Multiple endocrine neoplasia type 1 (MEN1) as a cancer predisposition syndrome: Clues into the mechanisms of MEN1-related carcinogenesis

Yale Journal of Biology and Medicine

Volumn 79, Issue 3-4, 2006, Pages 105-114

  Busygina, Valeria ^a   Bale, Allen E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOSOMAL INHERITANCE; CANCER SUSCEPTIBILITY; CARCINOGENESIS; FAMILIAL CANCER; GENE INACTIVATION; HUMAN; MULTIPLE ENDOCRINE NEOPLASIA; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1 GENE; NONHUMAN; ONCOGENE; PANCREAS ISLET; PARATHYROID ADENOMA; REVIEW; BIOLOGICAL MODEL; GENETIC PREDISPOSITION; GENETICS; MUTATION; NERVOUS SYSTEM TUMOR; PATHOLOGY; PHYSIOLOGY; PRECANCER; RISK FACTOR;

MEN1 PROTEIN, HUMAN; ONCOPROTEIN; UNCLASSIFIED DRUG;

GENETIC PREDISPOSITION TO DISEASE; HUMANS; MODELS, BIOLOGICAL; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1; MUTATION; NERVOUS SYSTEM NEOPLASMS; PRECANCEROUS CONDITIONS; PROTO-ONCOGENE PROTEINS; RISK FACTORS;

