Menin Is a Regulator of the Stress Response in Drosophila melanogaster

REFERENCES

• Abrams, J. M., K. White, L. I. Fessler, and H. Steller. 1993. Programmed cell death during Drosophila embryogenesis. Development 117:29–43.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Agarwal, S. K., M. B. Kester, L. V. Debelenko, C. Heppner, M. R. Emmert-Buck, M. C. Skarulis, J. L. Doppman, Y. S. Kim, I. A. Lubensky, Z. Zhuang, J. S. Green, S. C. Guru, P. Manickam, S. E. Olufemi, L. A. Liotta, S. C. Chandrasekharappa, F. S. Collins, A. M. Spiegel, A. L. Burns, and S. J. Marx. 1997. Germline mutations of the MEN1 gene in familial multiple endocrine neoplasia type 1 and related states. Hum. Mol. Genet. 6:1169–1175.
   PubMed Web of Science ®Google Scholar
• Andrulis, E. D., E. Guzman, P. Doring, J. Werner, and J. T. Lis. 2000. High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation. Genes Dev. 14:2635–2649.
   PubMed Web of Science ®Google Scholar
• Boellmann, F., T. Guettouche, Y. Guo, M. Fenna, L. Mnayer, and R. Voellmy. 2004. DAXX interacts with heat shock factor 1 during stress activation and enhances its transcriptional activity. Proc. Natl. Acad. Sci. USA 101:4100–4105.
   PubMedGoogle Scholar
• Busygina, V., K. Suphapeetiporn, L. R. Marek, R. S. Stowers, T. Xu, and A. E. Bale. 2004. Hypermutability in a Drosophila model for multiple endocrine neoplasia type 1. Hum. Mol. Genet. 13:2399–2408.
   PubMedGoogle Scholar
• Cavalli, G., and R. Paro. 1999. Epigenetic inheritance of active chromatin after removal of the main transactivator. Science 286:955–958.
   PubMed Web of Science ®Google Scholar
• 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 276:404–407.
   PubMed Web of Science ®Google Scholar
• Elefant, F., and K. B. Palter. 1999. Tissue-specific expression of dominant negative mutant Drosophila HSC70 causes developmental defects and lethality. Mol. Biol. Cell. 10:2101–2117.
   PubMedGoogle Scholar
• Feder, M. E., N. V. Cartano, L. Milos, R. A. Krebs, and S. L. Lindquist. 1996. Effect of engineering Hsp70 copy number on Hsp70 expression and tolerance of ecologically relevant heat shock in larvae and pupae of Drosophila melanogaster. J. Exp. Biol. 199:1837–1844.
   PubMedGoogle Scholar
• Feder, M. E., and G. E. Hofmann. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61:243–282.
   PubMed Web of Science ®Google Scholar
• Fridell, Y. W., and L. L. Searles. 1992. In vivo transcriptional analysis of the TATA-less promoter of the Drosophila melanogaster vermilion gene. Mol. Cell. Biol. 12:4571–4577.
   PubMed Web of Science ®Google Scholar
• Gallo, A., C. Cuozzo, I. Esposito, M. Maggiolini, D. Bonofiglio, 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.
   PubMedGoogle Scholar
• Gerber, M., K. Tenney, J. W. Conaway, R. C. Conaway, J. C. Eissenberg, and A. Shilatifard. 2005. Regulation of heat shock gene expression by RNA polymerase II elongation factor, elongin A. J. Biol. Chem. 280:4017–4020.
   PubMedGoogle Scholar
• Gong, W. J., and K. G. Golic. 2004. Genomic deletions of the Drosophila melanogaster Hsp70 genes. Genetics 168:1467–1476.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Honda, Y., and S. Honda. 1999. The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J. 13:1385–1393.
   PubMed Web of Science ®Google Scholar
• Hughes, C. M., O. Rozenblatt-Rosen, T. A. Milne, T. D. Copeland, S. S. Levine, J. C. Lee, D. N. Hayes, K. S. Shanmugam, A. Bhattacharjee, C. A. Biondi, G. F. Kay, N. K. Hayward, J. L. Hess, and M. Meyerson. 2004. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol. Cell. 13:587–597.
   PubMed Web of Science ®Google Scholar
• Ikeo, Y., A. Sakurai, and K. Hashizume. 1999. Characterization of the MEN1 gene product, menin, by site-specific polyclonal antibodies. Jpn. J. Cancer Res. 90:1088–1095.
   PubMedGoogle Scholar
• Inoue, H., M. Tateno, K. Fujimura-Kamada, G. Takaesu, T. Adachi-Yamada, J. Ninomiya-Tsuji, K. Irie, Y. Nishida, and K. Matsumoto. 2001. A Drosophila MAPKKK, D-MEKK1, mediates stress responses through activation of p38 MAPK. EMBO J. 20:5421–5430.
   PubMed Web of Science ®Google Scholar
• Jarecki, J., E. Johnson, and M. A. Krasnow. 1999. Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 99:211–220.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kim, H., J. E. Lee, E. J. Cho, J. O. Liu, and H. D. Youn. 2003. Menin, a tumor suppressor, represses JunD-mediated transcriptional activity by association with an mSin3A-histone deacetylase complex. Cancer Res. 63:6135–6139.
   PubMedGoogle Scholar
• Krebs, R. A., and M. E. Feder. 1998. Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is more too much. J. Insect Physiol. 44:1091–1101.
   PubMed Web of Science ®Google Scholar
• 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, R. V. Thakker, et al. 1997. Identification of the multiple endocrine neoplasia type 1 (MEN1) gene. The European Consortium on MEN1. Hum. Mol. Genet. 6:1177–1183.
