Nuclear-cytoplasmic shuttling of menin regulates nuclear translocation of β-catenin

Molecular and Cellular Biology

Volumn 29, Issue 20, 2009, Pages 5477-5487

  Cao, Yanan ^a   Liu, Ruixin ^a   Jiang, Xiuli ^a   Lu, Jieli ^a   Jiang, Jingjing ^a   Zhang, Changxian ^c   Li, Xiaoying ^a,d   Ning, Guang ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c CNRS   (France)

^d SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; EXPORTIN 1; METHIONINE; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DEREGULATION; FIBROBLAST; INSULINOMA; MOUSE; NONHUMAN; NUCLEAR EXPORT SIGNAL; PANCREAS ISLET CELL TUMOR; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BETA CATENIN; CELL NUCLEUS; CYTOPLASM; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; WNT PROTEINS;

MUS;

EID: 70350448825     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00335-09     Document Type: Article

References (46)

1. Agarwal, S. K., S. C. Guru, C. Heppner, M. R. Erdos, R. M. Collins, S. Y. Park, S. Saggar, S. C. Chandrasekharappa, F. S. Collins, A. M. Spiegel, S. J. Marx, and A. L. Burns. 1999. Menin interacts with the AP1 transcription factor JunD and represses JunD-activated transcription. Cell 96:143-152. (Pubitemid 29044161)
2. Barth, A. I., D. B. Stewart, and W. J. Nelson. 1999. T cell factor-activated transcription is not sufficient to induce anchorage-independent growth of epithelial cells expressing mutant beta-catenin. Proc. Natl. Acad. Sci. USA 96:4947-4952.
3. Bertolino, P., I. Radovanovic, H. Casse, A. Aguzzi, Z. Q. Wang, and C. X. Zhang. 2003. Genetic ablation of the tumor suppressor menin causes lethality at mid-gestation with defects in multiple organs. Mech. Dev. 120:549-560.
4. Bertolino, P., W. M. Tong, P. L. Herrera, H. Casse, C. X. Zhang, and Z. Q. Wang. 2003. Pancreatic β-cell-specific ablation of the multiple endocrine neoplasia type 1 (MEN1) gene causes full penetrance of insulinoma development in mice. Cancer Res. 63:4836-4841. (Pubitemid 37022614)
5. Chandrasekharappa, S. C., S. C. Guru, P. Manickam, S. E. Olufemi, F. S. Collins, M. R. Emmert-Buck, L. V. Debelenko, Z. Zhuang, I. A. Lubensky, L. A. Liotta, J. S. Crabtree, Y. Wang, B. A. Roe, J. Weisemann, M. S. Boguski, S. K. Agarwal, M. B. Kester, Y. S. Kim, C. Heppner, Q. Dong, A. M. Spiegel, A. L. Burns, and S. J. Marx. 1997. Positional cloning of the gene for multiple endocrine neoplasia-type 1. Science 18:404-407.
6. Chen, G., M. Wang, S. Farley, L. Y. Lee, L. C. Lee, and M. P. Sawicki. 2008. Menin promotes the Wnt signaling pathway in pancreatic endocrine cells. Mol. Cancer Res. 6:1894-1907.
7. Clevers, H. 2006. Wnt/β-catenin signaling in development and disease. Cell 127:469-480.
8. Cong, F., and V. Varmus. 2004. Nuclear-cytoplasmic shuttling of Axin regulates subcellular localization of β-catenin. Proc. Natl. Acad. Sci. USA 101:2882-2887.
9. Dessimoz, J., C. Bonnard, J. Huelsken, and A. Grapin-Botton. 2005. Pancreas- specific deletion of β-catenin reveals Wnt-dependent and Wnt-independent functions during development. Curr. Biol. 15:1677-1683.
10. Dreijerink, K. M., K. W. Mulder, G. S. Winkler, J. W. Höppener, C. J. Lips, and H. T. Timmers. 2006. Menin links estrogen receptor activation to histone H3K4 trimethylation. Cancer Res. 66:4929-4935.
11. Fabbro, M., and B. R. Henderson. 2003. Regulation of tumor suppressors by nuclear-cytoplasmic shuttling. Exp. Cell Res. 282:59-69.
