Structural basis of DDB1-and-Cullin 4-associated Factor 1 (DCAF1) recognition by merlin/NF2 and its implication in tumorigenesis by CD44-mediated inhibition of merlin suppression of DCAF1 function

Genes to Cells

Volumn 19, Issue 8, 2014, Pages 603-619

  Mori, Tomoyuki ^a   Gotoh, Shuhei ^a   Shirakawa, Maya ^a   Hakoshima, Toshio ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DDB1 AND CULLIN 4 ASSOCIATED FACTOR 1 PROTEIN; HERMES ANTIGEN; MERLIN; RADIXIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CARRIER PROTEIN; CD44 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN; VPRBP PROTEIN, HUMAN;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL NUCLEUS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; GENE REPRESSION; HYDROGEN BOND; HYDROPHOBICITY; INTRACELLULAR SPACE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; STOICHIOMETRY; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PATHOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD44; CARCINOGENESIS; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; CYTOSKELETAL PROTEINS; HUMANS; MEMBRANE PROTEINS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUROFIBROMIN 2; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84904763728     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/gtc.12161     Document Type: Article

References (51)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221.
2. Ahronowitz, I., Xin, W., Kiely, R., Sims, K., MacCollin, M. & Nunes, F.P. (2007) Mutational spectrum of the NF2 gene: a meta-analysis of 12 years of research and diagnostic laboratory findings. Hum. Mutat. 28, 1-12.
3. Baumgartner, R., Poernbacher, I., Buser, N., Hafen, E. & Stocker, H. (2010) The WW domain protein Kibra acts upstream of hippo in Drosophila. Dev. Cell 18, 309-316.
4. Brown, M.S., Ye, J., Rawson, R.B. & Goldstein, J.L. (2000) Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391-398.
5. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., Read, R.J., Rice, L.M., Simonson, T. & Warren, G.L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921.
6. Chen, V.B., Arendall, W.B. 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. & Richardson, D.C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21.
7. Emsley, P. & Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
8. Evans, D.G., Huson, S.M., Donnai, D., Neary, W., Blair, V., Newton, V. & Harris, R. (1992) A clinical study of type 2 neurofibromatosis. Q. J. Med. 84, 603-618.
9. Fehon, R.G., McClatchey, A.I. & Bretscher, A. (2010) Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11, 276-287.
10. Genevet, A., Wehr, M.C., Brain, R., Thompson, B.J. & Tapon, N. (2010) Kibra is a regulator of the salvador/warts/hippo signaling network. Dev. Cell 18, 300-308.
11. Gladden, A.B., Hebert, A.M., Schneeberger, E.E. & McClatchey, A.I. (2010) The NF2 tumor suppressor, Merlin, regulates epidermal development through the establishment of a junctional polarity complex. Dev. Cell 19, 727-739.
12. Hamada, K., Shimizu, T., Matsui, T., Tsukita, S., Tsukita, S. & Hakoshima, T. (2000) Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J. 19, 4449-4462.
13. Hamada, K., Shimizu, T., Yonemura, S., Tsukita, S., Tsukita, S. & Hakoshima, T. (2003) Structural basis of adhesion-molecule recognition by ERM proteins revealed by the crystal structure of the radixin-ICAM-2 complex. EMBO J. 22, 502-514.
14. Kabsch, W. (1976) A solution for the best rotation to relate two sets of vectors. Acta Crystallogr. A Biol. Crystallogr. A32, 922-923.
15. Lallemand, D., Curto, M., Saotome, I., Giovannini, M. & McClatchey, A.I. (2003) NF2 deficiency promotes tumorigenesis and metastasis by destabilizing adherens junctions. Genes Dev. 17, 1090-1100.
16. Lallemand, D., Manent, J., Couvelard, A., Watilliaux, A., Siena, M., Chareyre, F., Lampin, A., Niwa-Kawakita, M., Kalamarides, M. & Giovannini, M. (2009) Merlin regulates transmembrane receptor accumulation and signaling at the plasma membrane in primary mouse Schwann cells and in human schwannomas. Oncogene 28, 854-865.
