Altered adhesive structures and their relation to RhoGTPase activation in merlin-deficient Schwannoma

Brain Pathology

Volumn 19, Issue 1, 2009, Pages 27-38

  Flaiz, Christine ^a   Ammoun, Sylwia ^a   Biebl, Anja ^b   Hanemann, C Oliver ^a,c  

^a PENINSULA MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF ULM   (Germany)

^c PLYMOUTH UNIVERSITY PENINSULA SCHOOLS OF MEDICINE AND DENTISTRY   (United Kingdom)

Author keywords

Adhesion; Focal contacts; GTPases; Merlin; Neurofibromatosis; Schwannoma

Indexed keywords

BETA1 INTEGRIN; FOCAL ADHESION KINASE; MERLIN; PAXILLIN; PROTEIN BETA PIX; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; NEURILEMOMA; NEUROFIBROMATOSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SCHWANN CELL; SIGNAL TRANSDUCTION;

ACTINS; ADENOVIRIDAE; AMIDES; CELLS, CULTURED; ENZYME INHIBITORS; FOCAL ADHESIONS; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEURILEMMOMA; NEUROFIBROMIN 2; PAXILLIN; PEPTIDES; PYRIDINES; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SCHWANN CELLS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 57449097854     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2008.00165.x     Document Type: Article

References (54)

