The small GTPase Rac is involved in clustering of hippocampal neurons and fasciculation of their neurites

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 370, Issue 3, 2004, Pages 211-222

  Leemhuis, J ^a   Mayer, U ^a   Barth, H ^a   Schmidt, G ^a   Meyer, D K ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Cytotoxic necrotizing factor 1; Lethal toxin; N methyl D aspartate; Neuronal bundling; Neuronal clustering; PI3 kinase; Rac1

Indexed keywords

2 METHYL 1 [(4 METHYL 5 ISOQUINOLINE)SULFONYL]HOMOPIPERAZINE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CYTOTOXIC NECROTIZING FACTOR 1; DIZOCILPINE; GLUTAMATE RECEPTOR AGONIST; GUANOSINE TRIPHOSPHATASE; H 1152; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE METHYL ESTER; N METHYL DEXTRO ASPARTIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE INHIBITOR; RAC PROTEIN; RHO KINASE INHIBITOR; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CELL MIGRATION; CLOSTRIDIUM SORDELLII; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME MECHANISM; FARNESYLATION; FASCICULATION; HIPPOCAMPUS; INHIBITION KINETICS; MICROSCOPY; NERVE CELL; NEWBORN; NONHUMAN; PERIKARYON; PERINATAL DEVELOPMENT; RAT; REACTION ANALYSIS; TIME LAPSE MICROSCOPY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMIDES; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; DRUG INTERACTIONS; ENZYME ACTIVATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; GTP PHOSPHOHYDROLASES; HIPPOCAMPUS; N-METHYLASPARTATE; NEURITES; NEURONS; PYRIDINES; RAC1 GTP-BINDING PROTEIN; RATS; RATS, WISTAR; TRANSFECTION;

EID: 5444269191     PISSN: 00281298     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00210-004-0965-y     Document Type: Article

References (73)

