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http://dx.doi.org/10.5352/JLS.2011.21.2.194

The Caudal-Related Homeodomain Proteins Upregulate catalase Expression in Drosophila Hindgut and Human Colorectal Carcinoma Cells  

Park, Jae-Hong (Department of Molecular Biology, Pusan National University)
Park, So-Young (Department of Molecular Biology, Pusan National University)
Lee, Dong-Ho (Department of Molecular Biology, Pusan National University)
Kim, Young-Shin (Department of Research Institute of Genetic Engineering, Pusan National University)
Yoo, Mi-Ae (Department of Molecular Biology, Pusan National University)
Publication Information
Journal of Life Science / v.21, no.2, 2011 , pp. 194-201 More about this Journal
Abstract
Caudal-related homeodomain proteins play critical roles in intestine development and maintenance from Drosophila to humans. The loss or reduction of CDX1 and CDX2 are known to be associated with colon cancers. It has been well known that colorectal carcinogenesis is associated with serious oxidative stress and that catalase is decreased in colon carcinomas. However, the underlying molecular mechanisms remain elusive. Here, we report that Caudal-related homeodomain proteins positively regulate catalase expression in both Drosophila and humans. We found that Drosophila caudal heterozygotes have a decreased catalase expression and increased ROS generation in the hindgut, and that the overexpression of Caudal increases catalase promoter activity and catalase mRNA levels. We also found that CDX1 and CDX2 up-regulate catalase promoter activity and protein levels in HCT116 cells - human colorectal carcinoma cell lines. The level of catalase protein in several colorectal carcinoma cell lines was associated with CDX1 expression. These results suggest that CDX1 and CDX2 may be involved in intestinal homeostasis and tumorigenesis via regulation of catalase expression.
Keywords
Drosophila caudal; CDX1; CDX2; catalase; colorectal carcinoma;
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1 Wu, L. H. and J. A. Lengyel. 1998. Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125, 2433-2442.
2 Zhu, J. W., B. M. Yu, Y. B. Ji, M H. Zheng, and D. H. Li. 2002. Upregulation of vascular endothelial growth factor by hydrogen peroxide in human colon cancer. World J. Gastroenterol. 8, 153-157.
3 Silberg, D. G., G. P. Swain, E. R. Suh, and P. G. Traber. 2000. Cdx1 and Cdx2 expression during intestinal development. Gastroenterology 119, 961-971.   DOI
4 Skrzydlewska, E., S. Sulkowski, M. Koda, B. Zalewski, L. Kanczuga-Koda, and M. Sulkowska. 2005. Lipid peroxidation and antioxidant status in colorectal cancer. World J. Gastroenterol. 11, 403-406.   DOI
5 Tsutsumishita, Y., T. Onda, K. Okada, M. Takeda, H. Endou, S. Futaki, and M. Niwa. 1998. Involvement of $H_2O_2$ production in cisplatin-induced nephrotoxicity. Biochem. Biophys. Res. Commun. 242, 310-312.   DOI
6 Van Remmen, H., M. D. Williams, H. Yang, C. A. Walter, and A. Richardson. 1998. Analysis of the transcriptional activity of the 5'-flanking region of the rat catalase gene in transiently transfected cells and in transgenic mice. J. Cell Physiol. 174, 18-26.   DOI
7 Wang, W. W., D. L. Smith, and S. D. Zucker. 2004. Bilirubin inhibits iNOS expression and NO production in response to endotoxin in rats. Hepatology 40, 424-433.
