1519
12. Portales-Casamar E, Briançon-Marjollet A, Fromont S, Triboulet R, Debant A. Identification of novel neuronal isoforms of the Rho-GEF Trio. Biol Cell 2006; 98:183-93; PMID:16033331; http://dx.doi.org/10.1042/BC20050009
13. McPherson CE, Eipper BA, Mains RE. Genomic organization and differential expression of Kalirin isoforms. Gene 2002; 284:41-51; PMID:11891045; http://dx.doi.org/10.1016/S0378-1119(02)00386-4
14. Sun YJ, Nishikawa K, Yuda H, Wang YL, Osaka H, Fukazawa N, et al. Solo/Trio8, a membrane-associated short isoform of Trio, modulates endosome dynamics and neurite elongation. Mol Cell Biol 2006; 26:6923-35; PMID:16943433; http://dx.doi.org/10.1128/MCB.02474-05
15. Yoshizuka N, Moriuchi R, Mori T, Yamada K, Hasegawa S, Maeda T, et al. An alternative transcript derived from the trio locus encodes a guanosine nucleotide exchange factor with mouse cell-transforming potential. J Biol Chem 2004; 279:43998-4004; PMID:15308664; http://dx.doi.org/10.1074/jbc.M406082200
16. van Rijssel J, Hoogenboezem M, Wester L, Hordijk PL, Van Buul JD. The N-terminal DH-PH domain of Trio induces cell spreading and migration by regulating lamellipodia dynamics in a Rac1-dependent fashion. PLoS One 2012; 7:e29912; PMID:22238672; http://dx.doi.org/10.1371/journal.pone.0029912
17. Abe K, Whitehead IP, O'Bryan JP, Der CJ. Involvement of NH(2)-terminal sequences in the negative regulation of Vav signaling and transforming activity. J Biol Chem 1999; 274:30410-8; PMID: 10521418; http://dx.doi.org/10.1074/jbc. 274.43.30410
18. Vanderzalm PJ, Pandey A, Hurwitz ME, Bloom L, Horvitz HR, Garriga G. C. elegans CARMIL negatively regulates UNC-73/Trio function during neuronal development. Development 2009; 136: 1201-10; PMID:19244282; http://dx.doi.org/ 10.1242/dev.026666
19. Lee CS, Choi CK, Shin EY, Schwartz MA, Kim EG. Myosin II directly binds and inhibits Dbl family guanine nucleotide exchange factors: a possible link to Rho family GTPases. J Cell Biol 2010; 190:663-74; PMID:20713598; http://dx.doi.org/10.1083/jcb.201003057
20. Yano T, Yamazaki Y, Adachi M, Okawa K, Fort P, Uji M, et al. Tara up-regulates E-cadherin transcription by binding to the Trio RhoGEF and inhibiting Rac signaling. J Cell Biol 2011; 193:319-32; PMID: 21482718; http://dx.doi.org/10.1083/jcb.201009100
21. Neubrand VE, Thomas C, Schmidt S, Debant A, Schiavo G. Kidins220/ARMS regulates Rac1-dependent neurite outgrowth by direct interaction with the RhoGEF Trio. J Cell Sci 2010; 123:2111-23; PMID: 20519585; http://dx.doi.org/10.1242/ jcs.064055
22. Bellanger JM, Astier C, Sardet C, Ohta Y, Stossel TP, Debant A. The Rac1- and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin. Nat Cell Biol 2000; 2:888-92; PMID:11146652; http://dx.doi.org/10.1038/ 35046533
23. Bellanger JM, Estrach S, Schmidt S, Briançon-Marjollet A, Zugasti O, Fromont S, et al. Different regulation of the Trio Dbl-Homology domains by their associated PH domains. Biol Cell 2003; 95:625-34; PMID:14720465; http://dx.doi.org/10.1016/j.biolcel.2003.10.002
24. Ohta Y, Suzuki N, Nakamura S, Hartwig JH, Stossel TP. The small GTPase RalA targets filamin to induce filopodia. Proc Natl Acad Sci U S A 1999; 96:2122-8; PMID:10051605; http://dx.doi.org/10.1073/pnas.96.5.2122
25. Jeon YJ, Choi JS, Lee JY, Yu KR, Ka SH, Cho Y, et al. Filamin B serves as a molecular scaffold for type I interferon-induced c-Jun NH2-terminal kinase signaling pathway. Mol Biol Cell 2008; 19:5116-30; PMID: 18815275; http://dx.doi.org/10.1091/mbc.E08-06-0576