1. Allen WE, Zicha D, Ridley AJ, Jones GE (1998) A role for Cdc42 in macrophage chemotaxis. J Cell Biol 141:1147-1157
2. Arcaro A, Wymann MP (1993) Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem J 296:297-301
3. Atwal JK, Massie B, Miller FD, Kaplan DR (2000) The TrkB-Shc site signals neuronal survival and local axon growth via MEK and PI3-kinase. Neuron 27:265-277
4. Baldacini O, Green GA, Girardot R, Rihn B, Monteil H (1990) Fast purification of Clostridium sordellii cytotoxin. J Chromatogr 528:357-369
5. Balla T, Bondeva T, Varnai P (2000) How accurately can we image inositol lipids in living cells? Trends Pharmacol Sci 21:238-241
6. Banyard J, Anand-Apte B, Symons M, Zetter BR (2000) Motility and invasion are differentially modulated by Rho family GTPases. Oncogene 19:580-591
7. Bar-Sagi D, Hall A (2000) Ras and Rho GTPases: a family reunion. Cell 103:227-238
8. Barth H, Hofmann F, Olenik C, Just I, Aktories K (1998) The N-terminal part of the enzyme component (C2I) of the binary Clostridium botulinum C2 toxin interacts with the binding component C2II and functions as a carrier system for a Rho ADP-ribosylating C3-like fusion toxin. Infect Immun 66:1364-1369
9. Barth H, Olenik C, Sehr P, Schmidt G, Aktories K, Meyer DK (1999) Neosynthesis and activation of Rho by Escherichia coli cytotoxic necrotizing factor (CNF1) reverse cytopathic effects of ADP-ribosylated Rho. J Biol Chem 274:27407-27414
10. Benard V, Bohl BP, Bokoch GM (1999) Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J Biol Chem 274:13198-13204
11. + channels in neonatal rat hippocampal neurons. J Membr Biol 161:275-286
12. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576
13. Brock C, Schaefer M, Reusch HP, Czupalla C, Michalke M, Spicher K, Schultz G, Nurnberg B (2003) Roles of G beta gamma in membrane recruitment and activation of p110 gamma/p101 phosphoinositide 3-kinase gamma. J Cell Biol 160:89-99
14. Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296:1655-1657
15. Davies SP, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105
16. Diekmann D, Nobes CD, Burbelo PD, Abo A, Hall A (1995) Rac GTPase interacts with GAPs and target proteins through multiple effector sites. EMBO J 14:5297-5305
17. Doye A, Mettouchi A, Bossis G, Clement R, Buisson-Touati C, Flatau G, Gagnoux L, Piechaczyk M, Boquet P, Lemichez E (2002) CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 111:553-564
18. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629-635
19. Flatau G, Lemichez E, Gauthier M, Chardin P, Paris S, Fiorentini C, Boquet P (1997) Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387:729-733
20. Fukata Y, Oshiro N, Kinoshita N, Kawano Y, Matsuoka Y, Bennett V, Matsuura Y, Kaibuchi K (1999) Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J Cell Biol 145:347-361
21. Hofmann F, Rex G, Aktories K, Just I (1996) The ras-related protein Ra1 is monoglucosylated by Clostridium sordellii lethal toxin. Biochem Biophys Res Commun 227:77-81
22. Ikenoya M, Hidaka H, Hosoya T, Suzuki M, Yamamoto N, Sasaki Y (2002) Inhibition of rho-kinase-induced myristoylated alanine-rich C kinase substrate (MARCKS) phosphorylation in human neuronal cells by H-1152, a novel and specific Rho-kinase inhibitor. J Neurochem 81:9-16
23. Just I, Selzer J, Hofmann F, Green GA, Aktories K (1996) Inactivation of Ras by Clostridium sordellii lethal toxin-catalyzed glucosylation. J Biol Chem 271:10149-10153
24. Köhrmann M, Haubensak W, Hemraj I, Kaether C, Lessmann VJ, Kiebler MA (1999) Fast, convenient, and effective method to transiently transfect primary hippocampal neurons. J Neurosci Res 58:831-835
25. Kwong L, Wozniak MA, Collins AS, Wilson SD, Keely PJ (2003) R-Ras promotes focal adhesion formation through focal adhesion kinase and p130(Cas) by a novel mechanism that differs from integrins. Mol Cell Biol 23:933-949
26. Leemhuis J, Boutillier S, Schmidt G, Meyer DK (2002) The protein kinase A inhibitor H89 acts on cell morphology by inhibiting Rho kinase. J Pharmacol Exp Ther 300:1000-1007
27. Leemhuis J, Boutillier S, Barth H, Feuerstein TJ, Brock C, Nurnberg B, Aktories K, Meyer DK (2004) Rho GTPases and phosphoinositide 3-kinase organize formation of branched dendrites. J Biol Chem 279:585-596
28. Leopoldt D, Hanck T, Exner T, Maier U, Wetzker R, Nurnberg B (1998) Gbetagamma stimulates phosphoinositide 3-kinase-gamma by direct interaction with two domains of the catalytic p110 subunit. J Biol Chem 273:7024-7029
29. Lerm M, Pop M, Fritz G, Aktories K, Schmidt G (2002) Proteasomal degradation of cytotoxic necrotizing factor 1-activated rac. Infect Immun 70:4053-4058
30. Lerner EC, Qian Y, Blaskovich MA, Fossum RD, Vogt A, Sun J, Cox AD, Der CJ, Hamilton AD, Sebti SM (1995) Ras CAAX peptidomimetic FTI-277 selectively blocks oncogenic Ras signaling by inducing cytoplasmic accumulation of inactive Ras-Raf complexes. J Biol Chem 270:26802-26806
31. Lerner EC, Zhang TT, Knowles DB, Qian Y, Hamilton AD, Sebti SM (1997) Inhibition of the prenylation of K-Ras, but not H- or N-Ras, is highly resistant to CAAX peptidomimetics and requires both a farnesyltransferase and a geranylgeranyltransferase I inhibitor in human tumor cell lines. Oncogene 15:1283-1288
32. Li Z, Aizenman CD, Cline HT (2002) Regulation of rho GTPases by crosstalk and neuronal activity in vivo. Neuron 33:741-750
33. Maier U, Babich A, Nurnberg B (1999) Roles of non-catalytic subunits in gbetagamma-induced activation of class I phosphoinositide 3-kinase isoforms beta and gamma. J Biol Chem 274:29311-29317
34. Marin O, Rubenstein JL (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790
35. Markus A, Zhong J, Snider WD (2002) Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35:65-76
36. Nadarajah B, Parnavelas JG (2002) Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423-432
