Conditional Inactivation of the Men1 Gene Leads to Pancreatic and Pituitary Tumorigenesis but Does Not Affect Normal Development of These Tissues

Molecular and Cellular Biology

Volumn 24, Issue 8, 2004, Pages 3125-3131

  Biondi, Christine A ^a,e   Gartside, Michael G ^a   Waring, Paul ^b,c   Loffler, Kelly A ^a   Stark, Mitchell S ^a   Magnuson, Mark A ^d   Kay, Graham F ^a   Hayward, Nicholas K ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; GENE PRODUCT; METHIONINE; PROTEIN;

ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; EMBRYO; GENE INACTIVATION; GENE MUTATION; GENE TARGETING; GENOTYPE; HYPOPHYSIS TUMOR; INSULINOMA; KNOCKOUT GENE; MEN1 GENE; MOUSE; MULTIPLE ENDOCRINE NEOPLASIA; NONHUMAN; ORGANOGENESIS; PANCREAS ISLET; PANCREAS ISLET CELL HYPERPLASIA; PANCREAS TUMOR; PARATHYROID TUMOR; PRIORITY JOURNAL; PROLACTINOMA; TUMOR SUPPRESSOR GENE;

ANIMALS; EMBRYO; EXONS; FEMALE; GENE SILENCING; HYPERPLASIA; INSULINOMA; INTEGRASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1; PANCREAS; PANCREATIC NEOPLASMS; PITUITARY GLAND; PITUITARY NEOPLASMS; PROLACTINOMA; TRANSGENES; VIRAL PROTEINS;

ANIMALIA; MURINAE;

EID: 1842557785     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.8.3125-3131.2004     Document Type: Article

References (36)

