Semaphorin 4D/Plexin-B1-Mediated M-Ras GAP activity regulates actin-based dendrite remodeling through lamellipodin

Journal of Neuroscience

Volumn 32, Issue 24, 2012, Pages 8293-8305

  Tasaka, Gen Ichi ^a   Negishi, Manabu ^a   Oinuma, Izumi ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; EPITHELIAL NEUTROPHIL ACTIVATING FACTOR; F ACTIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; LAMELLIPODIN; PHOSPHOPROTEIN; PLEXIN; PLEXIN B1; RAP1 PROTEIN; RAS PROTEIN; SEMAPHORIN; SEMAPHORIN 4D; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DOWN REGULATION; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MICROTUBULE ASSEMBLY; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ANIMALS; ANTIGENS, CD; CARRIER PROTEINS; CEREBRAL CORTEX; CYTOSKELETON; DENDRITES; FEMALE; GENE KNOCKDOWN TECHNIQUES; GTPASE-ACTIVATING PROTEINS; HEK293 CELLS; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED ICR; NERVE TISSUE PROTEINS; NEURONS; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; RAS PROTEINS; RATS; RECEPTORS, CELL SURFACE; SEMAPHORINS; SIGNAL TRANSDUCTION;

EID: 84862249881     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0799-12.2012     Document Type: Article

References (45)

