Inactivation of Ras by p120GAP via focal adhesion kinase dephosphorylation mediates RGMa-induced growth cone collapse

Journal of Neuroscience

Volumn 29, Issue 20, 2009, Pages 6649-6662

  Endo, Mitsuharu ^a,b   Yamashita, Toshihide ^a,c  

^a OSAKA UNIVERSITY   (Japan)

^b KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HEMOJUVELIN; NEOGENIN; PROTEIN KINASE B; PROTEIN SH2; RAS PROTEIN; TYROSINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL STIMULATION; CELL STRAIN HEK293; CHO CELL; CONTROLLED STUDY; DISSOCIATION; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GROWTH CONE; GROWTH INHIBITION; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES; CELLS, CULTURED; CEREBRAL CORTEX; CRICETINAE; CRICETULUS; EMBRYO, MAMMALIAN; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GREEN FLUORESCENT PROTEINS; GROWTH CONES; HUMANS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURITES; NEURONS; P120 GTPASE ACTIVATING PROTEIN; PHOSPHORYLATION; RATS; RATS, WISTAR; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TIME FACTORS; TRANSFECTION; TYROSINE;

EID: 66249092433     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0927-09.2009     Document Type: Article

References (41)

1. Boguski MS, McCormick F ( 1993) Proteins regulating Ras and its relatives. Nature 366:643-654. (Pubitemid 24036012)
2. Brinks H, Conrad S, Vogt J, Oldekamp J, Sierra A, Deitinghoff L, Bechmann I, Alvarez-Bolado G, Heimrich B, Monnier PP, Mueller BK, Skutella T (2004) The repulsive guidance molecule RGMa is involved in the formation of afferent connections in the dentate gyrus. J Neurosci 24:3862-3869. (Pubitemid 38509416)
3. Brouns MR, Matheson SF, Settleman J (2001) p 190 RhoGAP is the principal Src substrate in brain and regulates axon outgrowth, guidance and fasciculation. Nat Cell Biol 3:361-367.
4. Calalb MB, Zhang X, Polte TR, Hanks SK (1996) Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem Biophys Res Commun 228:662-668. (Pubitemid 26421437)
5. Conrad S, Genth H, Hofmann F, Just I, Skutella T (2007) Neogenin-RGMa signaling at the growth cone is bone morphogenetic protein-independent and involves RhoA, ROCK, and PKC. J Biol Chem 7:784-792.
6. Dail M, Richter M, Godement P, Pasquale EB (2006) Eph receptors inactivate R-Ras through different mechanisms to achieve cell repulsion. J Cell Sci 119:1244-1254. (Pubitemid 43756542)
7. 2+-dependent membrane-binding proteins. Evidence for a direct interaction between annexin VI and P120GAP. J Biol Chem 271:24333-24336.
8. Elowe S, Holland SJ, Kulkami S, Pawson T (2001) Downregulation of the Ras-mitogen-activated protein kinase pathway by the EphB2 receptor tyrosine kinase is required for ephrin-induced neurite retraction. Mol Cell Biol 21:7429-7441. (Pubitemid 32953493)
9. Fivaz M, Bandara S, Inoue T, Meyer T (2008) Robust neuronal symmetry breaking by Ras-triggered local positive feedback. Curr Biol 18:44-50.
10. Grewal T, Enrich C (2006) Molecular mechanisms involved in Ras inactivation: the annexin A6-pl20GAP complex. Bioessays 28:1211-1220.
11. Grewal T, Evans R, Rentero C, Tebar F, Cubells L, de Diego I, Kirchhoff MF, Hughes WE, Heeren J, Rye KA, Rinninger F, Daly RJ, Pol A, Enrich C (2005) Annexin A6 stimulates the membrane recruitment of pl20GAP to modulate Ras and Raf-1 activity. Oncogene 24:5809-5820. (Pubitemid 43080072)
12. Hata K, Fujitani M, Yasuda Y, Doya H, Saito T, Yamagishi S, Mueller BK, Yamashita T (2006) RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J Cell Biol 173:47-58.
13. Hecker TP, Ding Q, Rege TA, Hanks SK, Gladson CL (2004) Overexpression of FAK promotes Ras activity through the formation of a FAK/ pl20RasGAP complex in malignant astrocytoma cells. Oncogene 23:3962-3971. (Pubitemid 38747924)
14. Iwashita S, Song SY (2008) RasGAPs: a crucial regulator of extracellular stimuli for homeostasis of cellular functions. Mol Biosyst 4:213-222.
15. Kang JS, Yi MJ, Zhang W, Feinleib JL, Cole F, Krauss RS (2004) Netrins and neogenin promote myotube formation. J Cell Biol 167:493-504. (Pubitemid 39489057)
16. Kubo T, Endo M, Hata K, Taniguchi J, Kitajo K, Tomura S, Yamaguchi A, Mueller BK, Yamashita T (2008) Myosin IIA is required for neurite outgrowth inhibition produced by repulsive guidance molecule. J Neurochem 105:113-126.
17. Kunath T, Gish G, Lickert H, Jones N, Pawson T, Rossant J (2003) Transgenic RNA interference in ES cell-derived embryos recapitulates a genetic null phenotype. Nat Biotechnol 21:559-561. (Pubitemid 36532022)