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 API transcription factor JunD and represses JunD-activated transcription. Cell 96:143-152.
2. 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.
3. Bertolino, P., W. M. Tong, D. Galendo, Z. Q. Wang, and C. X. Zhang. 2003. Heterozygous Men1 mutant mice develop a range of endocrine tumors mimicking multiple endocrine neoplasia type 1. Mol. Endocrinol. 11:1880-1892.
4. Bertolino, P., W. M. Tong, P. L. Herrera, H. Casse, C. X, Zhang, and Z. Q. Wang. 2003. Pancreatic beta-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.
5. Biondi, C., M. Gartside, I. Tonks, C. Paterson, N. K. Hayward, and G. F. Kay. 2002. Targeting and conditional inactivation of the murine Men1 locus using the Cre recombinase:loxP system. Genesis 32:150-151.
6. 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, V. 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 276:404-407.
7. Crabtree, J. S., P. C. Scacheri, J. M. Ward. L. Garrett-Beal, M. R. Emmert-Buck, K. A. Edgemon D. Lorang. S. K. Libutti, S. C. Chandrasekharappa, S. J. Marx, A. M. Spiegel, and F. S. Collins. 2001. A mouse model of multiple endocrine neoplasia, type 1, develops multiple endocrine tumors. Proc. Natl. Acad. Sci. USA 98:1118-1123.
8. Crabtree, J. S., P. C. Scacheri, J. M. Ward. S. R. McNally, G. P. Swain, C. Montagna, J. H. Hager, D. Hanaman, H. Edlund, M. A. Magnuson, L. Garrett-Beal, A. L. Burns, T. Ried, S. C. Chandrasekharappa, S. J. Marx, A. M. Spiegel, and F. S. Collins. 2003. Of mice and MEN1: insulinomas in a conditional mouse knockout. Mol. Cell. Biol. 23:6075-6085.
9. Gallo, A., C. Cuozzo, I. Esposito, M. Maggiolini, D. Bonoliglio, A. Vivacqua, M. Garramone, C. Weiss, D. Bohmann, and A. M. Musti. 2002. Menin uncouples Elk-1, JunD and c-Jun phosphorylation from MAP kinase activation. Oncogene 21:6434-6445.
10. Gannon, M., C. Shiota, C. Postic, C. V. Wright, and M. Magnuson. 2000. Analysis of the Cre-mediated recombination driven by rat insulin promoter in embryonic and adult mouse pancreas. Genesis 26:139-142.
11. Guru, S. C., N. B. Prasad, E. J. Shin, K. Hemavathy, J. Lu, Y. T. Ip, S. K. Agarwal, S. J. Marx, A. M. Spiegel, F. S. Collins, B. Oliver, and S. C. Chandrasekharappa. 2001. Characterization of a MEN1 ortholog from Drosophila melanogaster. Gene 263:31-38.
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. Heppner, C., M. B. Kester, S. K. Agarwal, L. V. Debelenko, M. R. Emmert-Buck, S. C. Guru, P. Manickam, S. E. Olufemi, M. C. Skarulis, J. L. Doppman, R. H. Alexander, Y. S. Kim, S. K. Saggar, I. A. Lubensky, Z. Zhuang, L. A. Liotta, S. C. Chandrasekharappa, F. S. Collins, A. M. Spiegel, A. L. Burns, and S. J. Marx. 1997. Somatic mutation of the MEN1 gene in parathyroid tumours. Nat. Genet. 16:375-378.
14. 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-kappaB proteins and inhibits NF-kappaB-mediated transactivation. Oncogene 20:4917-4925.
15. Jin, S., H. Mao, R. W. Schnepp, S. M. Sykes, A. C. Silva, A. D. D'Andrea, and X. Hua. 2003. Menin associates with FANCD2, a protein involved in repair of DNA damage. Cancer Res. 63:4204-4210.
16. Kaji, H., L. Canaff, D. Goltzman, and G. N. Hendy. 1999. Cell cycle regulation of menin expression. Cancer Res. 59:5097-5101.
17. 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 beta signaling. Proc. Natl. Acad. Sci. USA 98:3837-3842.
18. Karges, W., S. Maier, A. Wissmann, H. Dralle, H. M. Dosch, and B. O. Boehm. 1999. Primary structure, gene expression and chromosomal mapping of rodent homologs of the MEN1 tumor suppressor gene. Biochim. Biophys. Acta 1446:286-294.
19. Khodaei, S., K. P. O'Brien, J. Dumanski, F. K. Wong, and G. Weber. 1999. Characterization of the MEN1 ortholog in zebrafish. Biochem. Biophys. Res. Commun. 264:404-408.
20. Ki Wong, F., J. Burgess, M. Nordenskjold, C. Larsson, and B. Tean Teh. 2000. Multiple endocrine neoplasia type 1. Semin. Cancer Biol. 10:299-312.
21. Lemmens, I., W. J. Van de Ven, K. Kas, C. X. Zhang, S. Giraud, V. Wautot, N. Buisson, K. De Witte, J. Salandre, G. Lenoir, M. Pugeat, A. Calender, F. Parente, D. Quincey, P. Gaudray, M. J. De Wit, C. J. Lips, J. W. Hoppener, S. Khodaei, A. L. Grant, G. Weber, S. Kytola, B. T. Teh, F. Farnebo, and R. V. Thakker. 1997. Identification of the multiple endocrine neoplasia type 1 (MEN1) gene. The European Consortium on MEN1. Hum. Mol. Genet. 6:1177-1183.
