Cloning and characterization of SCHIP-1, a novel protein interacting specifically with spliced isoforms and naturally occurring mutant NF2 proteins

Molecular and Cellular Biology

Volumn 20, Issue 5, 2000, Pages 1699-1712

  Goutebroze, Laurence ^a,b   Brault, Estelle ^a,b   Muchardt, Christian ^c   Camonis, Jacques ^a   Thomas, Gilles ^a,b  

^a INSTITUT CURIE   (France)

^b FONDATION JEAN DAUSSET CEPH   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; ISOPROTEIN; MERLIN; MUTANT PROTEIN; PROTEIN SCHIP 1; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TERTIARY STRUCTURE; REACTION ANALYSIS; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CARRIER PROTEINS; CLONING, MOLECULAR; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NEOPLASM PROTEINS; NEUROFIBROMIN 2; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEINS; RNA SPLICING; SEQUENCE ALIGNMENT;

EID: 0033970229     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.5.1699-1712.2000     Document Type: Article

References (61)

1. Arakawa, H., N. Hayashi, H. Nagase, M. Ogawa, and Y. Nakamura. 1994. Alternative splicing of the NF2 gene and its mutation analysis of breast and colorectal cancers. Hum. Mol. Genet. 3:565-568.
2. Berryman, M., Z. Franck, and A. Bretscher. 1993. Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J. Cell Sci. 105:1025-1043.
3. Bianchi, A. B., T. Hara, V. Ramesh, J. Gao, A. J. P. Klein-Szanto, F. Morin, A. G. Menon, J. A. Trofatter, J. F. Gusella, B. R. Seizinger, and N. Kley. 1994. Mutations in transcript isoforms of the neurofibromatosis 2 gene in multiple human tumour types. Nat. Genet. 6:185-192.
4. Bianchi, A. B., S.-I. Mitsunaga, J. Q. Cheng, W. M. Klein, S. C. Jhanwar, B. Seizinger, N. Kley, A. J. P. Klein-Szanto, and J. R. Testa. 1995. High frequency of inactivating mutations in the neurofibromatosis type 2 gene (NF2) in primary malignant mesotheliomas. Proc. Natl. Acad. Sci. USA 92:10854-10858.
5. Bijlsma, E. K., P. Merel, D. A. Bosch, A. Westerveld, O. Delattre, G. Thomas, and T. J. M. Hulsebos, 1994. Analysis of mutations in the SCH gene in schwannomas. Genes Chromosomes Cancer 11:7-14.
6. Bloom, L., and H. R. Horvitz. 1997. The Caenorhabditis elegans gene unc-76 and its human homologs define a new gene family involved in axonal outgrowth and fasciculation. Proc. Natl. Acad. Sci. USA 94:3414-3429.
7. Bretscher, A. 1999. Regulation of cortical structure by the ezrin-radixinmoesin protein family. Curr. Opin. Cell Biol. 11:109-116.
8. DeClue, J. E., A. G. Papageorge, J. A. Fletcher, S. R. Diehl, N. Ratner, W. C. Vass, and D. R. Lowy. 1992. Abnormal regulation of mammalian p21ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis. Cell 69:265-273.
9. Deguen, B., L. Goutebroze, M. Giovannini, C. Boisson, R. van der Neut, M. C. Jaurand, and G. Thomas. 1998. Heterogeneity of mesothelioma cell lines as defined by altered genomic structure and expression of the NF2 gene. Int. J. Cancer 77:554-560.
10. Deguen, B., P. Merel, L. Goutebroze, M. Giovannini, H. Reggio, M. Arpin, and G. Thomas. 1998. Impaired interaction of naturally occurring mutant NF2 protein with actin-based cytoskeleton and membrane. Hum. Mol. Genet. 7:217-226.
11. den Bakker, M. A., P. H. J. Riegman, R. Arnold, C. P. Hekman, W. Boersma, P. J. A. Janssen, T. H. van der Kwast, and E. C. Zwathoff. 1995. The product of the NF2 tumor suppressor gene localizes near the plasma membrane and is highly expressed in muscle cells. Oncogene 10:757-763.