37. Nadarajah B, Alifragis P, Wong RO, Parnavelas JG (2003) Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb Cortex 13:607-611
38. Nishiyama T, Sasaki T, Takaishi K, Kato M, Yaku H, Araki K, Matsuura Y, Takai Y (1994) Rac p21 is involved in insulin-induced membrane ruffling and rho p21 is involved in hepatocyte growth factor- and 12-O-tetradecanoylphorbol-13- acetate (TPA)-induced membrane ruffling in KB cells. Mol Cell Biol 14:2447-2456
39. Nobes CD, Hall A (1995) Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62
40. Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235-1244
41. Piekorz RP, Nürnberg B (2004) Phospholipid kinases In: Enna SJ, Bylund (eds) X-Pharm. Elsevier, New York
42. Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JL (2000) Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740
43. Polleux F, Whitford KL, Dijkhuizen PA, Vitalis T, Ghosh A (2002) Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129:3147-3160
44. Popoff MR, Chaves-Olarte E, Lemichez E, Eichel-Streiber C, Thelestam M, Chardin P, Cussac D, Antonny B, Chavrier P, Flatau G, Giry M, de Gunzburg J, Boquet P (1996) Ras, Rap, and Rac small GTP-binding proteins are targets for Clostridium sordellii lethal toxin glucosylation. J Biol Chem 271:10217-10224
45. Price LS, Hajdo-Milasinovic A, Zhao J, Zwartkruis FJ, Collard JG, Bos JL (2004) Rap1 regulates E-cadherin-mediated cell-cell adhesion. J Biol Chem published online http://dx.doi.org//10.1074/jbc.M404917200 May 2004
46. Puglianiello A, Germani D, Rossi P, Cianfarani S (2000) IGF-I stimulates chemotaxis of human neuroblasts. Involvement of type 1 IGF receptor, IGF binding proteins, phosphatidylinositol-3 kinase pathway and plasmin system. J Endocrinol 165:123-131
47. Rameh LE, Cantley LC (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 274:8347-8350
48. Ridley AJ, Comoglio PM, Hall A (1995) Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol Cell Biol 15:1110-1122
49. Sarner S, Kozma R, Ahmed S, Lim L (2000) Phosphatidylinositol 3-kinase, Cdc42, and Rac1 act downstream of Ras in integrin-dependent neurite outgrowth in N1E-115 neuroblastoma cells. Mol Cell Biol 20:158-172
50. Sasaki Y, Suzuki M, Hidaka H (2002) The novel and specific Rho-kinase inhibitor (S)-(+)-2-methyl-1-[(4-methyl-5-isoquinoline) sulfonyl]-homopiperazine as a probing molecule for Rho-kinase-involved pathway. Pharmacol Ther 93:225-232
51. Satoh K, Ichihara K, Landon EJ, Inagami T, Tang H (2001) 3-Hydroxy-3-methylglutaryl-CoA reductase inhibitors block calcium-dependent tyrosine kinase Pyk2 activation by angiotensin II in vascular endothelial cells. Involvement of geranylgeranylation of small G protein Rap1. J Biol Chem 276:15761-15767
52. Schmidt G, Sehr P, Wilm M, Selzer J, Mann M, Aktories K (1997) Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387:725-729
53. Shaw LM, Rabinovitz I, Wang HH, Toker A, Mercurio AM (1997) Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion. Cell 91:949-960
54. Spaargaren M, Bos JL (1999) Rab5 induces Rac-independent lamellipodia formation and cell migration. Mol Biol Cell 10:3239-3250
55. Stoyanova S, Bulgarelli-Leva G, Kirsch C, Hanck T, Klinger R, Wetzker R, Wymann MP (1997) Lipid kinase and protein kinase activities of G-protein-coupled phosphoinositide 3-kinase gamma: structure-activity analysis and interactions with wortmannin. Biochem J 324:489-495
56. Takai Y, Sasaki T, Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81:153-208
57. Takaishi K, Kikuchi A, Kuroda S, Kotani K, Sasaki T, Takai Y (1993) Involvement of rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in cell motility. Mol Cell Biol 13:72-79
58. Tsuji T, Ishizaki T, Okamoto M, Higashida C, Kimura K, Furuyashiki T, Arakawa Y, Birge RB, Nakamoto T, Hirai H, Narumiya S (2002) ROCK and mDial antagonize in Rho-dependent Rac activation in Swiss 3T3 fibroblasts. J Cell Biol 157:819-830
59. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389:990-994
60. Vanhaesebroeck B, Waterfield MD (1999) Signaling by distinct classes of phosphoinositide 3-kinases. Exp Cell Res 253:239-254
61. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70:535-602
62. Vlahos CJ, Matter WF, Hui KY, Brown RF (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269:5241-5248
63. Von Kügelgen I, Nörenberg W, Illes P, Schobert A, Starke K (1997) Differences in the mode of stimulation of cultured rat sympathetic neurons between ATP and UDP. Neuroscience 78:935-941
64. Wang F, Herzmark P, Weiner OD, Srinivasan S, Servant G, Bourne HR (2002) Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat Cell Biol 4:513-518
65. Weiner OD, Neilsen PO, Prestwich GD, Kirschner MW, Cantley LC, Bourne HR (2002) A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat Cell Biol 4:509-513
66. Wilde C, Aktories K (2001) The Rho-ADP-ribosylating C3 exoenzyme from Clostridium botulinum and related C3-like transferases. Toxicon 39:1647-1660
67. Yamaguchi Y, Katoh H, Yasui H, Mori K, Negishi M (2001) Rho A inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J Biol Chem 276:18977-18983
68. Yang H, Shaw G, Raizada MK (2002) ANG II stimulation of neuritogenesis involves protein kinase B in brain neurons. Am J Physiol Regul Integr Comp Physiol 283:R107-R114
69. Zhang FL, Casey PJ (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 65:241-269
70. Zhang Z, Vuori K, Wang H, Reed JC, Ruoslahti E (1996) Integrin activation by R-ras. Cell 85:61-69
71. Zheng Y, Bagrodia S, Cerione RA (1994) Activation of phosphoinositide 3-kinase activity by Cdc42Hs binding to p85. J Biol Chem 269:18727-18730
72. Zou JX, Wang B, Kalo MS, Zisch AH, Pasquale EB, Ruoslahti E (1999) An Eph receptor regulates integrin activity through R-Ras. Proc Natl Acad Sci USA 96:13813-13818
73. Zou JX, Liu Y, Pasquale EB, Ruoslahti E (2002) Activated SRC oncogene phosphorylates R-ras and suppresses integrin activity. J Biol Chem 277:1824-1827