The tumor suppressor merlin interacts with microtubules and modulates Schwann cell microtubule cytoskeleton

Human Molecular Genetics

Volumn 16, Issue 14, 2007, Pages 1742-1751

  Muranen, Taru ^a   Grönholm, Mikaela ^a   Lampin, Aurelie ^b   Lallemand, Dominique ^b   Zhao, Fang ^a   Giovannini, Marco ^b   Carpén, Olli ^a,c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b INSERM   (France)

^c TURKU UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

MERLIN; NEUROFIBROMIN; SERINE; TUBULIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; GENE CONTROL; GENE INTERACTION; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VIVO STUDY; INTERPHASE; MENINGIOMA; MICROTUBULE; MOLECULAR MECHANICS; NEURILEMOMA; NEUROPATHOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; SCHWANN CELL; TUMOR SUPPRESSOR GENE;

ANIMALS; CATTLE; CELL LINE, TUMOR; CYTOSKELETON; ESCHERICHIA COLI; GLIOMA; HUMANS; INSECTS; MICE; MICROTUBULES; MODELS, BIOLOGICAL; NEUROFIBROMIN 2; PROTEIN ISOFORMS; SCHWANN CELLS; TUBULIN;

EID: 34547798554     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm122     Document Type: Article

References (42)

1. Gutmann, D.H. (1997) Molecular insights into neurofibromatosis 2. Neurobiol. Dis., 3, 247-261.
2. den Bakker, M.A., Riegman, P.H., Suurmeijer, A.P., Vissers, C.J., Sainio, M., Carpen, O. and Zwarthoff, E.C. (2000) Evidence for a cytoskeleton attachment domain at the N-terminus of the NF2 protein. J. Neurosci. Res., 62, 764-771.
3. Xu, H.M. and Gutmann, D.H. (1998) Merlin differentially associates with the microtubule and actin cytoskeleton. J. Neurosci. Res., 51 403-415.
4. Bretscher, A., Chambers, D., Nguyen, R. and Reczek, D. (2000) ERM-merlin and EBP50 protein families in plasma membrane organization and function. Annu. Rev. Cell Dev. Biol., 16, 113-143.
5. Gonzalez-Agosti, C., Wiederhold, T., Herndon, M.E., Gusella, J. and Ramesh, V. (1999) Interdomain interaction of merlin isoforms and its influence on intermolecular binding to NHE-RF. J. Biol. Chem., 274, 34438-34442.
6. Grönholm, M., Sainio, M., Zhao, F., Heiska, L., Vaheri, A. and Carpen, O. (1999) Homotypic and heterotypic interaction of the neurofibromatosis 2 tumor suppressor protein merlin and the ERM protein ezrin. J. Cell. Sci., 112, 895-904.
7. Nguyen, R., Reczek, D. and Bretscher, A. (2001) Hierarchy of merlin and ezrin N- and C-terminal domain interactions in homo- and heterotypic associations and their relationship to binding of scaffolding proteins EBP50 and E3KARP. J. Biol. Chem., 276, 7621-7629.
8. Shaw, R.J., Paez, J.G., Curto, M., Yaktine, A., Pruitt, W.M., Saotome, I., O'Bryan, J.P., Gupta, V., Ratner, N., Der, C.J. et al. (2001) The Nf2 tumor suppressor, merlin, functions in rac-dependent signaling. Dev. Cell, 1, 63-72.
9. Alfthan, K., Heiska, L., Grönholm, M., Renkema, G.H. and Carpen, O. (2004) Cyclic AMP-dependent protein kinase phosphorylates merlin at serine 518 independently of P21-activated kinase and promotes merlin-ezrin heterodimerization. J. Biol. Chem., 279, 18559-18566.
10. Fraenzer, J.T., Pan, H., Minimo, L., Jr, Smith, G.M., Knauer, D. and Hung, G. (2003) Overexpression of the NF2 gene inhibits schwannoma cell proliferation through promoting PDGFR degradation. Int. J. Oncol., 23, 1493-1500.