12. den Bakker, M. A., M. Tascilar, P. H. J. Riegman, A. C. P. Hekman, W. Boersma, P. J. A. Janssen, T. A. W. de Jong, W. Hendriks, T. H. van der Kwast, and E. C. Zwathoff. 1995. Neurofibromatosis type 2 protein colocalizes with elements of the cytoskeleton. Am. J. Pathol. 147:1339-1349.
13. Evans, D. G., S. M. Huson, D. Donnai, W. Neary, V. Blair, V. Newton, and R. Harris. 1992. A clinical study of type 2 neurofibromatosis. Q. J. Med. 84:603-618.
14. Franck, Z., R. Gary, and A. Bretscher. 1993. Moesin, like ezrin, colocalizes with actin in the cortical cytoskeleton in cultured cells, but its expression is more variable. J. Cell Sci. 105:219-231.
15. Gary, R., and A. Bretscher. 1995. Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol. Biol. Cell 6:1061-1075.
16. Giovannini, M., E. Robanus-Maansdag, M. Niwa-Kawakita, M. van der Valk, J. M. Woodruff, L. Goutebroze, P. Merel, A. Berns, and G. Thomas. 1999. Schwann cell hyperplasia and tumors in transgenic mice expressing a naturally occurring mutant NF2 protein. Genes Dev. 13:978-986.
17. Gonzalez-Agosti, C., L. Xu, D. Pinney, R. Beauchamp, W. Hobbs, J. Gusella, and V. Ramesh. 1996. The merlin tumor suppressor localizes preferentially in membrane ruffles. Oncogene 13:1239-1247.
18. Gronholm, M., M. Sainio, F. Zhao, L. Heiska, A. Vaheri, and O. Carpen. 1999. Homotypic and heterotypic interaction of the neurofibromatosis 2 tumor suppressor protein merlin and the ERM protein ezrin. J. Cell Sci. 112:895-904.
19. Gutmann, D. H., R. T. Geist, H.-M. Xu, J. S. Kim, and S. Saporito-Irwin. 1998. Defects in neurofibromatosis 2 protein function can arise at multiple levels. Hum. Mol. Genet. 7:335-345.
20. Gutmann, D. H., M. J. Giordano, A. S. Fishback, and A. Guha. 1997. Loss of merlin expression in sporadic meningiomas, ependymomas and schwannomas. Neurology 49:267-270.
21. Haase, V. H., J. A. Trofatter, M. MacCollin, E. Tarttelin, J. F. Gusella, and V. Ramesh. 1994. The murine NF2 homologue encodes a highly conserved merlin protein with alternative forms. Hum. Mol. Genet. 3:407-411.
22. Heiska, L., K. Alfthan, M. Gronholm, P. Vilja, A. Vaheri, and O. Carpen. 1998. Association of ezrin with intercellular adhesion molecule-1 and -2 (ICAM-1 and ICAM-2). Regulation by phosphatidylinositol 4, 5-bisphosphate. J. Biol. Chem. 273:21893-21900.
23. Hirao, M., N. Sato, T. Kondo, S. Yonemura, M. Monden, T. Sasaki, Y. Takai, S. Tsukita, and S. Tsukita. 1996. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and rho-dependent signaling pathway. J. Cell Biol. 135:37-51.
24. Huang, L., E. Ichimaru, K. Pestonjamasp, X. Cui, H. Nakamura, G. Y. Lo, F. I. Lin, E. J. Luna, and H. Furthmayr. 1998. Merlin differs from moesin in binding to F-actin and in its intra-and intermolecular interactions. Biochem. Biophys. Res. Commun. 248:548-553.
25. Huynh, D. P., T. Nechiporuk, and S.-M. Pulst. 1994. Alternative transcripts in the mouse neurofibromatosis type 2 (NF2) gene are conserved and code for schwannomins with distinct C-terminal domains. Hum. Mol. Genet. 3:1075-1079.
26. Kaiser, C., S. Michaelis, and A. Mitchell. 1994. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory. Cold Spring Harbor, N.Y.
27. Kimura, Y., H. Koga, N. Araki, N. Mugita, N. Fujita, H. Takeshima, T. Nishi, T. Yamashima, T. C. Saido, T. Yamasaki, K. Moritake, H. Saya, and M. Nakao. 1998. The involvement of calpain-dependent proteolysis of the tumor suppressor NF2 (merlin) in schwannomas and meningiomas. Nat. Med. 4:915-922.
28. Koga, H., N. Araki, H. Takeshima, T. Nishi, T. Hirota, Y. Kimura, M. Nakao, and H. Saya. 1998. Impairment of cell adhesion by expression of the mutant neurofibromatosis type 2 (NF2) genes which lack exons in the ERM-homology domain. Oncogene 17:801-810.