EID: 38549160824     PISSN: 00440086     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (68)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57-70.
2. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 1996;87(2)159-70.
3. Cooper GM. Oncogenes. 2nd ed. Sudbury, Massachusetts: Jones and Bartlett Publishers;1995.
4. Sherr CJ. Principles of tumor suppression. Cell. 2004;116(2):235-46.
5. Cress WD, Seto E. Histone deacetylases, transcriptional control, and cancer. J Cell Physiol. 2000;184(1):1-16.
6. Knudson AG Jr. Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci USA. 1971;68(4):820-3.
7. Friend SH, Bernards R, Rogelj S, Weinberg RA, Rapaport JM, Albert DM, Dryja TP. A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma. Nature. 1986;323(6089):643-6.
8. Garber JE, Offit K. Hereditary cancer predisposition syndromes. J Clin Oncol. 2005;23(2):276-92.
9. Fearon ER. Human cancer syndromes: clues to the origin and nature of cancer. Science. 1997;278(5340):1043-50.
10. Mulligan LM, Eng C, Healey CS, Clayton D, Kwok JB, Gardner E, et al. Specific mutations of the RET proto-oncogene are related to disease phenotype in MEN 2A and FMTC. Nat Genet. 1994;6(1):70-4.
11. Schmidt L, Duh FM, Chen F, Kishida T, Glenn G, Choyke P, et al. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nat Genet. 1997;16(1):68-73.
12. Knudson AG. Antioncogenes and human cancer. Proc Natl Acad Sci USA. 1993;90(23):10914-21.
13. Cannon-Albright LA, Skolnick MH. The genetics of familial breast cancer. Semin Oncol. 1996;23(1 Suppl 2):1-5.
14. Lancaster JM, Wooster R, Mangion J, Phelan CM, Cochran C, Gumbs C, et al. BRCA2 mutations in primary breast and ovarian cancers. Nat Genet. 1996;13(2):238-40.
15. Miki Y, Katagiri T, Kasumi F, Yoshimoto T, Nakamura Y. Mutation analysis in the BRCA2 gene in primary breast cancers. Nat Genet. 1996;13(2):245-7.
16. Teng DH, Bogden R, Mitchell J, Baumgard M, Bell R, Berry S, et al. Low incidence of BRCA2 mutations in breast carcinoma and other cancers. Nat Genet. 1996;13(2):241-4.
17. Yuen ST, Chan TL, Ho JW, Chan AS, Chung LP, Lam PW, et al. Germline, somatic and epigenetic events underlying mismatch repair deficiency in colorectal and HNPCC-related cancers. Oncogene. 2002;21(49):7585-92.
18. Kinzler KW, Vogelstein B. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature. 1997;386(6627):761, 763.
19. Schussheim DH, Skarulis MC, Agarwal SK, Simonds WF, Burns AL, Spiegel AM, Marx SJ. Multiple endocrine neoplasia type 1: new clinical and basic findings. Trends Endocrinol Metab. 2001;12(4):173-8.
20. Trump D, Farren B, Wooding C, Pang JT, Besser GM, Buchanan KD, et al. Clinical studies of multiple endocrine neoplasia type 1 (MEN1). Qjm. 1996;89(9):653-69.
21. Agarwal SK, Lee Burns A, Sukhodolets KE, Kennedy PA, Obungu VH, Hickman AB, et al. Molecular pathology of the MEN1 gene. Ann NY Acad Sci. 2004;1014:189-98.
22. Larsson C, Skogseid B, Oberg K, Nakamura Y, Nordenskjold M. Multiple endocrine neoplasia type 1 gene maps to chromosome 11 and is lost in insulinoma. Nature. 1988;332 (6159):85-7.
23. Chandrasekharappa SC, Guru SC, Manickam P, Olufemi SE, Collins FS, Emmert-Buck MR, et al. Positional cloning of the gene for multiple endocrine neoplasia-type 1. Science. 1997;276(5311):404-7.
24. Lemmens I, Van de Ven WJ, Kas K, Zhang CX, Giraud S, Wautot V, et al. Identification of the multiple endocrine neoplasia type 1 (MEN1) gene. The European Consortium on MEN1. Hum Mol Genet. 1997;6(7):1177-83.
25. Guru SC, Goldsmith PK, Burns AL, Marx SJ, Spiegel AM, Collins FS, Chandrasekharappa SC. Menin, the product of the MEN1 gene, is a nuclear protein. Proc Natl Acad Sci USA. 1998;95(4):1630-4.
26. Bassett JH, Rashbass P, Harding B, Forbes SA, Pannett AA, Thakker RV. Studies of the murine homolog of the multiple endocrine neoplasia type 1 (MEN1) gene, men1. J Bone Miner Res. 1999;14(1):3-10.
27. Guru SC, Crabtree JS, Brown KD, Dunn KJ, Manickam P, Prasad NB, et al. Isolation, genomic organization, and expression analysis of Men1, the murine homolog of the MEN1 gene. Mamm Genome. 1999;10(6):592-6.
28. Stewart C, Parente F, Piehl F, Farnebo F, Quincey D, Silins G, et al. Characterization of the mouse Men1 gene and its expression during development. Oncogene. 1998;17(19):2485-93.
29. Agarwal SK, Guru SC, Heppner C, Erdos MR, Collins RM, Park SY, et al. Menin interacts with the AP1 transcription factor JunD and represses JunD-activated transcription. Cell. 1999;96(1):143-52.
30. Gallo A, Cuozzo C, Esposito I, Maggiolini M, Bonofiglio D, Vivacqua A, et al. Menin uncouples Elk-1, JunD and c-Jun phosphorylation from MAP kinase activation. Oncogene. 2002;21(42):6434-45.
31. Yumita W, Ikeo Y, Yamauchi K, Sakurai A, Hashizume K. Suppression of insulin-induced AP-1 transactivation by menin accompanies inhibition of c-Fos induction. Int J Cancer. 2003;103(6):738-44.
32. Heppner C, Bilimoria KY, Agarwal SK, Kester M, Whitty LJ, Guru SC, et al. The tumor suppressor protein menin interacts with NF-kappaB proteins and inhibits NFkappaB-mediated transactivation. Oncogene. 2001;20(36):4917-25.
33. Kaji H, Canaff L, Lebrun JJ, Goltzman D, Hendy GN. Inactivation of menin, a Smad3-interacting protein, blocks transforming growth factor type beta signaling. Proc Natl Acad Sci USA. 2001;98(7):3837-42.
34. Lemmens IH, Forsberg L, Pannett AA, Meyen E, Piehl F, Turner JJ, et al. Menin interacts directly with the homeobox-containing protein Pem. Biochem Biophys Res Commun. 2001;286(2):426-31.
35. Chandrasekharappa SC, Teh BT. Functional studies of the MEN1 gene. J Intern Med. 2003;253(6):606-15.