1. Beckerle MC (1997) Zyxin: zinc fingers at sites of cell adhesion. Bioessays 11 : 949 957.
2. Benninger Y, Thurnherr T, Pereira JA, Krause S, Wu X, Chrostek-Grashoff A et al (2007) Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J Cell Biol 6 : 1051 1061.
3. Bershadsky AD, Ballestrem C, Carramusa L, Zilberman Y, Gilquin B, Khochbin S et al (2006) Assembly and mechanosensory function of focal adhesions: experiments and models. Eur J Cell Biol 3-4 : 165 173.
4. Burridge K, Chrzanowska-Wodnicka M (1996) Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 12 : 463 518.
5. Burridge K, Wennerberg K (2004) Rho and Rac take center stage. Cell 2 : 167 179.
6. del Pozo MA, Price LS, Alderson NB, Ren XD, Schwartz MA (2000) Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J 9 : 2008 2014.
7. del Pozo MA, Kiosses WB, Alderson NB, Meller N, Hahn KM, Schwartz MA (2002) Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat Cell Biol 3 : 232 239.
8. DeMali KA, Burridge K (2003) Coupling membrane protrusion and cell adhesion. J Cell Sci 116 (Pt 12 2389 2397.
9. Dickersin GR (1987) The electron microscopic spectrum of nerve sheath tumors. Ultrastruct Pathol 2-3 : 103 146.
10. Fernandez-Valle C, Tang Y, Ricard J, Rodenas-Ruano A, Taylor A, Hackler E et al (2002) Paxillin binds schwannomin and regulates its density-dependent localization and effect on cell morphology. Nat Genet 4 : 354 362.
11. Flaiz C, Kaempchen K, Matthies C, Hanemann CO (2007) Actin-rich protrusions and nonlocalized GTPase activation in merlin-deficient Schwannomas. J Neuropathol Exp Neurol 7 : 608 616.
12. Flaiz C, Utermark T, Parkinson DB, Poetsch A, Hanemann CO (2008) Impaired intercellular adhesion and immature adherens junctions in merlin-deficient human primary schwannoma cells. Glia 56 : 506 515.
13. Hall A (1994) Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu Rev Cell Biol 10 : 31 54.
14. Hanemann CO, Evans DG (2006) News on the genetics, epidemiology medical care and translational research of Schwannomas. J Neurol 12 : 1533 1541.
15. Hirokawa Y, Tikoo A, Huynh J, Utermark T, Hanemann CO, Giovannini M et al (2004) A clue to the therapy of neurofibromatosis type 2: NF2/merlin is a PAK1 inhibitor. Cancer J 1 : 20 26.
16. Hotchin NA, Hall A (1995) The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J Cell Biol 6 : 1857 1865.
17. James MF, Beauchamp RL, Manchanda N, Kazlauskas A, Ramesh V (2004) A NHERF binding site links the betaPDGFR to the cytoskeleton and regulates cell spreading and migration. J Cell Sci Pt 14 : 2951 2961.
18. James MF, Lelke JM, MacCollin M, Plotkin SR, Stemmer-Rachamimov AO, Ramesh V et al (2008) Modeling NF2 with human arachnoidal and meningioma cell culture systems: NF2 silencing reflects the benign character of tumor growth. Neurobiol Dis 29 : 278 292.
19. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 9 : 671 682.
20. Kaempchen K, Mielke K, Utermark T, Langmesser S, Hanemann CO (2003) Upregulation of the Rac1/JNK signaling pathway in primary human Schwannoma cells. Hum Mol Genet 11 : 1211 1221.
21. Kaverina I, Krylyshkina O, Small JV (2002) Regulation of substrate adhesion dynamics during cell motility. Int J Biochem Cell Biol 7 : 746 761.
22. Kissil JL, Wilker EW, Johnson KC, Eckman MS, Yaffe MB, Jacks T (2003) Merlin, the product of the Nf2 tumor suppressor gene, is an inhibitor of the p21-activated kinase, Pak1. Mol Cell 4 : 841 849.
23. Lallemand D, Curto M, Saotome I, Giovannini M, McClatchey AI (2003) NF2 deficiency promotes tumorigenesis and metastasis by destabilizing adherens junctions. Genes Dev 17 : 1090 1100.
24. Manser E, Loo TH, Koh CG, Zhao ZS, Chen XQ, Tan L et al (1998) PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol Cell 2 : 183 192.
25. Maruta H, He H, Tikoo A, Nur-e-Kamal M (1999) Cytoskeletal tumor suppressors that block oncogenic RAS signaling. Ann N Y Acad Sci 886 : 48 57.
26. Maruta H, Nheu TV, He H, Hirokawa Y (2003) Rho family-associated kinases PAK1 and rock. Prog Cell Cycle Res 5 : 203 210.
27. McClatchey AI, Saotome I, Mercer K, Crowley D, Gusella JF, Bronson RT et al (1998) Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly metastatic tumors. Gene Dev 8 : 1121 1133.
28. Melendez-Vasquez CV, Einheber S, Salzer JL (2004) Rho kinase regulates schwann cell myelination and formation of associated axonal domains. J Neurosci 16 : 3953 3963.
29. Nakai Y, Zheng Y, MacCollin M, Ratner N (2006) Temporal control of Rac in Schwann cell-axon interaction is disrupted in NF2-mutant Schwannoma cells. J Neurosci 13 : 3390 3395.
30. 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 1 : 53 62.
31. Nodari A, Zambroni D, Quattrini A, Court FA, D'Urso A, Recchia A et al (2007) Beta1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. J Cell Biol 6 : 1063 1075.
32. Obremski VJ, Hall AM, Fernandez-Valle C (1998) Merlin, the neurofibromatosis type 2 gene product, and beta1 integrin associate in isolated and differentiating Schwann cells. J Neurobiol 4 : 487 501.
33. Okada T, You L, Giancotti FG (2007) Shedding light on Merlin's wizardry. Trends Cell Biol 5 : 222 229.
34. Parkinson DB, Bhaskaran A, Droggiti A, Dickinson S, D'Antonio M, Mirsky R, Jessen KR (2004) Krox-20 inhibits Jun-NH2-terminal kinase/c-Jun to control Schwann cell proliferation and death. J Cell Biol. 164 (3 385 394.
35. Pelton PD, Sherman LS, Rizvi TA, Marchionni MA, Wood P, Friedman RA et al (1998) Ruffling membrane, stress fiber, cell spreading and proliferation abnormalities in human Schwannoma cells. Oncogene 17 : 2195 2209.
36. Ren XD, Kiosses WB, Schwartz MA (1999) Regulation of the small GTP-binding protein rho by cell adhesion and the cytoskeleton. EMBO J 3 : 578 585.
37. Rosenbaum C, Kluwe L, Mautner VF, Friedrich RE, Mueller HW, Hanemann CO (1998) Isolation and characterization of Schwann cells from neurofibromatosis type 2 patients. Neurobiol Dis 1 : 55 64.
38. Rosenberger G, Kutsche, K (2006) AlphaPIX and betaPIX and their role in focal adhesion formation. Eur J Cell Biol 3-4 : 265 274.
39. Rottner K, Krause M, Gimona M, Small JV, Wehland J (2001) Zyxin is not colocalized with vasodilator-stimulated phosphoprotein (VASP) at lamellipodial tips and exhibits different dynamics to vinculin, paxillin, and VASP in focal adhesions. Mol Biol Cell 10 : 3103 3113.
40. Sherman L, Xu HM, Geist RT, Saporito-Irwin S, Howells N, Ponta H et al (1997) Interdomain binding mediates tumor growth suppression by the NF2 gene product. Oncogene 20 : 2505 2509.
41. Svitkina TM, Borisy, GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 5 : 1009 1026.
42. ten Klooster JP, Jaffer ZM, Chernoff J, Hordijk PL (2006) Targeting and activation of Rac1 are mediated by the exchange factor beta-Pix. J Cell Biol 5 : 759 769.
43. Thurnherr T, Benninger Y, Wu X, Chrostek A, Krause SM, Nave KA et al (2006) Cdc42 and Rac1 signaling are both required for and act synergistically in the correct formation of myelin sheaths in the CNS. J Neurosci 40 : 10110 10119.
44. Tikoo A, Varga M, Ramesh V, Gusella J, Maruta H (1994) An anti-Ras function of neurofibromatosis type 2 gene product (NF2/Merlin). J Biol Chem 38 : 23387 23390.
45. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T et al (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 6654 : 990 994.
46. Utermark T, Kaempchen K, Hanemann CO (2003) Pathological adhesion of primary human Schwannoma cells is dependent on altered expression of integrins. Brain Pathol 3 : 352 363.
47. Utermark T, Schubert SJ, Hanemann CO (2005) Rearrangements of the intermediate filament GFAP in primary human Schwannoma cells. Neurobiol Dis 1 2 : 1 9.
48. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT et al (2004) FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 2 : 154 161.
49. Xiao GH, Beeser A, Chernoff J, Testa JR (2002) p21-activated Kinase Links Rac/Cdc42 Signaling to Merlin. J Biol Chem 2 : 883 886.
50. Xiao G, Gallagher R, Shetler J, Skele K, Altomare D, Pestell R, Jhanwar S, Testa J (2005) The NF2 tumor suppressor gene product, merlin, inhibits cell proliferation and cell cycle progression by repressing cyclin D1 expression. Mol Cell Biol 25 : 2384 2394.
51. Zaidel-Bar R, Ballestrem C, Kam Z, Geiger B (2003) Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 116 (Pt 22 4605 4613.
52. Zaidel-Bar R, Cohen M, Addadi L, Geiger B (2004) Hierarchical assembly of cell-matrix adhesion complexes. Biochem Soc Trans 32 (Pt 3 416 420.
53. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 8 : 858 867.
54. Zhao ZS, Manser E (2005) PAK and other Rho-associated kinases - effectors with surprisingly diverse mechanisms of regulation. Biochem J 386 (Pt 2 201 214.