1. Adler CE, Fetter RD, Bargmann CI (2006) UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat Neurosci 9:511-518.
2. 2 and lamellipodin accumulation at the leading edge thus influencing motility of MDA-MB-231 cells. Proc Natl Acad Sci U S A 107:21547-21552.
3. Behar O, Golden JA, Mashimo H, Schoen FJ, Fishman MC (1996) Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383:525-528.
4. Chang C, Adler CE, Krause M, Clark SG, Gertler FB, Tessier-Lavigne M, Bargmann CI (2006) MIG-10/Lamellipodin and AGE-1/PI3K promote axon guidance and outgrowth in response to slit and netrin. Curr Biol 16:854-862.
5. Christensen CR, Klingelhöfer J, Tarabykina S, Hulgaard EF, Kramerov D, Lukanidin E (1998) Transcription of a novel mouse semaphorin gene, M-semaH, correlates with the metastatic ability of mouse tumor cell lines. Cancer Res 58:1238-1244.
6. Ehrhardt A, Ehrhardt GR, Guo X, Schrader JW (2002) Rasandrelatives-jobsharing and networking keep an old family together. Exp Hematol 30:1089-1106.
7. Hu H, Marton TF, Goodman CS (2001) Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32:39-51.
8. Hung RJ, Yazdani U, Yoon J, Wu H, Yang T, Gupta N, Huang Z, van Berkel WJ, Terman JR (2010) Mical links semaphorins to F-actin disassembly. Nature 463:823-827.
9. Hung RJ, Pak CW, Terman JR (2011) Direct redox regulation of F-actin assembly and disassembly by Mical. Science 334:1710-1713.
10. Ito Y, Oinuma I, Katoh H, Kaibuchi K, Negishi M (2006) Sema4D/ plexin-B1 activates GSK-3β through R-Ras GAP activity, inducing growth cone collapse. EMBO Rep 7:704-709.
11. Katoh H, Yasui H, Yamaguchi Y, Aoki J, Fujita H, Mori K, NegishiM (2000) Small GTPase RhoG is a key regulator for neurite outgrowth in PC12 cells. Mol Cell Biol 20:7378-7387.
12. Katoh H, Harada A, Mori K, Negishi M (2002) Socius is a novel Rnd GTPase-interacting protein involved in disassembly of actin stress fibers. Mol Cell Biol 22:2952-2964.
13. Kimmelman AC, Nuñez Rodriguez N, Chan AM (2002) R-Ras3/M-Ras induces neuronal differentiation of PC12 cells through cell-type-specific activation of the mitogen-activated protein kinase cascade. Mol Cell Biol 22:5946-5961.
14. Kolodkin AL, Matthes DJ, Goodman CS (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389-1399.
15. Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB (2003) Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 19:541-564.
16. Krause M, Leslie JD, Stewart M, Lafuente EM, Valderrama F, Jagannathan R, Strasser GA, Rubinson DA, Liu H, Way M, Yaffe MB, Boussiotis VA, Gertler FB (2004) Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev Cell 7:571-583.
17. Kumanogoh A, Kikutani H (2003) Immune semaphorins: a new area of semaphorin research. J Cell Sci 116:3463-3470.
18. Kwiatkowski AV, Rubinson DA, Dent EW, Edward van Veen J, Leslie JD, Zhang J, Mebane LM, Philippar U, Pinheiro EM, Burds AA, Bronson RT, Mori S, Fässler R, Gertler FB (2007) Ena/VASP Is Required for neuritogenesis in the developing cortex. Neuron 56:441-455.
19. Liu BP, Strittmatter SM (2001) Semaphorin-mediated axonal guidance via Rho-related G proteins. Curr Opin Cell Biol 13:619-626.
20. Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
21. Lyulcheva E, Taylor E, Michael M, Vehlow A, Tan S, Fletcher A, Krause M, Bennett D (2008) Drosophila pico and its mammalian ortholog lamellipodin activate serum response factor and promote cell proliferation. Dev Cell 15:680-690.
22. Michael M, Vehlow A, Navarro C, Krause M (2010) c-Abl, Lamellipodin, and Ena/VASP proteins cooperate in dorsal ruffling of fibroblasts and axonal morphogenesis. Curr Biol 20:783-791.
23. Oinuma I, Ishikawa Y, Katoh H, Negishi M (2004a) The semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 305:862-865.
24. Oinuma I, Katoh H, Negishi M (2004b) Molecular dissection of the semaphorin 4D receptor plexin-B1-stimulated R-Ras GTPase-activating protein activity and neurite remodeling in hippocampal neurons. J Neurosci 24:11473-11480.
25. Oinuma I, Katoh H, NegishiM (2006) Semaphorin 4D/Plexin-B1-mediated R-Ras GAP activity inhibits cell migration by regulating β1 integrin activity. J Cell Biol 173:601-613.
26. Oinuma I, Katoh H, Negishi M (2007) R-Ras controls axon specification upstream of glycogen synthase kinase-3β through integrin-linked kinase. J Biol Chem 282:303-318.
27. Oinuma I, Ito Y, Katoh H, Negishi M (2010) Semaphorin 4D/Plexin-B1 stimulates PTEN activity through R-Ras GTPase-activating protein activity, inducing growth cone collapse in hippocampal neurons. J Biol Chem 285:28200-28209.
28. Pinheiro EM, Xie Z, Norovich AL, Vidaki M, Tsai LH, Gertler FB (2011) Lpd depletion reveals that SRF specifies radial versus tangential migration of pyramidal neurons. Nat Cell Biol 13:989-995.
29. Quinn CC, Pfeil DS, Chen E, Stovall EL, Harden MV, Gavin MK, Forrester WC, Ryder EF, Soto MC, Wadsworth WG (2006) UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/ RIAM/Lamellipodin. Curr Biol 16:845-853.
30. Quinn CC, Pfeil DS, Wadsworth WG (2008) CED-10/Rac1 mediates axon guidance by regulating the asymmetric distribution of MIG-10/Lamellipodin. Curr Biol 18:808-813.
31. Saito T, Nakatsuji N (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240:237-246.
32. Saito Y, Oinuma I, Fujimoto S, Negishi M (2009) Plexin-B1 is a GTPase activating protein for M-Ras, remodelling dendrite morphology. EMBO Rep 10:614-621.
33. Salazar MA, Kwiatkowski AV, Pellegrini L, Cestra G, Butler MH, Rossman KL, Serna DM, Sondek J, Gertler FB, De Camilli P (2003) Tuba, a novel protein containing bin/amphiphysin/Rvs and Dbl homology domains, links dynamin to regulation of the actin cytoskeleton. J Biol Chem 278:49031-49043.
34. Self AJ, Hall A (1995) Purification of recombinant Rho/Rac/G25K from Escherichia coli. Methods Enzymol 256:3-10.
35. Smith K, Humphreys D, Hume PJ, Koronakis V (2010) Enteropathogenic Escherichia coli recruits the cellular inositol phosphatase SHIP2 to regulate actin-pedestal formation. Cell Host Microbe 7:13-24.
36. Sun P, Watanabe H, Takano K, Yokoyama T, Fujisawa J, Endo T (2006) Sustained activation of M-Ras induced by nerve growth factor is essential for neuronal differentiation of PC12 cells. Genes Cells 11:1097-1113.
37. Swiercz JM, Kuner R, Behrens J, Offermanns S (2002) Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35:51-63.
38. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M, Tessier-Lavigne M, Comoglio PM (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80.
39. Terman JR, Mao T, Pasterkamp RJ, Yu HH, Kolodkin AL (2002) MICALs, a family of conserved flavoprotein oxidoreductases, function in plexinmediated axonal repulsion. Cell 109:887-900.
40. Toyofuku T, Yoshida J, Sugimoto T, Zhang H, Kumanogoh A, Hori M, Kikutani H (2005) FARP2 triggers signals for Sema3A-mediated axonal repulsion. Nat Neurosci 8:1712-1719.
41. Uesugi K, Oinuma I, Katoh H, NegishiM (2009) Different requirement for Rnd GTPases of R-Ras GAP activity of Plexin-C1 and Plexin-D1. J Biol Chem 284:6743-6751.
42. Vikis HG, Li W, Guan KL (2002) The plexin-B1/Rac interaction inhibitsPAKactivation and enhances Sema4D ligand binding. Genes Dev 16:836-845.
43. Wang Y, He H, Srivastava N, Vikarunnessa S, Chen YB, Jiang J, Cowan CW, Zhang X (2012) Plexins are GTPase-activating proteins for Rap and are activated by induced dimerization. Sci Signal 5:ra6.
44. Whitford KL, Ghosh A (2001) Plexin signaling via off-track and rho family GTPases. Neuron 32:1-3.
45. Worzfeld T, Püschel AW, Offermanns S, Kuner R (2004) Plexin-B family members demonstrate nonredundant expression patterns in the developing mouse nervous system: an anatomical basis for morphogenetic effects of Sema4D during development. Eur J Neurosci 19:2622-2632.