GSK-3β protein phosphorylates and stabilizes HLXB9 protein in insulinoma cells to form a targetable mechanism of controlling insulinoma cell proliferation

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 5386-5398

  Desai, Shruti S ^a   Modali, Sita D ^a   Parekh, Vaishali I ^a   Kebebew, Electron ^b   Agarwal, Sunita K ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIFFERENTIATION; DOWNSTREAM TARGET; EXPRESSED GENES; INSULINOMA CELLS; PANCREATIC ISLET; PANCREATIC NEUROENDOCRINE TUMORS; PROAPOPTOTIC ACTIVITY; TISSUE SPECIFICS;

CELL CULTURE; CELL DEATH; CELL PROLIFERATION; TUMORS;

PROTEINS;

B LYMPHOCYTE DIFFERENTIATION FACTOR; GLYCOGEN SYNTHASE KINASE 3BETA; HLXB9 PROTEIN; METHIONINE; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN TISSUE; INSULINOMA; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; RAT; TISSUE SPECIFICITY;

DIFFERENTIATION; GSK-3Β; HLXB9; INSULINOMA; MEN1; MENIN; NEUROENDOCRINOLOGY; PANCREATIC ISLETS; PROLIFERATION; TUMOR;

ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; CYTOPLASM; GLYCOGEN SYNTHASE KINASE 3; HOMEODOMAIN PROTEINS; HUMANS; INSULIN-SECRETING CELLS; INSULINOMA; MICE; PHOSPHORYLATION; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS; RATS; TRANSCRIPTION FACTORS;

EID: 84896859088     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.533612     Document Type: Article

References (40)

