Recapitulation of pancreatic neuroendocrine tumors in human multiple endocrine neoplasia type I syndrome via Pdx1-directed inactivation of men 1

Cancer Research

Volumn 69, Issue 5, 2009, Pages 1858-1866

  Jennifer Shen, H C ^a   He, Mei ^a   Powell, Anathea ^a   Adem, Asha ^a   Lorang, Dominique ^a   Heller, Charles ^a   Grover, Amelia C ^a   Ylaya, Kris ^a   Hewitt, Stephen M ^b   Marx, Stephen J ^b   Spiegel, Allen M ^c   Libutti, Steven K ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

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

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHIONINE; TRANSCRIPTION FACTOR PDX 1; VASCULOTROPIN; HOMEODOMAIN PROTEIN; INSULIN PROMOTER FACTOR 1; MEN1 PROTEIN, HUMAN; MEN1 PROTEIN, MOUSE; ONCOPROTEIN; TRANSACTIVATOR PROTEIN; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; GENE FREQUENCY; GENE INACTIVATION; GENE LOSS; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROENVIRONMENT; MOUSE; MULTIPLE ENDOCRINE NEOPLASIA; NEUROENDOCRINE TUMOR; NONHUMAN; PANCREAS; PANCREAS TUMOR; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; STEM CELL; UPREGULATION; VASCULARIZATION; ANIMAL; PANCREAS ISLET; PHYSIOLOGY;

ANIMALS; CELL PROLIFERATION; HOMEODOMAIN PROTEINS; HUMANS; ISLETS OF LANGERHANS; MICE; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; TRANS-ACTIVATORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 62449205669     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-3662     Document Type: Article

References (49)