17. Li, W., Cooper, J., Karajannis, M.A. & Giancotti, F.G. (2012) Merlin: a tumour suppressor with functions at the cell cortex and in the nucleus. EMBO Rep. 13, 204-215.
18. Li, W., You, L., Cooper, J., Schiavon, G., Pepe-Caprio, A., Zhou, L., Ishii, R., Giovannini, M., Hanemann, C.O., Long, S.B., Erdjument-Bromage, H., Zhou, P., Tempst, P. & Giancotti, F.G. (2010) Merlin/NF2 suppresses tumorigenesis by inhibiting the E3 ubiquitin ligase CRL4(DCAF1) in the nucleus. Cell 140, 477-490.
19. McClatchey, A.I. & Fehon, R.G. (2009) Merlin and the ERM proteins - regulators of receptor distribution and signaling at the cell cortex. Trends Cell Biol. 19, 198-206.
20. McClatchey, A.I. & Giovannini, M. (2005) Membrane organization and tumorigenesis-the NF2 tumor suppressor, Merlin. Genes Dev. 19, 2265-2277.
21. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. & Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674.
22. Mori, T., Kitano, K., Fukami, Y., Terawaki, S. & Hakoshima, T. (2008) Structural basis for CD44 recognition by ERM proteins. J. Biol. Chem. 283, 29602-29612.
23. Murakami, D., Okamoto, I., Nagano, O., Kawano, Y., Tomita, T., Iwatsubo, T., De Strooper, B., Yumoto, E. & Saya, H. (2003) Presenilin-dependent gamma-secretase activity mediates the intramembranous cleavage of CD44. Oncogene 22, 1511-1516.
24. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255.
25. Nagano, O. & Saya, H. (2004) Mechanism and biological significance of CD44 cleavage. Cancer Sci. 95, 930-935.
26. Naor, D., Wallach-Dayan, S.B., Zahalka, M.A. & Sionov, R.V. (2008) Involvement of CD44, a molecule with a thousand faces, in cancer dissemination. Semin. Cancer Biol. 18, 260-267.
27. Okada, T., Lopez-Lago, M. & Giancotti, F.G. (2005) Merlin/NF-2 mediates contact inhibition of growth by suppressing recruitment of Rac to the plasma membrane. J. Cell Biol. 171, 361-371.
28. Okada, T., You, L. & Giancotti, F.G. (2007) Shedding light on Merlin's wizardry. Trends Cell Biol. 17, 222-229.
29. Okamoto, I., Kawano, Y., Murakami, D., Sasayama, T., Araki, N., Miki, T., Wong, A.J. & Saya, H. (2001) Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway. J. Cell Biol. 155, 755-762.
30. Okamoto, I., Tsuiki, H., Kenyon, L.C., Godwin, A.K., Emlet, D.R., Holgado-Madruga, M., Lanham, I.S., Joynes, C.J., Vo, K.T., Guha, A., Matsumoto, M., Ushio, Y., Saya, H. & Wong, A.J. (2002) Proteolytic cleavage of the CD44 adhesion molecule in multiple human tumors. Am. J. Pathol. 160, 441-447.
31. Otwinowski, Z. & Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
32. Pearson, M.A., Reczek, D., Bretscher, A. & Karplus, P.A. (2000) Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101, 259-270.
33. Pelletier, L., Guillaumot, P., Frêche, B., Luquain, C., Christiansen, D., Brugière, S., Garin, J. & Manié, S.N. (2006) Gamma-secretase-dependent proteolysis of CD44 promotes neoplastic transformation of rat fibroblastic cells. Cancer Res. 66, 3681-3687.
34. Ramesh, V. (2004) Merlin and the ERM proteins in Schwann cells, neurons and growth cones. Nat. Rev. Neurosci. 5, 462-470.