1. Thakker, R. V., Newey, P. J., Walls, G. V., Bilezikian, J., Dralle, H., Ebeling, P. R., Melmed, S., Sakurai, A., Tonelli, F., and Brandi, M. L. (2012) Clinical practice guidelines for multiple endocrine neoplasia type 1 (MEN1). J. Clin. Endocrinol. Metab. 97, 2990-3011
2. Marx, S. J. (2005) Molecular genetics of multiple endocrine neoplasia types 1 and 2. Nat. Rev. Cancer 5, 367-375
3. Agarwal, S. K. (2013) Multiple endocrine neoplasia type 1. Front. Horm. Res. 41, 1-15
4. Shen, H. C., He, M., Powell, A., Adem, A., Lorang, D., Heller, C., Grover, A. C., Ylaya, K., Hewitt, S. M., Marx, S. J., Spiegel, A. M., and Libutti, S. K. (2009) Recapitulation of pancreatic neuroendocrine tumors in human multiple endocrine neoplasia type I syndrome via Pdx1-directed inactivation of Men1. Cancer Res. 69, 1858-1866
5. Piret, S. E., and Thakker, R. V. (2011) Mouse models for inherited endocrine and metabolic disorders. J. Endocrinol. 211, 211-230
6. Shen, H. C., Ylaya, K., Pechhold, K., Wilson, A., Adem, A., Hewitt, S. M., and Libutti, S. K. (2010) Multiple endocrine neoplasia type 1 deletion in pancreatic α-cells leads to development of insulinomas in mice. Endocrinology 151, 4024-4030
7. Lu, J., Herrera, P. L., Carreira, C., Bonnavion, R., Seigne, C., Calender, A., Bertolino, P., and Zhang, C. X. (2010) α cell-specific Men1 ablation triggers the transdifferentiation of glucagon-expressing cells and insulinoma development. Gastroenterology 138, 1954-1965
8. Scacheri, P. C., Crabtree, J. S., Kennedy, A. L., Swain, G. P., Ward, J. M., Marx, S. J., Spiegel, A. M., and Collins, F. S. (2004) Homozygous loss of menin is well tolerated in liver, a tissue not affected in MEN1. Mamm. Genome. 15, 872-877 (Pubitemid 40064198)
9. Jensen, R. T., Berna, M. J., Bingham, D. B., and Norton, J. A. (2008) Inherited pancreatic endocrine tumor syndromes. Advances in molecular pathogenesis, diagnosis, management, and controversies. Cancer 113, 1807-1843
10. Jiao, Y., Shi, C., Edil, B. H., de Wilde, R. F., Klimstra, D. S., Maitra, A., Schulick, R. D., Tang, L. H., Wolfgang, C. L., Choti, M. A., Velculescu, V. E., Diaz, L. A., Jr., Vogelstein, B., Kinzler, K. W., Hruban, R. H., and Papadopoulos, N. (2011) DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331, 1199-1203
11. Oberg, K., Casanovas, O., Castaño, J. P., Chung, D., Delle Fave, G., Denèfle, P., Harris, P., Khan, M. S., Kulke, M. H., Scarpa, A., Tang, L. H., and Wiedenmann, B. (2013) Molecular pathogenesis of neuroendocrine tumors. Implications for current and future therapeutic approaches. Clin. Cancer Res. 19, 2842-2849
12. Kaidanovich-Beilin, O., and Woodgett, J. R. (2011) GSK-3. Functional insights from cell biology and animal models. Front. Mol. Neurosci. 4, 40
13. Kunnimalaiyaan, M., Vaccaro, A. M., Ndiaye, M. A., and Chen, H. (2007) Inactivation of glycogen synthase kinase-3 β, a downstream target of the Raf-1 pathway, is associated with growth suppression in medullary thyroid cancer cells. Mol. Cancer Ther. 6, 1151-1158 (Pubitemid 46554586)
14. Shi, K., Parekh, V. I., Roy, S., Desai, S. S., and Agarwal, S. K. (2013) The embryonic transcription factor Hlxb9 is a menin interacting partner that controls pancreatic β-cell proliferation and the expression of insulin regulators. Endocr. Relat. Cancer 20, 111-122
15. Scacheri, P. C., Davis, S., Odom, D. T., Crawford, G. E., Perkins, S., Halawi, M. J., Agarwal, S. K., Marx, S. J., Spiegel, A. M., Meltzer, P. S., and Collins, F. S. (2006) Genome-wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet. 2, e51
16. Harrison, K. A., Thaler, J., Pfaff, S. L., Gu, H., and Kehrl, J. H. (1999) Pancreas dorsal lobe agenesis and abnormal islets of Langerhans in Hlxb9-deficient mice. Nat. Genet. 23, 71-75 (Pubitemid 29418791)
17. Li, H., Arber, S., Jessell, T. M., and Edlund, H. (1999) Selective agenesis of the dorsal pancreas in mice lacking homeobox gene Hlxb9. Nat. Genet. 23, 67-70 (Pubitemid 29418790)
18. Li, H., and Edlund, H. (2001) Persistent expression of Hlxb9 in the pancreatic epithelium impairs pancreatic development. Dev. Biol. 240, 247-253 (Pubitemid 33141121)
19. Harrison, K. A., Druey, K. M., Deguchi, Y., Tuscano, J. M., and Kehrl, J. H. (1994) A novel human homeobox gene distantly related to proboscipedia is expressed in lymphoid and pancreatic tissues. J. Biol. Chem. 269, 19968-19975 (Pubitemid 24250916)
20. Thaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J., and Pfaff, S. L. (1999) Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23, 675-687 (Pubitemid 29411558)
21. Guru, S. C., Goldsmith, P. K., Burns, A. L., Marx, S. J., Spiegel, A. M., Collins, F. S., and Chandrasekharappa, S. C. (1998) Menin, the product of the MEN1 gene, is a nuclear protein. Proc. Natl. Acad. Sci. U.S.A. 95, 1630-1634 (Pubitemid 28103444)