26. Del Valle-Pérez B, Martínez VG, Lacasa-Salavert C, Figueras A, Shapiro SS, Takafuta T, et al. Filamin B plays a key role in vascular endothelial growth factor-induced endothelial cell motility through its interaction with Rac-1 and Vav-2. J Biol Chem 2010; 285:10748-60; PMID:20110358; http://dx.doi.org/10.1074/jbc.M109.062984
27. Rossman KL, Der CJ, Sondek J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 2005; 6:167-80; PMID:15688002; http://dx.doi.org/10.1038/nrm1587
28. Aravind L, Neuwald AF, Ponting CP. Sec14p-like domains in NF1 and Dbl-like proteins indicate lipid regulation of Ras and Rho signaling. Curr Biol 1999; 9: R195-7; PMID:10209105; http://dx.doi.org/10.1016/S0960-9822(99)80127-4
29. Bankaitis VA, Mousley CJ, Schaaf G. The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trends Biochem Sci 2010; 35:150-60; PMID:19926291; http://dx.doi.org/10.1016/j.tibs.2009.10.008
30. Mousley CJ, Tyeryar KR, Vincent-Pope P, Bankaitis VA. The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking. Biochim Biophys Acta 2007; 1771:727-36; PMID:17512778; http://dx.doi.org/10.1016/j.bbalip.2007.04.002
31. Kostenko EV, Mahon GM, Cheng L, Whitehead IP. The Sec14 homology domain regulates the cellular distribution and transforming activity of the Rho-specific guanine nucleotide exchange factor Dbs. J Biol Chem 2005; 280:2807-17; PMID:15531584; http://dx.doi.org/10.1074/jbc.M411139200
32. Djinovic-Carugo K, Gautel M, Ylänne J, Young P. The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett 2002; 513:119-23; PMID:11911890; http://dx.doi.org/10.1016/S0014-5793(01)03304-X
33. Xin X, Ferraro F, Bäck N, Eipper BA, Mains RE. Cdk5 and Trio modulate endocrine cell exocytosis. J Cell Sci 2004; 117:4739-48; PMID:15331630; http://dx.doi.org/10.1242/jcs.01333
34. Ciccotosto GD, Schiller MR, Eipper BA, Mains RE. Induction of integral membrane PAM expression in AtT-20 cells alters the storage and trafficking of POMC and PC1. J Cell Biol 1999; 144:459-71; PMID: 9971741; http://dx.doi.org/10. 1083/jcb.144.3.459
35. Alam MR, Steveson TC, Johnson RC, Bäck N, Abraham B, Mains RE, et al. Signaling mediated by the cytosolic domain of peptidylglycine alpha-amidating monooxygenase. Mol Biol Cell 2001; 12:629-44; PMID:11251076
36. Chen SY, Huang PH, Cheng HJ. Disrupted-in-Schizophrenia 1-mediated axon guidance involves TRIO-RAC-PAK small GTPase pathway signaling. Proc Natl Acad Sci U S A 2011; 108:5861-6; PMID: 21422296; http://dx.doi.org/10.1073/pnas. 1018128108
37. Estrach S, Schmidt S, Diriong S, Penna A, Blangy A, Fort P, et al. The Human Rho-GEF trio and its target GTPase RhoG are involved in the NGF pathway, leading to neurite outgrowth. Curr Biol 2002; 12:307-12; PMID:11864571; http://dx.doi.org/10.1016/S0960-9822(02)00658-9
38. Rojas RJ, Yohe ME, Gershburg S, Kawano T, Kozasa T, Sondek J. Galphaq directly activates p63RhoGEF and Trio via a conserved extension of the Dbl homology-associated pleckstrin homology domain. J Biol Chem 2007; 282:29201-10; PMID:17606614; http://dx.doi.org/10.1074/jbc.M703458200
39. Williams SL, Lutz S, Charlie NK, Vettel C, Ailion M, Coco C, et al. Trio 's Rho-specific GEF domain is the missing Galpha q effector in C. elegans. Genes Dev 2007; 21:2731-46; PMID:17942708; http://dx.doi.org/10.1101/gad.1592007