11. Scoles, D.R., Huynh, D.P., Chen, M.S., Burke, S.P., Gutmann, D.H. and Pulst, S.M. (2000) The neurofibromatosis 2 tumor suppressor protein interacts with hepatocyte growth factor-regulated tyrosine kinase substrate. Hum. Mol. Genet., 9, 1567-1574.
12. Lloyd, T.E., Atkinson, R., Wu, M.N., Zhou, Y., Pennetta, G. and Bellen, H.J. (2002) Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell, 108, 261-269.
13. Maitra, S., Kulikauskas, R.M., Gavilan, H. and Fehon, R.G. (2006) The tumor suppressors merlin and expanded function cooperatively to modulate receptor endocytosis and signaling. Curr. Biol., 16, 702-709.
14. Fisk, H.A., Mattison, C.P. and Winey, M. (2002) Centrosomes and tumour suppressors. Curr. Opin. Cell Biol., 14, 700-705.
15. Hergovich, A., Lisztwan, J., Barry, R., Ballschmieter, P. and Krek, W. (2003) Regulation of microtubule stability by the von hippel-lindau tumour suppressor protein pVHL. Nat. Cell Biol., 5, 64-70.
16. Murray, J.W. and Wolkoff, A.W. (2003) Roles of the cytoskeleton and motor proteins in endocytic sorting. Adv. Drug Deliv. Rev., 55 1385-1403.
17. Muranen, T., Grönholm, M., Renkema, G.H. and Carpen, O. (2005) Cell cycle-dependent nucleocytoplasmic shuttling of the neurofibromatosis 2 tumour suppressor merlin. Oncogene, 24, 1150-1158.
18. Stokowski, R.P. and Cox, D.R. (2000) Functional analysis of the neurofibromatosis type 2 protein by means of disease-causing point mutations. Am. J. Hum. Genet., 66, 873-891.
19. Grönholm, M., Muranen, T., Toby, G.G., Utermark, T., Hanemann, C.O., Golemis, E.A. and Carpen, O. (2006) A functional association between merlin and HEI10, a cell cycle regulator. Oncogene, 25, 4389-4398.
20. Kissil, J.L., Johnson, K.C., Eckman, M.S. and Jacks, T. (2002) Merlin phosphorylation by p21-activated kinase 2 and effects of phosphorylation on merlin localization. J. Biol. Chem., 277, 10394-10399.
21. Morrison, H., Sherman, L.S., Legg, J., Banine, F., Isacke, C., Haipek, C.A., Gutmann, D.H., Ponta, H. and Herrlich, P. (2001) The NF2 tumor suppressor gene product, merlin, mediates contact inhibition of growth through interactions with CD44. Genes Dev., 15, 968-980.
22. Xiao, G.H., Beeser, A., Chernoff, J. and Testa, J.R. (2002) p21-activated kinase links Rac/Cdc42 signaling to merlin. J. Biol. Chem., 277, 883-886.
23. Rong, R., Surace, E.I., Haipek, C.A., Gutmann, D.H. and Ye, K. (2004) Serine 518 phosphorylation modulates merlin intramolecular association and binding to critical effectors important for NF2 growth suppression. Oncogene, 23, 8447-8454.
24. Giovannini, M., Robanus-Maandag, E., van derValk, M., Niwa-Kawakita,M., Abramowski, V., Goutebroze, L.,Woodruff, J.M., Berns, A. and Thomas, G. (2000) Conditional biallelic Nf2 mutation in the mouse promotes manifestations of human neurofibromatosis type 2. Gene Dev., 14 1617-1630.
25. Utemark, T., Schubert, S.J. and Hanemann, C.O. (2005) Rearrangements of the intermediate filament GFAP in primary human schwannoma cells. Neurobiol. Dis., 19, 1-9.
26. Ozer, R.S. and Halpain, S. (2000) Phosphorylation-dependent localization of microtubule-associated protein MAP2c to the actin cytoskeleton. Mol. Biol. Cell, 11, 3573-3587.