8 Wong, N. A., M. P. Britton, G. S. Choi, T. K. Stanton, D. C. Bicknell, J. L. Wilding, and W. F. Bodmer. 2004. Loss of CDX1 expression in colorectal carcinoma: promoter methylation, mutation, and loss of heterozygosity analyses of 37 cell lines. Proc. Natl. Acad. Sci. USA 101, 574-579.   DOI
9 Werling, R. W., H. Yaziji, C. E. Bacchi, and A. M. Gown. 2003. CDX2, a highly sensitive and specific marker of adenocarcinomas of intestinal origin: an immunohistochemical survey of 476 primary and metastatic carcinomas. Am. J. Surg. Pathol. 27, 303-310.   DOI
10 de Winter, B. Y., L. van Nassauw, J. G. de Man, F. de Jonge, A. J. Bredenoord, T. C. Seerden, A. G. Herman, J. P. Timmermans, and P. A. Pelckmans. 2005. Role of oxidative stress in the pathogenesis of septic ileus in mice. Neurogastroenterol. Motil. 17, 251-261.   DOI
11 Mallo, G. V., H. Rechreche, J. M. Frigerio, D. Rocha, A. Zweibaum, M. Lacasa, B. R. Jordan, N. J. Dusetti, J. C. Dagorn, and J. L. Iovanna. 1997. Molecular cloning, sequencing and expression of the mRNA encoding human Cdx1 and Cdx2 homeobox. Down-regulation of Cdx1 and Cdx2 mRNA expression during colorectal carcinogenesis. Int. J. Cancer 74, 35-44.   DOI
12 McGinnis, W. and R. Krumlauf. 1992. Homeobox genes and axial patterning. Cell 68, 283-302.   DOI
13 Michiels, C., M. Raes, O. Toussaint, and J. Remacle. 1994. Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic. Biol. Med. 17, 235-248.   DOI
14 Nenoi, M., S. Ichimura, K. Mita, O. Yukawa, and I. L. Cartwright. 2001. Regulation of the catalase gene promoter by Sp1, CCAAT-recognizing factors, and a WT1/Egr-related factor in hydrogen peroxide-resistant HP100 cells. Cancer Res. 61, 5885-5894.
15 Sanders, L. M., C. E. Henderson, M. Y. Hong, R. Barhoumi, R. C. Burghardt, N. Wang, C. M. Spinka, R. J. Carroll, N. D. Turner, R. S. Chapkin, and J. R. Lupton. 2004. An increase in reactive oxygen species by dietary fish oil coupled with the attenuation of antioxidant defenses by dietary pectin enhances rat colonocyte apoptosis. J. Nutr. 134, 3233-3238.
16 Park, S. Y., Y.S. Kim, D. J. Yang, and M. A. Yoo. 2004. Transcriptional regulation of the Drosophila catalase gene by the DRE/DREF system. Nucleic Acids Res. 32, 1318-1324.   DOI
17 Ren, P., D. G. Silberg, and A. E. Sirica. 2000. Expression of an intestine-specific transcription factor (CDX1) in intestinal metaplasia and in subsequently developed intestinal type of cholangiocarcinoma in rat liver. Am. J. Pathol. 156, 621-627.   DOI
18 Rhee, S. G. 1999. Redox signaling: hydrogen peroxide as intracellular messenger. Exper. Mol. Med. 35, 53-59.
19 Joseph, P., T. K. Muchnok, M. L. Klishis, J. R. Roberts, J. M. Antonini, W. Z. Whong, and T. Ong. 2001. Cadmium-induced cell transformation and tumorigenesis are associated with transcriptional activation of c-fos, c-jun, and c-myc proto-oncogenes: role of cellular calcium and reactive oxygen species. Toxicol. Sci. 61, 295-303.   DOI   ScienceOn
20 Kessel, M. and P. Gruss. 1990. Murine developmental control genes. Science 249, 374-379.   DOI
21 Kim, H. S., T. B. Lee, and C. H. Choi. 2001. Down-regulation of catalase gene expression in the doxorubicin-resistant AML subline AML-2/DX100. Biochem. Biophys. Res. Commun. 281, 109-114.   DOI
22 Kuhnlein, R. P., G. Bronner, H. Taubert, and R. Schuh. 1997. Regulation of Drosophila spalt gene expression. Mech. Dev. 66, 107-118.   DOI
23 Luo, D. and T. A. Rando. 2003. The regulation of catalase gene expression in mouse muscle cells is dependent on the CCAAT-binding factor NF-Y. Biochem. Biophys. Res. Commun. 303, 609-618.   DOI
24 Lauer, C., A. Volkl, S. Riedl, H. D. Fahimi, and K. Beier. 1999. Impairment of peroxisomal biogenesis in human colon carcinoma. Carcinogenesis 20, 985-989.   DOI
25 Lewis, A. D., I. D. Hickson, C. N. Robson, A. L. Harris, J. D. Hayes, S. A. Griffiths, M. M. Manson, A. E. Hall, J. E. Moss, and C. R. Wolf. 1988. Amplification and increased expression of alpha class glutathione S-transferase-encoding genes associated with resistance to nitrogen mustards. Proc. Natl. Acad. Sci. USA 85, 8511- 8515.   DOI
26 Lewis, M. T. 2000. Homeobox genes in mammary gland development and neoplasia. Breast Cancer Res. 2, 158-169.   DOI
27 Crissey, M. A., R. J. Guo, S. Funakoshi, J. Kong, J. Liu, and J. P. Lynch. 2010. Cdx2 levels modulate intestinal epithelium maturity and Paneth cell development. Gastroenterology 140, 517-528.