40. Kraynov VS, Chamberlain C, Bokoch GM, Schwartz MA, Slabaugh S, Hahn KM. Localized Rac activation dynamics visualized in living cells. Science 2000; 290: 333-7; PMID:11030651; http://dx.doi.org/10.1126/science.290.5490.333
41. Pertz O, Hodgson L, Klemke RL, Hahn KM. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 2006; 440:1069-72; PMID:16547516; http://dx.doi.org/10.1038/nature04665
42. Welch CM, Elliott H, Danuser G, Hahn KM. Imaging the coordination of multiple signalling activities in living cells. Nat Rev Mol Cell Biol 2011; 12:749-56; PMID:22016058; http://dx.doi.org/10.1038/nrm3212
43. Rabiner CA, Mains RE, Eipper BA. Kalirin: a dual Rho guanine nucleotide exchange factor that is so much more than the sum of its many parts. Neuroscientist 2005; 11:148-60; PMID:15746383; http://dx.doi.org/10.1177/ 1073858404271250
44. Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, et al. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 2003; 37:263-74; PMID:12546821; http://dx.doi.org/10.1016/S0896-6273(02)01168-6
45. Ratovitski EA, Alam MR, Quick RA, McMillan A, Bao C, Kozlovsky C, et al. Kalirin inhibition of inducible nitric-oxide synthase. J Biol Chem 1999; 274:993-9; PMID:9873042; http://dx.doi.org/10.1074/jbc.274.2.993
46. Steven R, Kubiseski TJ, Zheng H, Kulkarni S, Mancillas J, Ruiz Morales A, et al. UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell 1998; 92:785-95; PMID:9529254; http://dx.doi.org/10.1016/S0092-8674(00)81406-3
47. Awasaki T, Saito M, Sone M, Suzuki E, Sakai R, Ito K, et al. The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 2000; 26:119-31; PMID:10798397; http://dx.doi.org/10.1016/S0896-6273(00)81143-5
48. Bateman J, Shu H, Van Vactor D. The guanine nucleotide exchange factor trio mediates axonal development in the Drosophila embryo. Neuron 2000; 26:93-106; PMID:10798395; http://dx.doi.org/10.1016/S0896-6273(00)81141-1
49. Liebl EC, Forsthoefel DJ, Franco LS, Sample SH, Hess JE, Cowger JA, et al. Dosage-sensitive, reciprocal genetic interactions between the Abl tyrosine kinase and the putative GEF trio reveal trio's role in axon pathfinding. Neuron 2000; 26:107-18; PMID:10798396; http://dx.doi.org/10.1016/S0896-6273(00)81142-3
50. Newsome TP, Schmidt S, Dietzl G, Keleman K, Asling B, Debant A, et al. Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 2000; 101:283-94; PMID:10847683; http://dx.doi.org/10.1016/S0092-8674(00)80838-7
51. O'Brien SP, Seipel K, Medley QG, Bronson R, Segal R, Streuli M. Skeletal muscle deformity and neuronal disorder in Trio exchange factor-deficient mouse embryos. Proc Natl Acad Sci U S A 2000; 97:12074-8; PMID:11050238; http://dx.doi.org/10.1073/pnas. 97.22.12074
52. Forsthoefel DJ, Liebl EC, Kolodziej PA, Seeger MA. The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor Frazzled in Drosophila. Development 2005; 132:1983-94; PMID: 15790972; http://dx.doi.org/10. 1242/dev.01736
53. Briançon-Marjollet A, Ghogha A, Nawabi H, Triki I, Auziol C, Fromont S, et al. Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol Cell Biol 2008; 28:2314-23; PMID: 18212043; http://dx.doi.org/10.1128/MCB.00998-07
54. Peng YJ, He WQ, Tang J, Tao T, Chen C, Gao YQ, et al. Trio is a key guanine nucleotide exchange factor coordinating regulation of the migration and morphogenesis of granule cells in the developing cerebellum. J Biol Chem 2010; 285:24834-44; PMID:20516067; http://dx.doi.org/10.1074/jbc.M109.096537