   PubMed Web of Science ®Google Scholar
• Lin, S. Y., and S. J. Elledge. 2003. Multiple tumor suppressor pathways negatively regulate telomerase. Cell 113:881–889.
   PubMed Web of Science ®Google Scholar
• Lis, J. T., J. A. Simon, and C. A. Sutton. 1983. New heat shock puffs and (beta)-galactosidase activity resulting from transformation of Drosophila with an hsp70-lacZ hybrid gene. Cell 35:403–410.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Marx, S. J. 1998. Multiple endocrine neoplasia type 1, p. 489–506. In B. Vogelstein and K. W. Kinzler (ed.), The genetic basis of human cancer. McGraw Hill, New York, NY.
   Google Scholar
• Migliaccio, E., M. Giorgio, S. Mele, G. Pelicci, P. Reboldi, P. P. Pandolfi, L. Lanfrancone, and P. G. Pelicci. 1999. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402:309–313.
   PubMed Web of Science ®Google Scholar
• Morey, M., F. Serras, and M. Corominas. 2003. Halving the selenophosphate synthetase gene dose confers hypersensitivity to oxidative stress in Drosophila melanogaster. FEBS Lett. 534:111–114.
   PubMedGoogle Scholar
• Morrow, G., S. Battistini, P. Zhang, and R. M. Tanguay. 2004. Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. J. Biol. Chem. 279:43382–43385.
   PubMed Web of Science ®Google Scholar
• Ohkura, N., M. Kishi, T. Tsukada, and K. Yamaguchi. 2001. Menin, a gene product responsible for multiple endocrine neoplasia type 1, interacts with the putative tumor metastasis suppressor nm23. Biochem. Biophys. Res. Commun. 282:1206–1210.
   PubMed Web of Science ®Google Scholar
• Rabindran, S. K., R. I. Haroun, J. Clos, J. Wisniewski, and C. Wu. 1993. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259:230–234.
   PubMed Web of Science ®Google Scholar
• Riabowol, K. T., L. A. Mizzen, and W. J. Welch. 1988. Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science 242:433–436.
   PubMed Web of Science ®Google Scholar
• Sarge, K. D., S. P. Murphy, and R. I. Morimoto. 1993. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol. Cell. Biol. 13:1392–1407.
   PubMed Web of Science ®Google Scholar
• Shi, Y., D. D. Mosser, and R. I. Morimoto. 1998. Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12:654–666.
   PubMed Web of Science ®Google Scholar
• Sorger, P. K., and H. C. Nelson. 1989. Trimerization of a yeast transcriptional activator via a coiled-coil motif. Cell 59:807–813.
   PubMed Web of Science ®Google Scholar
• Sowa, H., H. Kaji, L. Canaff, G. N. Hendy, T. Tsukamoto, T. Yamaguchi, K. Miyazono, T. Sugimoto, and K. Chihara. 2003. Inactivation of menin, the product of the multiple endocrine neoplasia type 1 gene, inhibits the commitment of multipotential mesenchymal stem cells into the osteoblast lineage. J. Biol. Chem. 278:21058–21069.
   PubMedGoogle Scholar
• Sowa, H., H. Kaji, R. Kitazawa, S. Kitazawa, T. Tsukamoto, S. Yano, T. Tsukada, L. Canaff, G. N. Hendy, T. Sugimoto, and K. Chihara. 2004. Menin inactivation leads to loss of transforming growth factor beta inhibition of parathyroid cell proliferation and parathyroid hormone secretion. Cancer Res. 64:2222–2228.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Su, T. T., and B. Jaklevic. 2001. DNA damage leads to a cyclin A-dependent delay in metaphase-anaphase transition in the Drosophila gastrula. Curr. Biol. 11:8–17.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Syken, J., T. De-Medina, and K. Munger. 1999. TID1, a human homolog of the Drosophila tumor suppressor l(2)tid, encodes two mitochondrial modulators of apoptosis with opposing functions. Proc. Natl. Acad. Sci. USA 96:8499–8504.
   PubMed Web of Science ®Google Scholar
• Westwood, J. T., J. Clos, and C. Wu. 1991. Stress-induced oligomerization and chromosomal relocalization of heat shock factor. Nature 353:822–827.
   PubMed Web of Science ®Google Scholar
• Westwood, J. T., and C. Wu. 1993. Activation of Drosophila heat shock factor: conformational change associated with a monomer-to-trimer transition. Mol. Cell. Biol. 13:3481–3486.
   PubMed Web of Science ®Google Scholar
• Xian Ma, Y., S. Fan, J. Xiong, R. Q. Yuan, Q. Meng, M. Gao, I. D. Goldberg, S. A. Fuqua, R. G. Pestell, and E. M. Rosen. 2003. Role of BRCA1 in heat shock response. Oncogene 22:10–27.
   PubMed Web of Science ®Google Scholar
• Yaguchi, H., N. Ohkura, T. Tsukada, and K. Yamaguchi. 2002. Menin, the multiple endocrine neoplasia type 1 gene product, exhibits GTP-hydrolyzing activity in the presence of the tumor metastasis suppressor nm23. J. Biol. Chem. 277:38197–38204.
   PubMedGoogle Scholar
• Yokoyama, A., Z. Wang, J. Wysocka, M. Sanyal, D. J. Aufiero, I. Kitabayashi, W. Herr, and M. L. Cleary. 2004. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24:5639–5649.
   PubMed Web of Science ®Google Scholar
• Zimmerman, J. L., W. Petri, and M. Meselson. 1983. Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell 32:1161–1170.
   PubMed Web of Science ®Google Scholar
• Zuo, J., R. Baler, G. Dahl, and R. Voellmy. 1994. Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure. Mol. Cell. Biol. 14:7557–7568.
   PubMedGoogle Scholar