22. Stambolic, V., and Woodgett, J. R. (1994) Mitogen inactivation of glycogen synthase kinase-3 β in intact cells via serine 9 phosphorylation. Biochem. J. 303, 701-704 (Pubitemid 24325998)
23. Ang, Y. S., Tsai, S. Y., Lee, D. F., Monk, J., Su, J., Ratnakumar, K., Ding, J., Ge, Y., Darr, H., Chang, B., Wang, J., Rendl, M., Bernstein, E., Schaniel, C., and Lemischka, I. R. (2011) Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145, 183-197
24. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y., and Yamamura, K. (1990) Establishment of a pancreatic β-cell line that retains glucose-inducible insulin-secretion. Special reference to expression of glucose transporter isoforms. Endocrinology 127, 126-132 (Pubitemid 20228111)
25. O'Dowd, J. F. (2009) The isolation and purification of rodent pancreatic islets of Langerhans. Methods Mol. Biol. 560, 37-42
26. Sukhodolets, K. E., Hickman, A. B., Agarwal, S. K., Sukhodolets, M. V., Obungu, V. H., Novotny, E. A., Crabtree, J. S., Chandrasekharappa, S. C., Collins, F. S., Spiegel, A. M., Burns, A. L., and Marx, S. J. (2003) The 32-kilodalton subunit of replication protein A interacts with menin, the product of the MEN1 tumor suppressor gene. Mol. Cell. Biol. 23, 493-509 (Pubitemid 36050544)
27. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 105, 10762-10767
28. Sutherland, C. (2011) What are the bona fide GSK3 substrates? Int. J. Alzheimers Dis. 10.4061/2011/505607
29. Culbert, A. A., Brown, M. J., Frame, S., Hagen, T., Cross, D. A., Bax, B., and Reith, A. D. (2001) GSK-3 inhibition by adenoviral FRAT1 overexpression is neuroprotective and induces Tau dephosphorylation and β-catenin stabilisation without elevation of glycogen synthase activity. FEBS Lett. 507, 288-294 (Pubitemid 33030251)
30. Crabtree, J. S., Scacheri, P. C., Ward, J. M., Garrett-Beal, L., Emmert-Buck, M. R., Edgemon, K. A., Lorang, D., Libutti, S. K., Chandrasekharappa, S. C., Marx, S. J., Spiegel, A. M., and Collins, F. S. (2001) A mouse model of multiple endocrine neoplasia, type 1, develops multiple endocrine tumors. Proc. Natl. Acad. Sci. U.S.A. 98, 1118-1123 (Pubitemid 32121196)
31. Ojeda, L., Gao, J., Hooten, K. G., Wang, E., Thonhoff, J. R., Dunn, T. J., Gao, T., and Wu, P. (2011) Critical role of PI3K/Akt/GSK3β in motorneuron specification from human neural stem cells in response to FGF2 and EGF. PLoS ONE 6, e23414
32. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer. The next generation. Cell 144, 646-674
33. Zhuang, Z., Vortmeyer, A. O., Pack, S., Huang, S., Pham, T. A., Wang, C., Park, W. S., Agarwal, S. K., Debelenko, L. V., Kester, M., Guru, S. C., Manickam, P., Olufemi, S. E., Yu, F., Heppner, C., Crabtree, J. S., Skarulis, M. C., Venzon, D. J., Emmert-Buck, M. R., Spiegel, A. M., Chandrasekharappa, S. C., Collins, F. S., Burns, A. L., Marx, S. J., and Lubensky, I. A. (1997) Somatic mutations of the MEN1 tumor suppressor gene in sporadic gastrinomas and insulinomas. Cancer Res. 57, 4682-4686 (Pubitemid 27468966)
34. Semache, M., Zarrouki, B., Fontés, G., Fogarty, S., Kikani, C., Chawki, M. B., Rutter, J., and Poitout, V. (2013) Per-Arnt-Sim kinase regulates pancreatic duodenal homeobox-1 protein stability via phosphorylation of glycogen synthase kinase 3β in pancreatic β-cells. J. Biol. Chem. 288, 24825-24833
35. Rocques, N., Abou Zeid, N., Sii-Felice, K., Lecoin, L., Felder-Schmittbuhl, M. P., Eychène, A., and Pouponnot, C. (2007) GSK-3-mediated phosphorylation enhances Maf-transforming activity. Mol. Cell. 28, 584-597 (Pubitemid 350137803)
36. Greenblatt, D. Y., Ndiaye, M., Chen, H., and Kunnimalaiyaan, M. (2010) Lithium inhibits carcinoid cell growth in vitro. Am. J. Transl. Res. 2, 248-253
37. Cao, Q., Lu, X., and Feng, Y. J. (2006) Glycogen synthase kinase-3 β positively regulates the proliferation of human ovarian cancer cells. Cell Res. 16, 671-677 (Pubitemid 44091443)
38. Chen, G., A. J., Wang, M., Farley, S., Lee, L. Y., Lee, L. C., and Sawicki, M. P. (2008) Menin promotes the Wnt signaling pathway in pancreatic endocrine cells. Mol. Cancer Res. 6, 1894-1907
39. Rulifson, I. C., Karnik, S. K., Heiser, P. W., ten Berge, D., Chen, H., Gu, X., Taketo, M. M., Nusse, R., Hebrok, M., and Kim, S. K. (2007) Wnt signaling regulates pancreatic beta cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 104, 6247-6252 (Pubitemid 47186080)
40. Geddes, J. R., Burgess, S., Hawton, K., Jamison, K., and Goodwin, G. M. (2004) Long-term lithium therapy for bipolar disorder. Systematic review and meta-analysis of randomized controlled trials. Am. J. Psychiatry 161, 217-222 (Pubitemid 38419270)