35. Ratajczak, M.Z. (2005) Cancer stem cells-normal stem cells "Jedi" that went over to the "dark side". Folia Histochem. Cytobiol. 43, 175-181.
36. Rouleasu, G.A., Merel, P., Lutchman, M., et al. (1993) Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 363, 515-521.
37. Sainio, M., Zhao, F., Heiska, L., Turunen, O., den Bakker, M., Zwarthoff, E., Lutchman, M., Rouleau, G.A., Jääskeläinen, J., Vaheri, A. & Carpén, O. (1997) Neurofibromatosis 2 tumor suppressor protein colocalizes with ezrin and CD44 and associates with actin-containing cytoskeleton. J. Cell Sci. 110, 2249-2260.
38. Shimizu, T., Seto, A., Maita, N., Hamada, K., Tsukita, S., Tsukita, S. & Hakoshima, T. (2002) Structural basis for neurofibromatosis Type 2: crystal structure of the Merlin FERM domain. J. Biol. Chem. 277, 10332-10336.
39. Smith, W.J., Nassar, N., Bretscher, A., Cerione, R.A. & Karplus, P.A. (2003) Structure of the active N-terminal domain of Ezrin. Conformational and mobility changes identify keystone interactions. J. Biol. Chem. 278, 4949-4956.
40. Takai, Y., Kitano, K., Terawaki, S., Maesaki, R. & Hakoshima, T. (2007) Structural basis of PSGL-1 binding to ERM proteins. Genes Cells 12, 1329-1338.
41. Takai, Y., Kitano, K., Terawaki, S., Maesaki, R. & Hakoshima, T. (2008) Structural basis of the cytoplasmic tail of adhesion molecule CD43 and its binding to ERM proteins. J. Mol. Biol. 381, 634-644.
42. Terawaki, S., Kitano, K. & Hakoshima, T. (2007) Structural basis for type II membrane protein binding by ERM proteins revealed by the radixin-neutral endopeptidase 24.11 (NEP) complex. J. Biol. Chem. 282, 19854-19861.
43. Terawaki, S., Maesaki, R. & Hakoshima, T. (2006) Structural basis of NHERF recognition by ERM proteins. Structure 14, 777-789.
44. Thorne, R.F., Legg, J.W. & Isacke, C.M. (2004) The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events. J. Cell Sci. 117, 373-380.
45. Trofatter, J.A., MacCollin, M.M., Rutter, J.L., et al. (1993) A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 72, 791-800.
46. Tsukita, S., Oishi, K., Sato, N., Sagara, J., Kawai, A. & Tsukita, S. (1994) ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126, 391-401.
47. Venkatachalam, C.M. (1968) Stereochemical criteria for polypeptides and proteins. V. Conformation of a system of three linked peptide units. Biopolymers 6, 1425-1436.
48. Yi, C., Troutman, S., Fera, D., Stemmer-Rachamimov, A., Avila, J.L., Christian, N., Persson, N.L., Shimono, A., Speicher, D.W., Marmorstein, R., Holmgren, L. & Kissil, J.L. (2011) A tight junction-associated Merlin-angiomotin complex mediates Merlin's regulation of mitogenic signaling and tumor suppressive functions. Cancer Cell 19, 527-540.
49. Yonemura, S., Hirao, M., Doi, Y., Takahashi, N., Kondo, T., Tsukita, S. & Tsukita, S. (1998) Ezrin/Radixin/Moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43 and ICAM-2. J. Cell Biol. 140, 885-895.
50. Yu, J., Zheng, Y., Dong, J., Klusza, S., Deng, W.M. & Pan, D. (2010) Kibra functions as a tumor suppressor protein that regulates hippo signaling in conjunction with merlin and expanded. Dev. Cell 18, 288-299.
51. Zöller, M. (2011) CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat. Rev. Cancer 11, 254-267.