1. Chandrasekharappa SC, Guru SC, Manickam P, et al. Positional cloning of the gene for multiple endocrine neoplasia-type 1. Science 1997;276:404-07
2. Lemmens I, Van de Ven WJ, Kas K, et al. Identification of the multiple endocrine neoplasia type 1 (MEN1) gene. The European Consortium on MEN1. Hum Mol Genet 1997;6:1177-83.
3. Marx S, Spiegel AM, Skarulis MC, Doppman JL, Collins FS, Llotta LA. Multiple endocrine neoplasia type I: clinical and genetic topics. Ann Intern Med 1998:129: 484-94.
4. Trump D, Farren B, Wooding C, et al. Clinical studies of multiple endocrine neoplasia type 1 (MENl). O Jm 1996;89:653-69.
5. Stratakis CA, Schussheim DH, Freedman SM, et al. Pituitary macroadenoma in. a 5-year-old: an. early expression of multiple endocrine neoplasia type 1. J Clin Endocrinol Metab 2000;85:4776-4780.
6. Knudson AG, Jr. Mutation, and cancer: statistical study of retinoblastoma. Proc Natl Acad Sei USA. 1971:68: 820-823.
7. Guru SC, Manickam P1 Crabtree JS1 Olufemi SE1 Agarwal SK, Debelenko LV. Identification and charac-terization of the multiple endocrine neoplasia type I (MENl) gene. J Intern Med 1998;243:433-39
8. Ludwig L, Schleithoff L, Kessler H, Wagner PK, Boehm BO, Karges W. Loss of wild-type MENI gene expression in multiple endocrine neoplasia type 1-associated parathyroid adenoma Endocr J 1999;46:539-44.
9. Valdês N, Alvarez V, Diaz-Cadorniga F, et al. Multiple endocrine neoplasia type I (MENl): LOH studies in a affected family and in sporadic cases. Anticancer Res 1998:18:2685-2689.
10. Heppner C, Rester MB, Agarwal SK, et al. Somatic mutation of the MENl gene in parathyroid tumours. Nat Genet 1997;16:375-78.
11. Wang EH, Ebrahimi SA, Wu AY, Kashefi C, Pássaro E, Jr., Sawicki MP. Mutation of the MENIN gene in sporadic pancreatic endocrine tumors. Cancer Res 1998;58:4417-4420.
12. Lemos MC, Thakker RV. Multiple endocrine neoplasia type 1 (MENI): analysis of 1.336 mutations reported in the first decade following identification of the gene. Hum Mutat 2008;29:22-32.
13. Agarwal SK, Kennedy PA, Scacheri PC, et al. Menin molecular interactions: insights into normal functions and tumorigenesis. Horm Metab Res 2005;37:369-374.
14. Balogli K, Racz K, Patocs A, Hunyady L. Menin and its interacting proteins: elucidation of menin function. Trends Endocrinol Metab 2006;17:357-364.
15. Hughes CM, Rozenblatt-Rosen O, Milne TA1 et al. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. MoI Cell 2004;13:587-597.
16. Chen YX, Yan J1 Keeshan K, et al. The tumor suppressor menin regulates hematopoiesis and myeloid transformation by influencing Hox gene expression. Proc Natl Acad Sei U S A 2006;103:1018-23
17. Yokoyama A, Somervaille TC, Smith KS, Rozen-blatt-Rosen O, Meyerson M, Cleary ML. The menin tumor suppressor protein is an essential oncogenic cofactor for MLL-associated leukemogenesis. Cell 2005;123:207-218.
18. Yokoyama A, Wang Z, Wysocka J, et al. Leukemia proto-oncoprotein. MLL forms a SETI.-like histone methyltransferase complex with menin to regulate Hox gene expression. MoI Cell Biol 2004;24:5639-5649.
19. Karnik SK, Hughes CM, Gu X, et al. Menin regulates pancreatic islet growth by promoting histone methyla-tion and expression of genes encoding p27Kipl and pl8INK4c. Proc Natl Acad Sei U S A 2005;102:14659-14664
20. Karnik SK, Chen H, McLean GW, et al. Menin controls growth of pancreatic-cells in pregnant mice and promotes gestational diabetes mellitus. Science 2007;318:806-09.
21. Bertolino P, Tong WM, Galendo D, Wang ZQ, Zhang CX. Heterozygous Menl. mutant mice develop a range of endocrine tumors mimicking multiple endocrine neo-plasia type 1. MoI Endocrinol 2003;17:1880-92.
22. Crabtree JS, Scacheri PC, Ward JM, et al. A mouse model of multiple endocrine neoplasia, type I, develops multiple endocrine tumors. Proc Natl Acad Sei U S A 2001;98:1118-1123.
23. Loffler KA, Biondi CA, Gartslde M, et al. Broad tumor spectrum in a mouse model of multiple endocrine neoplasia type 1. Int J Cancer 2007;120:259-267.
24. Basse JH, Rashbass P1 Harding B1 Forbes SA, Pannett AA, Thakker RV. Studies of the murine homolog of the multiple endocrine neoplasia type I (MENI) gene, menl. J Bone Miner Res 1999;14:3-10.
25. Guru. SC, Crabtree JS, Brown KD, et al. Isolation, genomic organization, and expression analysis of Menl, the murine homolog of the MENl gene. Mamm Genome 1999;10:592-96.
26. Bertolino P, Radovanovic I, Casse H, Aguzzi A, Wang ZQ, Zhang CX. Genetic ablation of the tumor suppressor menin causes lethality at mid-gestation with defects in multiple organs. Mech Dev 2003:120: 549-560.
27. Libuttl SK, Crabtree JS, Lorang D, et al. Parathyroid gland-specific deletion of the mouse Menl gene results in parathyroid neoplasia and hypercalcémie hyperpara-thyroidism. Cancer Res 2003;63:8022-28.
28. Bertolino P, Tong WM, Herrera PL, Casse H, Zhang CX, Wang ZQ. Pancreatic-cell-specific ablation of the multiple endocrine neoplasia type 1 (MENl) gene causes full penetrance of Insulinoma development in mice. Cancer Res 2003;63:4836-41.
29. Crabtree JS, Scacheri PC, Ward JM, et al. Of mice and MENl: insulinomas in a conditional mouse knockout. MoI Cell Biol 2003;23:6075-6085.
30. Biondi CA, Gartside MG, Waring P, et al. Conditional, inactivation of the MENl gene leads to pancreatic and pituitary tumorigenesis but does not affect normal development of these tissues. MoI Cell Biol 2004:24: 3125-3131.
31. Stewart C, Parente F, Piehl F, et al. Characterization of the mouse Menl gene and its expression during development. Oncogene 1998;17:2485-2493.
32. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002;129:2447-2457.
33. Thurston G, Baluk P, Hirata A, McDonald DM. Permeability-related changes revealed at endothelial cell borders in inflamed venules by lectin binding. Am J Physiol 1996;271:2547-62.
34. Blansfield JA, Caragacianu. D, Alexander HR III, et al. Combining agents that target the tumor microenviron-ment improves the efficacy of anticancer therapy. Clin Cancer Res 2008;14:270-80.
35. Chow LQ, Eckhardt SG. Sunitinib: from rational design to clinical efficacy. J CUn Oncol 2007;25:884-896.
36. Schnepp RW, Chen. YX, Wang H, et al. Mutation, of tumor suppressor gene Menl acutely enhances prolif-eration of pancreatic islet cells. Cancer Res 2006:66: 5707-1.5.
37. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005;438:932-936.
38. Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 1989;339:58-61.
39. Mendel DB, Laird AD, Xin X, et al. In vivo antitumor activity of SUI1248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and plate-let-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 2003;9:327-337.
40. Scacheri PC, Crabtree JS, Kennedy AL, et al. Homozygous loss of menin is well tolerated in liver, a tissue not affected in MENl. Mamm Genome 2004:15: 872-877.
41. BaI F, Pei XH, Nishikawa T, Smith MD, Xiong Y. p,18Ink4c, but not p27.K.ipl, collaborates with Menl to suppress neuroendocrine organ tumors. MbI Cell Biol 2007;27:1495-1504.
42. Franklin DS, Godfrey VI, O'Brien DA, Deng C, Xiong Y. Functional collaboration between different cyclin-dependent kinase inhibitors suppresses tumor growth with distinct tissue specificity. MoI Cell Biol 2000;20: 6147-6158.
43. Lammert E, Gu G, McLaughlin M, et al. Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 2003;13:1070-74
44. Jiang FX, Naseli! G, Harrison LC. Distinct distribution of laminin and its integrin receptors in the pancreas. J Histochem Cytochem 2002;50:1625-1632.
45. Nikolova G, Jabs N, Konstantinova I, et al. The vascular basement membrane: a niche for insulin gene expression, and cell proliferation. Dev Cell 2006:10: 397-405.
46. Korsisaari N, Ross J, Wu X, et al. Blocking vascular endothelial growth factor-A inhibits the growth of pituitary adenomas and lowers serum, prolactin level in a mouse model of multiple endocrine neoplasia type 1. Clin Cancer Res 2008;14:249-258.
47. Fabian MA, Biggs WH Hi, Treiber DK, et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat Biotechnol 2005;23:329-336.
48. Hanahan D. Heritable formation of pancreatic-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature 1985:315: 115-22
49. Inoue M Hager J.H Ferrara N Gerber HPHanahan D, VEGF-A has a critical, nonredundant role in. angiogenic switching and pancreatic cell carcinogenesis. Cancer Cell 2002;1:193-202.