55. Le Gall M, De Mattei C, Giniger E. Molecular separation of two signaling pathways for the receptor, Notch. Dev Biol 2008; 313:556-67; PMID:18062953; http://dx.doi.org/10.1016/j.ydbio.2007.10.030
56. Song JK, Giniger E. Noncanonical Notch function in motor axon guidance is mediated by Rac GTPase and the GEF1 domain of Trio. Dev Dyn 2011; 240:324-32; PMID:21246649; http://dx.doi.org/10.1002/dvdy.22525
57. Watari-Goshima N, Ogura K, Wolf FW, Goshima Y, Garriga G. C. elegans VAB-8 and UNC-73 regulate the SAX-3 receptor to direct cell and growth-cone migrations. Nat Neurosci 2007; 10:169-76; PMID: 17237778; http://dx.doi.org/10. 1038/nn1834
58. Charrasse S, Comunale F, Fortier M, Portales-Casamar E, Debant A, Gauthier-Rouvière C. M-cadherin activates Rac1 GTPase through the Rho-GEF trio during myoblast fusion. Mol Biol Cell 2007; 18:1734-43; PMID:17332503; http://dx.doi.org/10.1091/mbc.E06-08-0766
59. Bouquier N, Vignal E, Charrasse S, Weill M, Schmidt S, Léonetti JP, et al. A cell active chemical GEF inhibitor selectively targets the Trio/RhoG/Rac1 signaling pathway. Chem Biol 2009; 16:657-66; PMID: 19549603; http://dx.doi.org/10.1016/j.chembiol.2009.04.012
60. Jaffe AB, Hall A. Rho GTPases in transformation and metastasis. Adv Cancer Res 2002; 84:57-80; PMID: 11883532; http://dx.doi.org/10.1016/S0065- 230X(02)84003-9
61. Salhia B, Tran NL, Chan A, Wolf A, Nakada M, Rutka F, et al. The guanine nucleotide exchange factors trio, Ect2, and Vav3 mediate the invasive behavior of glioblastoma. Am J Pathol 2008; 173:1828-38; PMID: 19008376; http://dx.doi.org/10.2353/ajpath.2008.080043
62. Lane J, Martin TA, Mansel RE, Jiang WG. The expression and prognostic value of the guanine nucleotide exchange factors (GEFs) Trio, Vav1 and TIAM-1 in human breast cancer. Int Semin Surg Oncol 2008; 5:23; PMID:18925966; http://dx.doi.org/10.1186/1477-7800-5-23
63. Sosa MS, Lopez-Haber C, Yang C, Wang H, Lemmon MA, Busillo JM, et al. Identification of the Rac-GEF PRex1 as an essential mediator of ErbB signaling in breast cancer. Mol Cell 2010; 40:877-92; PMID: 21172654; http://dx.doi.org/ 10.1016/j.molcel.2010.11.029
64. Adamowicz M, Radlwimmer B, Rieker RJ, Mertens D, Schwarzbach M, Schraml P, et al. Frequent amplifications and abundant expression of TRIO, NKD2, and IRX2 in soft tissue sarcomas. Genes Chromosomes Cancer 2006; 45:829-38; PMID:16752383; http://dx.doi.org/10.1002/gcc.20343
65. Zheng M, Simon R, Mirlacher M, Maurer R, Gasser T, Forster T, et al. TRIO amplification and abundant mRNA expression is associated with invasive tumor growth and rapid tumor cell proliferation in urinary bladder cancer. Am J Pathol 2004; 165:63-9; PMID:15215162; http://dx.doi.org/10.1016/S0002-9440(10)63275-0
66. Yamada K, Moriuchi R, Mori T, Okazaki E, Kohno T, Nagayasu T, et al. Tgat, a Rho-specific guanine nucleotide exchange factor, activates NF-kappaB via physical association with IkappaB kinase complexes. Biochem Biophys Res Commun 2007; 355:269-74; PMID:17292329; http://dx.doi.org/10.1016/j.bbrc.2007.01.147
67. Bouquier N, Fromont S, Zeeh JC, Auziol C, Larrousse P, Robert B, et al. Aptamer-derived peptides as potent inhibitors of the oncogenic RhoGEF Tgat. Chem Biol 2009; 16:391-400; PMID:19389625; http://dx.doi.org/10.1016/j.chembiol. 2009.02.006