29. Kuroda, S., N. Nakagawa, C. Tokunaga, K. Tatematsu, and K. Tanizawa. 1999. Mammalian homologue of the Caenorhabditis elegans UNC-76 protein involved in axonal outgrowth is a protein kinase C zeta-interacting protein. J. Cell Biol. 144:403-411.
30. Lee, J. H., V. Sundaram, D. J. Stein, S. E. Kinney, D. W. Stacey, and M. Golubic. 1997. Reduced expression of schwannomin/merlin in human sporadic meningiomas. Neurosurgery 40:578-587.
31. Lutchman, M., and G. A. Rouleau. 1995. The neurofibromatosis type 2 gene product, schwannomin, suppresses growth of NIH 3T3 cells. Cancer Res. 55:2270-2274.
32. Magendantz, M., M. D. Henry, A. Lander, and F. Solomon. 1995. Interdomain interactions of radixin in vitro. J. Biol. Chem. 270:25324-25327.
33. Mangeat, P., C. Roy, and M. Martin. 1999. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9:187-192.
34. Matsui, T., M. Maeda, Y. Doi, S. Yonemura, M. Amano, K. Kaibuchi, S. Tsukita, and S. Tsukita. 1998. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140:647-657.
35. Merel, P., K. Hoang-Xuan, M. Sanson, A. Moreau-Aubry, E. K. Bijlsma, C. Lazaro, J. P. Moisan, F. Resche, I. Nishisho, X. Estivill, J. Y. Delattre, M. Poisson, C. Theillet, T. Hulsebos, O. Delattre, and G. Thomas. 1995. Predominant occurence of somatic mutations of the NF2 gene in meningiomas and schwannomas. Genes Chromosomes Cancer 13:211-216.
36. + exchange, is a common interactor for merlin and ERM (MERM) proteins. J. Biol. Chem. 273:1273-1276.
37. Nishi, T., H. Takeshima, K. Hamada, K. Yoshizato, H. Koga, K. Sato, K. Yamamoto, I. Kitamura, M. Kochi, J.-I. Kuratsu, H. Saya, and Y. Ushio. 1997. Neurofibromatosis 2 gene has novel alternative splicings which controls intracellular protein binding. Int. J. Oncol. 10:1025-1029.
38. Pykett, M. J., M. Murphy, P. R. Harnish, and D. L. George. 1994. The neurofibromatosis 2 (NF2) tumor suppressor gene encodes multiple alternatively spliced transcripts. Hum. Mol. Genet. 3:559-564.
39. Rempel, S. A., K. Schwechheimer, R. L. Davis, W. K. Cavenee, and M. L. Rosenblum. 1993. Loss of heterozygosity for loci on chromosome 10 is associated with morphologically malignant meningioma progression. Cancer Res. 53:2386-2392.
40. Rogers, S., R. Wells, and M. Rechsteiner. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234: 364-368.
41. Rouleau, G. A., P. Merel, M. Lutchman, M. Sanson, J. Zucman, C. Marineau, K. Hoang-Xuan, S. Demczuk, C. Desmaze, B. Plougastel, S. M. Pulst, G. Lenoir, E. Bijlsma, R. Fashold, J. Dumanski, P. de Jong, D. Parry, R. Eldrige, A. Aurias, O. Delattre, and G. Thomas. 1993. Alteration in a new gene encoding a putative membrane-organizing protein causes neurofibromatosis type 2. Nature 363:515-521.
42. Ruttledge, M. H., J. Sarrazin, S. Rangaratnam, C. M. Phelan, E. Twist, P. Merel, O. Delattre, G. Thomas, M. Nordenskjold, V. P. Collins, J. P. Dumanski, and G. A. Rouleau. 1994. Evidence for the complete inactivation of the NF2 gene in the majority of sporadic meningiomas. Nat. Genet. 6:180-184.
43. Sainio, M., F. Zhao, L. Heiska, O. Turunen, M. den Bakker, E. Zwarthoff, M. Lutchman, G. A. Rouleau, J. Jääskeläinen, A. Vaheri, and O. Carpén. 1997. Neurofibromatosis 2 tumor suppressor protein colocalizes with ezrin and CD44 and associates with actin-containing cytoskeleton. J. Cell Sci. 110: 2249-2260.
44. Sainz, J., D. P. Huynh, K. Figueroa, N. K. Ragge, M. E. Baser, and S. M. Pulst. 1994. Mutations of the neurofibromatosis type 2 gene and lack of the gene product in vestibular schwannomas. Hum. Mol. Genet. 3:885-891.