27. Rubino, H.M., Dammerman, M., Shafit-Zagardo, B. and Erlichman, J. (1989) Localization and characterization of the binding site for the regulatory subunit of type II cAMP-dependent protein kinase on MAP2. Neuron, 3, 631-638.
28. Grönholm, M., Vossebein, L., Carlson, C.R., Kuja-Panula, J., Teesalu, T., Alfthan, K., Vaheri, A., Rauvala, H., Herberg, F.W., Tasken, K. et al. (2003) Merlin links to the cAMP neuronal signaling pathway by anchoring the RIbeta subunit of protein kinase A. J. Biol. Chem., 278, 41167-41172.
29. Lamb, N.J., Cavadore, J.C., Labbe, J.C., Maurer, R.A. and Fernandez, A. (1991) Inhibition of cAMP-dependent protein kinase plays a key role in the induction of mitosis and nuclear envelope breakdown in mammalian cells. EMBO J., 10, 1523-1533.
30. Banerjee, M., Worth, D., Prowse, D.M. and Nikolic, M. (2002) Pak1 phosphorylation on t212 affects microtubules in cells undergoing mitosis. Curr. Biol., 12, 1233-1239.
31. Koga, H., Araki, N., Takeshima, H., Nishi, T., Hirota, T., Kimura, Y., Nakao, M. and Saya, H. (1998) Impairment of cell adhesion by expression of the mutant neurofibromatosis type 2 (NF2) genes which lack exons in the ERM-homology domain. Oncogene, 20, 801-810.
32. Lallemand, D., Curto, M., Saotome, I., Giovannini, M. and McClatchey, A.I. (2003) NF2 deficiency promotes tumorigenesis and metastasis by destabilizing adherens junctions. Genes Dev., 17, 1090-1100.
33. Petiot, A., Faure, J., Stenmark, H. and Gruenberg, J. (2003) PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J. Cell Biol., 162, 971-979.
34. Lakadamyali, M., Rust, M.J. and Zhuang, X. (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell, 124, 997-1009.
35. Kita, K., Wittmann, T., Nathke, I.S. and Waterman-Storer, C.M. (2006) Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol. Biol. Cell, 17, 2331-2345.
36. Lolkema, M.P., Mehra, N., Jorna, A.S., van Beest, M., Giles, R.H. and Voest, E.E. (2004) The von Hippel-Lindau tumor suppressor protein influences microtubule dynamics at the cell periphery. Exp. Cell Res. 301, 139-146.
37. Rosenbaum, C., Kluwe, L., Mautner, V.F., Friedrich, R.E., Muller, H.W. and Hanemann, C.O. (1998) Isolation and characterization of schwann cells from neurofibromatosis type 2 patients. Neurobiol. Dis., 5, 55-64.
38. Manent, J., Oguievetskaia, K., Bayer, J., Ratner, N. and Giovannini, M. (2003) Magnetic cell sorting for enriching schwann cells from adult mouse peripheral nerves. J. Neurosci. Methods, 123, 167-173.
39. den Bakker, M.A., Riegman, P.H., Hekman, R.A., Boersma, W., Janssen, P.J., van der Kwast, T.H. and Zwarthoff, E.C. (1995) The product of the NF2 tumour suppressor gene localizes near the plasma membrane and is highly expressed in muscle cells. Oncogene, 10, 757-763.
40. Lutchman, M. and Rouleau, G.A. (1995) The neurofibromatosis type 2 gene product, schwannomin, suppresses growth of NIH 3T3 cells. Cancer Res. 55, 2270-2274.
41. Huber, L.J. and Chao, M.V. (1995) Mesenchymal and neuronal cell expression of the p75 neurotrophin receptor gene occur by different mechanisms. Dev. Biol., 167, 227-238.
42. Hyman, A.A., Drexel, D., Kellog, D., Salser, S., Sawin, K., Steffen, P., Wordeman, L. and Mitchison, T.J. (1991) Preparation of modified tubulins. Meth. Enzymol., 196, 478-486.