28 Cuzzocrea, S., D. P. Riley, A. P. Caputi, and D. Salvemini. 2001. Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol. Rev. 53, 135-159.
29 Domon-Dell, C., A. Schneider, V. Moucadel, E. Guerin, D. Guenot, S. Aguillon, I. Duluc, E. Martin, J. Iovanna, J. F. Launay, B. Duclos, M. P. Chenard, C. Meyer, P. Oudet, M. Kedinger, M. P. Gaub, and J. N. Freund. 2003. Cdx1 homeobox gene during human colon cancer progression. Oncogene 22, 7913-7921.   DOI
30 Fischer, J. A., E. Giniger, T. Maniatis, and M. Ptashne. 1988. GAL4 activates transcription in Drosophila. Nature 332, 853-856.   DOI
31 Gupta, A., S. F. Rosenberger, and G. T. Bowden. 1999. Increased ROS levels contribute to elevated transcription factor and MAP kinase activities in malignantly progressed mouse keratinocyte cell lines. Carcinogenesis 20, 2063-2073.   DOI
32 Jackson, A. L. and L. A. Loeb. 2001. The contribution of endogenous sources of DNA damage to the multiple mutations in cancer. Mutat. Res. 477, 7-21.   DOI
33 Han, K. 1996. An efficient DDAB-mediated transfection of Drosophila S2 cells. Nucleic Acids Res. 24, 4362-4363.   DOI
34 Hunt, C. R., J. E. Sim, S. J. Sullivan, T. Featherstone, W. Golden, C. Von Kapp-Herr, R. A. Hock, R. A. Gomez, A. J. Parsian, and D. R. Spitz. 1998. Genomic instability and catalase gene amplification induced by chronic exposure to oxidative stress. Cancer Res. 58, 3986-3992.
35 Hwang, M. S., Y. S. Kim, N. H. Choi, J. H. Park, E. J. Oh, E. J Kwon, M. Yamaguchi, and M. A. Yoo. 2002. The caudal homeodomain protein activates Drosophila E2F gene expression. Nucleic Acids Res. 30, 5029-5035.   DOI
36 Albuszies, G. and U. B. Bruckner. 2003. Antioxidant therapy in sepsis. Intensive Care Med. 29, 1632-1636.   DOI
37 Almeida, R., E. Silva, F. Santos-Silva, D. G. Silberg, J. Wang, C. De Bolos, and L. David. 2003. Expression of intestine- specific transcription factors, CDX1 and CDX2, in intestinal metaplasia and gastric carcinomas. J. Pathol. 199, 36-40.   DOI
38 Butler, H., S. Levine, X. Wang, S. Bonyadi, G. Fu, P. Lasko, B. Suter, and R. Doerig. 2001. Map position and expression of the genes in the 38 region of Drosophila. Genetics 158, 1597-1614.
39 Baba Y., K. Nosho, K. Shima, E. Freed, N. Irahara, J. Philips, J. A. Meyerhardt, J. L. Hornick, R. A. Shivdasani, C. S. Fuchs, and S. Ogino. 2009. Relationship of CDX2 loss with molecular features and prognosis in colorectal cancer. Clin. Cancer Res. 15, 4665-4673.   DOI
40 Bartsch, H., J. Nair, and R. W. Owen. 2002. Exocyclic DNA adducts as oxidative stress markers in colon carcinogenesis: potential role of lipid peroxidation, dietary fat and antioxidants. Biol. Chem. 383, 915-921.   DOI
41 Chawengsaksophak, K., R. James, V. E. Hammond, F. Kontgen, and F. Beck. 1997. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386, 84-87.   DOI
42 Choi, Y. J., T. Y. Choi, M. Yamaguchi, A. Matsukage, Y. S. Kim, and M. A. Yoo. 2004. Transcriptional regulation of the Drosophila caudal homeobox gene by DRE/DREF. Nucleic Acids Res. 32, 3734-3742.   DOI