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http://dx.doi.org/10.5483/BMBRep.2014.47.9.196

Role of NADH: quinone oxidoreductase-1 in the tight junctions of colonic epithelial cells  

Nam, Seung Taek (Department of Life Science, College of Natural Science, Daejin University)
Hwang, Jung Hwan (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Kim, Dae Hong (Department of Life Science, College of Natural Science, Daejin University)
Park, Mi Jung (Department of Life Science, College of Natural Science, Daejin University)
Lee, Ik Hwan (Department of Life Science, College of Natural Science, Daejin University)
Nam, Hyo Jung (Department of Life Science, College of Natural Science, Daejin University)
Kang, Jin Ku (Department of Life Science, College of Natural Science, Daejin University)
Kim, Sung Kuk (Department of Life Science, College of Natural Science, Daejin University)
Hwang, Jae Sam (Department of Agricultural Biology, National Academy of Agricultural Science, RDA)
Chung, Hyo Kyun (Department of Internal Medicine, Chungnam National University)
Shong, Minho (Department of Internal Medicine, Chungnam National University)
Lee, Chul-Ho (Laboratory Animal Resource Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Kim, Ho (Department of Life Science, College of Natural Science, Daejin University)
Publication Information
BMB Reports / v.47, no.9, 2014 , pp. 494-499 More about this Journal
Abstract
NADH:quinone oxidoreductase 1 (NQO1) is known to be involved in the regulation of energy synthesis and metabolism, and the functional studies of NQO1 have largely focused on metabolic disorders. Here, we show for the first time that compared to NQO1-WT mice, NQO1-KO mice exhibited a marked increase of permeability and spontaneous inflammation in the gut. In the DSS-induced colitis model, NQO1-KO mice showed more severe inflammatory responses than NQO1-WT mice. Interestingly, the transcript levels of claudin and occludin, the major tight junction molecules of gut epithelial cells, were significantly decreased in NQO1-KO mice. The colons of NQO1-KO mice also showed high levels of reactive oxygen species (ROS) and histone deacetylase (HDAC) activity, which are known to affect transcriptional regulation. Taken together, these novel findings indicate that NQO1 contributes to the barrier function of gut epithelial cells by regulating the transcription of tight junction molecules.
Keywords
Barrier dysfunction of epithelial cells; Chromosome condensation; Claudin-1; Gut epithelial cell tight junction; Gut inflammation; Histone acetylation/deacetylation; NQO1 knockout mice; Occludin; Transcription;
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1 Ito, K., Hanazawa, T., Tomita, K., Barnes, P. J., and Adcock, I. M. (2004) Oxidative stress reduces histone deacetylase 2 activity and enhances IL-8 gene expression: role of tyrosine nitration. Biochem. Biophys. Res. Commun. 315, 240-245.   DOI   ScienceOn
2 Rahman, I., Gilmour, P. S., Jimenez, L. A., and MacNee, W. (2002) Oxidative stress and TNF-alpha induce histone acetylation and NF-kappaB/AP-1 activation in alveolar epithelial cells: potential mechanism in gene transcription in lung inflammation. Mol. Cell. Biochem. 234, 239-248.
3 Miura, K., Taura, K., Kodama, Y., Schnabl, B., and Brenner, D. A. (2008) Hepatitis C virus-induced oxidative stress suppresses hepcidin expression through increased histone deacetylase activity. Hepatology 48, 1420-1429.   DOI   ScienceOn
4 Baumgart, D. C., Olivier, W. A., Reya, T., Peritt, D., Rombeau, J. L., and Carding, S. R. (1998) Mechanisms of intestinal epithelial cell injury and colitis in interleukin 2 (IL2)-deficient mice. Cell Immunol. 187, 52-66.   DOI   ScienceOn
5 Nam, H. J., Kang, J. K., Kim, S. K., Ahn, K. J., Seok, H., Park, S. J., Chang, J. S., Pothoulakis, C., Lamont, J. T., and Kim, H. (2012) Clostridium difficile toxin A decreases acetylation of tubulin, leading to microtubule depolymerization through activation of histone deacetylase 6, and this mediates acute inflammation. J. Biol. Chem. 285, 32888-32896.