45. Sato, N., N. Funayama, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1992. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. J. Cell Sci. 103:131-143.
46. Scherer, S. S., and D. H. Gutmann. 1996. Expression of the neurofibromatosis 2 tumor suppressor gene product, merlin, in Schwann cells. J. Neurosci. Res. 46:595-605.
47. Schiavo, G., S. L. Osborne, and J. G. Sgouros. 1998. Synaptotagmins: more isoforms than functions? Biochem. Biophys. Res. Commun. 248:1-8.
48. Schmucker, B., W. G. Ballhausen, and M. Kressel. 1997. Subcellular localization and expression pattern of the neurofibromatosis type 2 protein merlin/schwannomin. Eur. J. Cell Biol. 72:46-53.
49. Scoles, D. R., D. P. Huynh, P. A. Morcos, E. R. Coulsell, N. G. G. Robinson, F. Tamanoi, and S. M. Pulst. 1998. Neurofibromatosis 2 tumour suppressor schwannomin interacts with βII-spectrin. Nat. Genet. 18:354-359.
50. Shaw, R. J., A. I. McClatchey, and T. Jacks. 1998. Localization and functional domains of the neurofibromatosis type II tumor suppressor, merlin. Cell Growth Differ. 9:287-296.
51. Shaw, R. J., A. I. McClatchey, and T. Jacks. 1998. Regulation of the neurofibromatosis type 2 tumor suppressor protein, merlin, by adhesion and growth arrest stimuli. J. Biol. Chem. 273:7757-7764.
52. Sherman, L., H.-M. Xu, R. T. Geist, S. Saporo-Irwin, N. Howells, H. Ponta, P. Herrlich, and D. H. Gutmann. 1997. Interdomain binding mediates tumor growth suppression by the NF2 gene product. Oncogene 15: 2505-2509.
53. Stemmer-Rachamimov, A. O., C. Gonzalez-Agosti, L. Xu, J. A. Burwick, R. Beauchamp, D. Pinney, D. N. Louis, and V. Ramesh. 1997. Expression of NF2-encoded merlin and related ERM family proteins in the human central nervous system. J. Neuropathol. Exp. Neurol. 56:735-742.
54. Stemmer-Rachamimov, A. O., L. Xu, C. Gonzalez-Agosti, J. A. Burwick, D. Pinney, R. Beauchamp, L. B. Jacoby, J. F. Gusella, V. Ramesh, and D. N. Louis. 1997. Universal absence of merlin, but not other ERM family members, in schwannomas. Am. J. Pathol. 151:1649-1654.
55. Takeshima, H., I. Izawa, P. S. Lee, N. Safdar, V. A. Levin, and H. Saya. 1994. Detection of cellular proteins that interact with the NF2 tumor suppressor gene product. Oncogene 9:2135-2144.
56. Takeuchi, K., N. Sato, H. Kasahara, N. Funayama, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1994. Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members. J. Cell Biol. 125:1371-1384.
57. Tikoo, A., M. Varga, V. Ramesh, J. Gusella, and H. Maruta. 1994. An anti-ras function of neurofibromatosis type 2 gene product (NF2/merlin). J. Biol. Chem. 269:23387-23390.
58. Trofatter, J. A., M. M. MacCollin, J. L. Rutter, J. R. Murrell, M. P. Duyao, D. M. Parry, R. Eldridge, N. Kley, A. G. Menon, K. Pulaski, V. H. Haase, C. M. Ambrose, D. Munroe, C. Bove, J. L. Haines, R. L. Martuza, M. E. MacDonald, B. R. Seizinger, M. P. Short, A. J. Buckler, and J. F. Gusella. 1993. A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 72:791-800.
59. Turunen, O., M. Sainio, J. Jaaskelainen, O. Carpen, and A. Vaheri. 1998. Structure-function relationships in the ezrin family and the effect of tumor-associated point mutations in neurofibromatosis 2 protein. Biochim. Biophys. Acta 1387:1-16.
60. Turunen, O., T. Wahlström, and A. Vaheri. 1994. Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J. Cell Biol. 126:1445-1453.
61. Xu, H. M., and D. H. Gutmann. 1998. Merlin differentially associates with the microtubule and actin cytoskeleton. J. Neurosci. Res. 51:403-415.