18. Li S, Nakamura S, Hattori S (1997) Activation ofR-Ras GTPase by GTPaseactivating proteins for Ras, Gapl(m), and pl20GAP. J Biol Chem 272:19328-19332.
19. Lowy DR, Zhang K,DeClue JE,Willumsen BM (1991) Regulation of p21ras activity. Trends Genet 7:346-351.
20. MafiesS,MiraE,Gómez-MoutonC,ZhaoZJ,LacalleRA,Martínez- AC(1999)ConcertedactivityoftyrosinephosphataseSHP- 2andfocaladhesionkinaseinregulationofcellmotility.MolCellBiol19:3125-3135. (Pubitemid29144557)
21. MarshallMS,HillWS,NgAS,VogelUS,SchaberMD,ScolnickEM,DixonRA,SigalIS, GibbsJB(1989)AC-terminaldomainofGAPissufficient-stimulaterasp21GTPaseactivity. EMBOJ8:1105-1110.(Pubitemid19273277)
22. MarteBM,Rodriguez-VicianaP,WennströmS,WarnePH,DownwardJ(1997) R-Rascanactivatethephosphoinositide3- kinasebutnottheMAPkinasearmoftheRaseffectorpathways.CurrBiol7:63-70. (Pubitemid27058941)
23. McGladeJ,BrunkhorstB,AndersonD,MbamaluG,SettlemanJ,DedharS, Rozakis-AdcockM,ChenLB,PawsonT(1993)TheN- terminalregionofGAPregulatescytoskeletalstructureandcelladhesion.EMBOJ12: 3073-3081.(Pubitemid23232738)
24. Monnier PP, Sierra A, Macchi P, Deitinghoff L, Andersen JS, Mann M, Fiad M, Hornberger MR, Stahl B, Bonhoeffer F, Mueller BK (2002) RGM is a repulsive guidance molecule for retinal axons. Nature 419:392-395.
25. MoranMF,PolakisP,McCormickF,PawsonT,EllisC(1991) Proteintyrosinekinasesregulatethephosphorylation,proteininteractions, subcellulardistribution,andactivityofp2IrasGTPase-activatingprotein. MoICellBiol11:1804-1812.(Pubitemid21895546)
26. Ohshima Y, Kubo T, Koyama R, Ueno M, Nakagawa M, Yamashita T (2008) Regulation of axonal elongation and pathfinding from the entorhinal cortex to the dentate gyrus in the hippocampus by the chemokine stromal cell-derived factor 1 alpha. J Neurosci 28:8344-8353.
27. Oinuma I, Ishikawa Y, Katoh H, Negishi M (2004) The Semaphorin 4D receptor Plexin-Bl is a GTPase activating protein for R-Ras. Science 305:862-865. (Pubitemid 39038420)
28. Oinuma I, Katoh H, Negishi M (2007) R-Ras controls axon specification upstream of glycogen synthase kinase-3beta through integrin-linked kinase. J Biol Chem 282:303-318. (Pubitemid 47076649)
29. Pawson T, Gish GD, Nash P (2001) SH2 domains, interaction modules and cellular wiring. Trends Cell Biol 11:504-511. (Pubitemid 33079144)
30. Rafiq K, Kolpakov MA, Abdelfettah M, Streblow DN, Hassid A, Dell'Italia LJ, SabriA (2006) Role of protein-tyrosine phosphatase SHP2 in focal adhesion kinase down-regulation during neutrophil cathepsin G-induced cardiomyocytes anoikis. J Biol Chem 281:19781-19792.
31. Rajagopalan S, Deitinghoff L, Davis D, Conrad S, Skutella T, Chedotal A, Mueller BK, Strittmatter SM (2004) Neogenin mediates the action of repulsive guidance molecule. Nat Cell Biol 6:756-762. (Pubitemid 39144481)
32. Ren XR, Ming GL, Xie Y, Hong Y, Sun DM, Zhao ZQ, Feng Z, Wang Q, Shim S, Chen ZF, Song HJ, Mei L, Xiong WC (2004) Focal adhesion kinase in netrin-1 signaling. Nat Neurosci 7:1204-1212. (Pubitemid 39426240)
33. Ren XR, Hong Y, Feng Z, Yang HM, Mei L, Xiong WC (2008) Tyrosine phosphorylation of netrin receptors in netrin-1 signaling. Neurosignals 16:235-245.
34. ReyI,Taylor-HarrisP,vanErpH,HallA(1994)R-rasinteractswithrasGAP, neurofibrominandc-rafbutdoesnotregulatecellgrowthordifferentiation.Oncogene9: 685-692.(Pubitemid24065905)
35. Serpente N, Birling MC, Price J (1996) The regulation of the expression, phosphorylation, and protein associations of ppl25FAK during rat brain development. MoI Cell Neurosci 7:391-403. (Pubitemid 26250827)
36. Settleman J, Albright CF, Foster LC, Weinberg RA (1992) Association between GTPase activators for Rho and Ras families. Nature 359:153-154.
37. TraheyM,McCormickF(1987)AcytoplasmicproteinstimulatesnormalN- rasp21GTPase,butdoesnotaffectoncogenicmutants.Science238:542-545. (Pubitemid17147042)
38. Yoshida J, Kubo T, Yamashita T (2008) Inhibition of branching and spine maturation by repulsive guidance molecule in cultured cortical neurons. Biochem Biophys Res Commun 372:725-729.
39. Yoshimura T, Arimura N, Kawano Y, Kawabata S, Wang S, Kaibuchi K (2006) Ras regulates neuronal polarity via the PI3-kinase/Akt/ GSK-3beta/CRMP-2 pathway. Biochem Biophys Res Commun 340:62-68. (Pubitemid 41827648)
40. YueY, LypowyJ, Hedhli N, Abdellatif M (2004) Ras GTPase-activating protein binds to Akt and is required for its activation. J Biol Chem 279:12883-12889. (Pubitemid 38445863)
41. Zheng Y, Quilliam LA (2003) Activation of the Ras superfamily of small GTPases. EMBO Rep 4:463-468.