36. La P, Silva AC, Hou Z, Wang H, Schnepp RW, Yan N, et al. Direct binding of DNA by tumor suppressor menin. J Biol Chem. 2004;279(47):49045-54.
37. Kim H, Lee JE, Cho EJ, Liu JO, Youn HD. Menin, a tumor suppressor, represses JunD-mediated transcriptional activity by association with an mSin3A-histone deacetylase complex. Cancer Res. 2003;63(19):6135-9.
38. Yokoyama A, Wang Z, Wysocka J, Sanyal M, Aufiero DJ, Kitabayashi I, et al. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol. 2004;24(13):5639-49.
39. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, et al. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell. 2004;13(4):587-97.
40. Milne TA, Hughes CM, Lloyd R, Yang Z, Rozenblatt-Rosen O, Dou Y, et al. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc Natl Acad Sci USA. 2005;102(3):749-54.
41. Yokoyama A, Somervaille TC, Smith KS, Rozenblatt-Rosen O, Meyerson M, Cleary ML. The menin tumor suppressor protein is an essential oncogenic cofactor for MLL-associated leukemogenesis. Cell. 2005;123(2):207-18.
42. Scacheri PC, Davis S, Odom DT, Crawford GE, Perkins S, Halawi MJ, et al. Genome-wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet. 2006;2(4):e51.
43. Agarwal SK, Impey S, McWeeney S, Scacheri PC, Collins FS, Goodman RH, et al. Distribution of menin-occupied regions in chromatin specifies a broad role of menin in transcriptional regulation. Neoplasia. 2007;9(2):101-7.
44. Itakura Y, Sakurai A, Katai M, Ikeo Y, Hashizume K. Enhanced sensitivity to alkylating agent in lymphocytes from patients with multiple endocrine neoplasia type 1. Biomed Pharmacother. 2000;54 Suppl 1:187s-90s.
45. Jin S, Mao H, Schnepp RW, Sykes SM, Silva AC, D'Andrea AD, Hua X. Menin associates with FANCD2, a protein involved in repair of DNA damage. Cancer Res. 2003;63(14):4204-10.
46. Sukhodolets KE, Hickman AB, Agarwal SK, Sukhodolets MV, Obungu VH, Novotny EA, et al. The 32-kilodalton subunit of replication protein A interacts with menin, the product of the MEN1 tumor suppressor gene. Mol Cell Biol. 2003;23(2):493-509.
47. Binz SK, Sheehan AM, Wold MS. Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair (Amst). 2004;3(8-9):1015-24.
48. Busygina V, Suphapeetiporn K, Marek LR, Stowers RS, Xu T, Bale AE. Hypermutability in a Drosophila model for multiple endocrine neoplasia type 1. Hum Mol Genet. 2004;13(20):2399-408.
49. Busygina V, Kottemann MC, Scott KL, Plon SE, Bale AE. Multiple Endocrine Neoplasia Type 1 Interacts with Forkhead Transcription Factor CHES1 in DNA Damage Response. Cancer Res. 2006;66(17):8397-403.
50. Kim YS, Burns AL, Goldsmith PK, Heppner C, Park SY, Chandrasekharappa SC, et al. Stable overexpression of MEN1 suppresses tumorigenicity of RAS. Oncogene. 1999;18(43):5936-42.
51. 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(5):549-60.
52. Schnepp RW, Hou Z, Wang H, Petersen C, Silva A, Masai H, Hua X. Functional interaction between tumor suppressor menin and activator of S-phase kinase. Cancer Res. 2004;64(18):6791-6.
53. Biondi CA, Gartside MG, Waring P, Loffler KA, Stark MS, Magnuson MA, et al. Conditional inactivation of the MEN1 gene leads to pancreatic and pituitary tumorigenesis but does not affect normal development of these tissues. Mol Cell Biol. 2004;24(8):3125-31.
54. Crabtree JS, Scacheri PC, Ward JM, Garrett-Beal L, Emmert-Buck MR, Edgemon KA, et al. A mouse model of multiple endocrine neoplasia, type 1, develops multiple endocrine tumors. Proc Natl Acad Sci USA. 2001;98(3):1118-23.
55. Crabtree JS, Scacheri PC, Ward JM, McNally SR, Swain GP, Montagna C, et al. Of mice and MEN1: Insulinomas in a conditional mouse knockout. Mol Cell Biol. 2003;23(17):6075-85.
56. Suphapeetiporn K, Greally JM, Walpita D, Ashley T, Bale AE. MEN1 tumor-suppressor protein localizes to telomeres during meiosis. Genes Chromosomes Cancer. 2002;35 (1):81-5.
57. Lin SY, Elledge SJ. Multiple tumor suppressor pathways negatively regulate telomerase. Cell. 2003;113(7):881-9.
58. Lopez-Egido J, Cunningham J, Berg M, Oberg K, Bongcam-Rudloff E, Gobl A. Menin's interaction with glial fibrillary acidic protein and vimentin suggests a role for the intermediate filament network in regulating menin activity. Exp Cell Res. 2002;278(2):175-83.
59. Obungu VH, Lee Burns A, Agarwal SK, Chandrasekharapa SC, Adelstein RS, Marx SJ. Menin, a tumor suppressor, associates with nonmuscle myosin II-A heavy chain. Oncogene. 2003;22(41):6347-58.
60. Heasley LE, Han SY. JNK regulation of oncogenesis. Mol Cells. 2006;21(2):167-73.
61. Zebisch A, Czernilofsky AP, Keri G, Smigelskaite J, Sill H, Troppmair J. Signaling through RAS-RAF-MEK-ERK: from basics to bedside. Curr Med Chem. 2007;14(5):601-23.
62. Matsuzaki K, Okazaki K. Transforming growth factor-beta during carcinogenesis: the shift from epithelial to mesenchymal signaling. J Gastroenterol. 2006; 41(4):295-303.
63. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol. 2005;5(10):749-59.
64. Pei XH, Bai F, Smith MD, Xiong Y. p18Ink4c Collaborates with Men1 to Constrain Lung Stem Cell Expansion and Suppress Non-Small-Cell Lung Cancers. Cancer Res. 2007;67(7):3162-70.
65. Bai F, Pei XH, Nishikawa T, Smith MD, Xiong Y. p18Ink4c, but not p27Kip1, collaborates with Men1 to suppress neuroendocrine organ tumors. Mol Cell Biol. 2007;27 (4):1495-504.
66. Morrison AJ, Shen X. Chromatin modifications in DNA repair. Results Probl Cell Differ. 2006; 41:109-25.
67. Sung P, Klein H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol. 2006;7(10):739-50.
68. Staalesen V, Falck J, Geisler S, Bartkova J, Borresen-Dale AL, Lukas J, et al. Alternative splicing and mutation status of CHEK2 in stage III breast cancer. Oncogene. 2004;23 (52):8535-44.