22. Lemmens, I. H., L. Forsberg, A. A. Pannett, E. Meyen, F. Piehl, J. J. Turner, W. J. Van de Ven, R. V. Thakker, C. Larsson, and K. Kas. 2001. Menin interacts directly with the homeobox-containing protein Pem. Biochem. Biophys. Res. Commun. 286:426-431.
23. Lobe, C. G., K. E. Koop, W. Kreppner, H. Lomeli, M. Gertsenstein, and A. Nagy. 1999. Z/AP, a double reporter for Cre-mediated recombination. Dev. Biol. 208:281-292.
24. Mahler, J. F., and M. Elwell. 2002. Pituitary gland, p. 491-507. In R. R. Maronpot (ed.), Pathology of the mouse, vol. 1. Cache River Press, Vienna, Ill.
25. Manickam, P., A. M. Vogel, S. K. Agarwal, T. Oda, A. M. Spiegel, S. J. Marx, F. S. Collins, B. M. Weinstein, and S. C. Chandrasekharappa. 2000. Isolation, characterization, expression and functional analysis of the zebrafish ortholog of MEN1. Mamm. Genome 11:448-454.
26. Maruyama, K., T. Tsukada, M. Honda, N. Nara-Ashizawa, K. Noguchi, J. Cheng, N. Ohkura, K. Sasaki, and K. Yamaguchi. 2000. Complementary DNA structure and genomic organization of Drosophila menin. Mol. Cell. Endocrinol. 168:135-140.
27. Postic, C., M. Shiota, K. D. Niswender, T. L. Jetton, Y. Chen, J. M. Moates, K. D. Shelton, J. Lindner, A. D. Cherrington, and M. A. Magnuson. 1999. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic β cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem. 274:305-315.
28. Sauer, B., and N. Henderson. 1988. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc. Natl. Acad. Sci. USA 85:5166-5170.
29. Stewart, C., F. Parente, F. Piehl, F. Farnebo, D. Quincey, G. Silins, L. Bergman, G. F. Carle, I. Lemmens, S. Grimmond, C. Z. Xian, S. Khodei, B. T. Teh, J. Lagercrantz, P. Siggers, A. Calender, V. Van de Vem, K. Kas, G. Weber, N. Hayward, P. Gaudray, and C. Larsson. 1998. Characterization of the mouse Men1 gene and its expression during development. Oncogene 17:2485-2493.
30. Sukhodolets, K. E., A. B. Hickman, S. K. Agarwal, M. V. Sukhodolets, V. H. Obungu, E. A. Novotny, J. S. Crabtree, S. C. Chandrasekharappa, F. S. Collins, A. M. Spiegel, A. L. Burns, and S. J. Marx. 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.
31. van Kesteren, R. E., N. I. Syed, D. W. Munno, Bouwman, Z. P. J., Feng, W. P. Geraerts, and A. B. Smit. 2001. Synapse formation between central neurons requires postsynaptic expression of the MEN1 tumor suppressor gene. J. Neurosci. 21:RC161.
32. Wautot, V., S. Khodaei, L. Frappart, N. Buisson, E. Baro, G. M. Lenoir, A. Calender, C. X. Zhang, and G. Weber. 2000. Expression analysis of endogenous menin, the product of the multiple endocrine neoplasia type 1 gene, in cell lines and human tissues. Int. J. Cancer 85:877-881.
33. Williams, B. O., L. Remington, D. M. Albert, S. Mukai, R. T. Bronson, and T. Jacks. 1994. Cooperative tumorigenic effects of germline mutations in Rb and p53. Nat. Genet. 7:480-484.
34. Yumita, Y. W., Ikeo, K. Yamauchi, A. Sakurai, and K. Hashizume. 2003. Suppression of insulin-induced AP-1 transactivation by menin accompanies inhibition of c-Fos induction. Int. J. Cancer 103:738-744.
35. Zhuang, Z., A. O. Vortmeyer, S. Pack, S. Huang, T. A. Pham, C. Wang, W. S. Park, S. K. Agarwal, L. V. Debelenko, M. Kester, S. C. Guru, P. Manickam, S. E. Olufemi, F. Yu, C. Heppner, J. S. Crabtree, M. C. Skarulis, D. J. Venzon, M. R. Emmert-Buck, A. M. Spiegel, S. C. Chandrasekharappa, F. S. Collins, A. L. Burns, S. J. Marx, and I. A. Lubensky. 1997. Somatic mutations of the MEN1 tumor suppressor gene in sporadic gastrinomas and insulinomas. Cancer Res. 57:4682-4686.
36. Zhuang, Z., S. Z. Ezzat, A. O. Vortmeyer, R. Weil, E. H. Oldfield, W. S. Park, S. Pack, S. Huang, S. K. Agarwal, S. C. Guru, P. Manickam, L. V. Debelenko, M. B. Kester, S. E. Olufemi, C. Heppner, J. S. Crabtree, A. L. Burns, A. M. Spiegel, S. J. Marx, S. C. Chandrasekharappa, F. S. Collins, M. R. Emmert-Buck, L. A. Liotta, S. L. Asa, and I. A. Lubensky. 1997. Somatic mutations of the MEN1 tumor suppressor gene in pituitary tumors. Cancer Res. 57:5446-5451.