12. Guru, S. C., P. K. Goldsmith, A. L. Burns, S. J. Marx, A. M. Spiegel, F. S. Collins, and S. C. Chandrasekharappa. 1998. Menin, the product of the MEN1 gene, is a nuclear protein. Proc. Natl. Acad. Sci. USA 95:1630-1634.
13. Heiser, P. W., J. Lau, M. M. Taketo, P. L. Herrera, and M. Hebrok. 2006. Stabilization of β-catenin impacts pancreas growth. Development 133:2023-2032.
14. Henderson, B. R. 2000. Nuclear-cytoplasmic shuttling of APC regulates β-catenin subcellular localization and turnover. Nat. Cell Biol. 2:653-660.
15. Heppner, C., K. Y. Bilimoria, S. K. Agarwal, M. Kester, L. J. Whitty, S. C. Guru, S. C. Chandrasekharappa, F. S. Collins, A. M. Spiegel, S. J. Marx, and A. L. Burns. 2001. The tumor suppressor protein menin interacts with NF-κB proteins and inhibits NF-κB-mediated transactivation. Oncogene 20:4917-4925. (Pubitemid 32769781)
16. Hussein, N., J. Lu, H. Casse, S. Fontanière, A. M. Morera, S. M. Guittot, A. Calender, N. Di Clemente, and C. X. Zhang. 2008. Deregulation of anti-Mullerian hormone/BMP and transforming growth factor-beta pathways in Leydig cell lesions developed in male heterozygous multiple endocrine neoplasia type 1 mutant mice. Endocrinol. Relat. Cancer 15:217-227.
17. Jin, T. 2008. The WNT signalling pathway and diabetes mellitus. Diabetologia 51:1771-1780.
18. Kaji, H., L. Canaff, J. J. Lebrun, D. Goltzman, and G. N. Hendy. 2001. Inactivation of menin, a Smad3-interacting protein, blocks transforming growth factor type β signaling. Proc. Natl. Acad. Sci. USA 98:3837-3842.
19. INK4c. Proc. Natl. Acad. Sci. USA 102:14659-14664.
20. Karnik, S. K., H. Chen, G. W. McLean, J. J. Heit, X. Gu, A. Y. Zhang, M. Fontaine, M. H. Yen, and S. K. Kim. 2007. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 318:806-809.
21. Korinek, V., N. Barker, K. Willert, M. Molenaar, J. Roose, G. Wagenaar, M. Markman, W. Lamers, O. Destree, and H. Clevers. 1998. Two members of the Tcf family implicated in Wnt/beta-catenin signaling during embryogenesis in the mouse. Mol. Cell. Biol. 18:1248-1256.
22. Köster, M., T. Frahm, and H. Hauser. 2005. Nucleocytoplasmic shuttling revealed by FRAP and FLIP technologies. Curr. Opin. Biotechnol. 16:28-34.
23. La, P., A. Desmond, Z. Hou, A. C. Silva, R. W. Schnepp, and X. Hua. 2006. Tumor suppressor menin: the essential role of nuclear localization signal domains in coordinating gene expression. Oncogene 25:3537-3546.
24. Larsson, C., B. Skogseid, K. Oberg, Y. Nakamura, and M. Nordenskjöld. 1988. Multiple endocrine neoplasia type 1 gene maps to chromosome 11 and is lost in insulinoma. Nature 332:85-87. (Pubitemid 18083554)
25. Liu, Z., K. Tanabe, E. Bernal-Mizrachi, and M. A. Permutt. 2008. Mice with beta cell overexpression of GSK-3β have reduced beta cell mass and proliferation. Diabetologia 51:623-631.
26. Logan, C. Y., and R. Nusse. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20:781-810.
27. Major, M. B., N. D. Camp, J. D. Berndt, X. Yi, S. J. Goldenberg, C. Hubbert, T. L. Biechele, A. C. Gingras, N. Zheng, M. J. Maccoss, S. Angers, and R. T. Moon. 2007. Wilms tumor suppressor WTX negatively regulates WNT/β-catenin signaling. Science 316:1043-1046. (Pubitemid 46799493)
28. Milne, T. A., C. M. Hughes, R. Lloyd, Z. Yang, O. Rozenblatt-Rosen, Y. Dou, R. W. Schnepp, C. Krankel, V. A. Livolsi, D. Gibbs, X. Hua, R. G. Roeder, M. Meyerson, and J. L. Hess. 2005. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc. Natl. Acad. Sci. USA 102:749-754.
29. Morin, P. J., A. B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, and K. W. Kinzler. 1997. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275:1787-1790.
30. Murtaugh, L. C. 2008. The what, where, when and how of Wnt/β-catenin signaling in pancreas development. Organogenesis 4:81-86.
31. Mussmann, R., M. Geese, F. Harder, S. Kegel, U. Andag, A. Lomow, U. Burk, D. Onichtchouk, C. Dohrmann, and M. Austen. 2007. Inhibition of GSK3 promotes replication and survival of pancreatic beta cells. J. Biol. Chem. 282:12030-12037.
32. Persad, S., A. A. Troussard, T. R. McPhee, D. J. Mulholland, and S. Dedhar. 2001. Tumor suppressor PTEN inhibits nuclear accumulation of beta-catenin and T cell/lymphoid enhancer factor 1-mediated transcriptional activation. J. Cell Biol. 153:1161-1174. (Pubitemid 34289256)
33. Piñol-Roma, S., and G. Dreyfuss. 1993. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730-732.
34. Rodriguez, J. A., S. Schüchner, W. W. Au, M. Fabbro, and B. R. Henderson. 2004. Nuclear-cytoplasmic shuttling of BARD1 contributes to its proapoptotic activity and is regulated by dimerization with BRCA1. Oncogene 23:1809-1820.
35. Rosin-Arbesfeld, R., F. Townsley, and M. Bienz. 2000. The APC tumour suppressor has a nuclear export function. Nature 406:1009-1012. (Pubitemid 30690468)
36. Rulifson, I. C., S. K. Karnik, P. W. Heiser, D. ten Berge, H. Chen, X. Gu, M. M. Taketo, R. Nusse, M. Hebrok, and S. K. Kim. 2007. Wnt signaling regulates pancreatic β cell proliferation. Proc. Natl. Acad. Sci. USA 104:6247-6252.
37. Schnepp, R. W., Y. X. Chen, H. Wang, T. Cash, A. Silva, J. A. Diehl, E. Brown, and X. Hua. 2006. Mutation of tumor suppressor gene Men1 acutely enhances proliferation of pancreatic islet cells. Cancer Res. 66:5707-5715.
38. Sierra, J., T. Yoshida, C. A. Joazeiro, and K. A. Jones. 2006. The APC tumor suppressor counteracts β-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev. 20:586-600. (Pubitemid 43345324)
39. Stommel, J. M., N. D. Marchenko, G. S. Jimenez, U. M. Moll, T. J. Hope, and G. M. Wahl. 1999. A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J. 18:1660-1672.
40. Theillaumas, A., M. Blanc, C. Couderc, G. Poncet, W. Bazzi, C. Bernard, M. Cordier-Bussat, J. Y. Scoazec, and C. Roche. 2008. Relation between menin expression and NF-kappaB activity in an intestinal cell line. Mol. Cell Endocrinol. 291:109-115.
41. Thyssen, G., T. H. Li, L. Lehmann, M. Zhuo, M. Sharma, and Z. Sun. 2006. LZTS2 is a novel β-catenin-interacting protein and regulates the nuclear export of β-catenin. Mol. Cell. Biol. 26:8857-8867.
42. Welters, H. J., and R. N. Kulkarni. 2008. Wnt signaling: relevance to β-cell biology and diabetes. Trends Endocrinol. Metab. 19:349-355.
43. Yaguchi, H., N. Ohkura, M. Takahashi, Y. Nagamura, I. Kitabayashi, and T. Tsukada. 2004. Menin missense mutants associated with multiple endocrine neoplasia type 1 are rapidly degraded via the ubiquitin-proteasome pathway. Mol. Cell. Biol. 24:6569-6580.
44. Yan, J., Y. Yang, H. Zhang, C. King, H. M. Kan, Y. Cai, C. X. Yuan, G. S. Bloom, and X. Hua. 2009. Menin interacts with IQGAP1 to enhance intercellular adhesion of beta-cells. Oncogene 28:973-982.
45. Yokoyama, A., T. C. Somervaille, K. S. Smith, O. Rozenblatt-Rosen, M. Meyerson, and M. L. Cleary. 2005. The Menin tumor suppressor protein is an essential oncogenic cofactor for MLL-associated leukemogenesis. Cell 123:207-218. (Pubitemid 41457212)
46. Yu, X., and R. C. Malenka. 2003. Beta-catenin is critical for dendritic morphogenesis. Nat. Neurosci. 6:1169-1177.