6 Sade, H., Holloway, K., Romero, I. A., and Male, D. (2009) Transcriptional control of occludin expression in vascular endothelia: regulation by Sp3 and YY1. Biochim Biophys. Acta 1789, 175-184.   DOI   ScienceOn
7 Dufresne, J., and Cyr, D. G. (2007) Activation of an SP binding site is crucial for the expression of claudin 1 in rat epididymal principal cells. Biol. Reprod. 76, 825-832.   DOI   ScienceOn
8 Marks, P. A., Richon, V. M., Breslow, R., and Rifkind, R. A. (2001) Histone deacetylase inhibitors as new cancer drugs. Curr. Opin. Oncol. 13, 477-483.   DOI   ScienceOn
9 Richon, V. M., Sandhoff, T. W., Rifkind, R. A., and Marks, P. A. (2000) Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc. Natl. Acad. Sci. U. S. A. 97, 10014-10019.   DOI   ScienceOn
10 Richon, V. M., Zhou, X., Rifkind, R. A., and Marks, P. A. (2001) Histone deacetylase inhibitors: development of suberoylanilide hydroxamic acid (SAHA) for the treatment of cancers. Blood Cells Mol. Dis. 27, 260-264.   DOI   ScienceOn
11 Marks, P. A., Richon, V. M., and Rifkind, R. A. (2000) Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J. Natl. Cancer Inst. 92, 1210-1216.   DOI   ScienceOn
12 Begleiter, A., Hewitt, D., Maksymiuk, A. W., Ross, D. A., and Bird, R. P. (2006) A NAD(P)H:quinone oxidoreductase 1 polymorphism is a risk factor for human colon cancer. Cancer Epidemiol. Biomarkers. Prev. 15, 2422-2426.   DOI   ScienceOn
13 Kang, K. A., Zhang, R., Kim, G. Y., Bae, S. C., and Hyun, J. W. (2012) Epigenetic changes induced by oxidative stress in colorectal cancer cells: methylation of tumor suppressor RUNX3. Tumour Biol. 33, 403-412.   DOI
14 Tokuda, S., Miyazaki, H., Nakajima, K., Yamada, T., and Marunaka, Y. (2010) NaCl flux between apical and basolateral side recruits claudin-1 to tight junction strands and regulates paracellular transport. Biochem. Biophys. Res. Commun. 393, 390-396.   DOI   ScienceOn
15 Alscher, K. T., Phang, P. T., McDonald, T. E., and Walley, K. R. (2001) Enteral feeding decreases gut apoptosis, permeability, and lung inflammation during murine endotoxemia. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G569-576.   DOI
16 Denizot, J., Sivignon, A., Barreau, F., Darcha, C., Chan, H. F., Stanners, C. P., Hofman, P., Darfeuille-Michaud, A., and Barnich, N. (2012) Adherent-invasive Escherichia coli induce claudin-2 expression and barrier defect in CEABAC10 mice and Crohn's disease patients. Inflamm. Bowel. Dis. 18, 294-304.   DOI   ScienceOn
17 Su, L., Shen, L., Clayburgh, D. R., Nalle, S. C., Sullivan, E. A., Meddings, J. B., Abraham, C., and Turner, J. R. (2009) Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 136, 551-563.   DOI   ScienceOn
18 Schnoor, M., Betanzos, A., Weber, D. A., and Parkos, C. A. (2009) Guanylate-binding protein-1 is expressed at tight junctions of intestinal epithelial cells in response to interferon- gamma and regulates barrier function through effects on apoptosis. Immunol. 2, 33-42.
19 Pothoulakis, C., Castagliuolo, I., LaMont, J. T., Jaffer, A., O'Keane, J. C., Snider, R. M., and Leeman, S. E. (1994) CP-96,345, a substance P antagonist, inhibits rat intestinal responses to Clostridium difficile toxin A but not cholera toxin. Proc. Natl. Acad. Sci. U. S. A. 91, 947-951.   DOI   ScienceOn
20 Rhee, S. H., Im, E., Riegler, M., Kokkotou, E., O'Brien, M., and Pothoulakis, C. (2005) Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc. Natl. Acad. Sci. U. S. A. 102, 13610-13615.   DOI   ScienceOn
21 Winski, S. L., Koutalos, Y., Bentley, D. L., and Ross, D. (2002) Subcellular localization of NAD(P)H:quinone oxidoreductase 1 in human cancer cells. Cancer Res. 62, 1420-1424.
22 Berger, F., Ramirez-Hernandez, M. H., and Ziegler, M. (2004) The new life of a centenarian: signalling functions of NAD(P). Trends Biochem. Sci. 29, 111-118.   DOI   ScienceOn
23 Pollak, N., Dolle, C., and Ziegler, M. (2007) The power to reduce: pyridine nucleotides--small molecules with a multitude of functions. Biochem. J. 402, 205-218.   DOI   ScienceOn
24 Jaiswal, A. K. (2000) Regulation of genes encoding NAD(P)H: quinone oxidoreductases. Free Radic. Biol. Med. 29, 254-262.   DOI   ScienceOn
25 Hwang, J. H., Kim, D. W., Jo, E. J., Kim, Y. K., Jo, Y. S., Park, J. H., Yoo, S. K., Park, M. K., Kwak, T. H., Kho, Y. L., Han, J., Choi, H. S., Lee, S. H., Kim, J. M., Lee, I., Kyung, T., Jang, C., Chung, J., Kweon, G. R. and Shong, M. (2009) Pharmacological stimulation of NADH oxidation ameliorates obesity and related phenotypes in mice. Diabetes 58, 965-974.   DOI   ScienceOn
26 Oh, G. S., Kim, H. J., Choi, J. H., Shen, A., Choe, S. K., Karna, A., Lee, S. H., Jo, H. J., Yang, S. H., Kwak, T. H., Lee, C. H., Park, R. and So, H. S. (2014) Pharmacological activation of NQO1 increases NAD levels and attenuates cisplatin-mediated acute kidney injury in mice. Kidney Int. 85, 547-560.   DOI   ScienceOn
27 Nagumo, Y., Han, J., Bellila, A., Isoda, H., and Tanaka, T. (2008) Cofilin mediates tight-junction opening by redistributing actin and tight-junction proteins. Biochem. Biophys. Res. Commun. 377, 921-925.   DOI   ScienceOn
28 Palming, J., Sjoholm, K., Jernas, M., Lystig, T. C., Gummesson, A., Romeo, S., Lonn, L., Lonn, M., Carlsson, B., and Carlsson, L. M. (2007) The expression of NAD(P)H:quinone oxidoreductase 1 is high in human adipose tissue, reduced by weight loss, and correlates with adiposity, insulin sensitivity, and markers of liver dysfunction. J. Clin. Endocrinol. Metab. 92, 2346-2352.   DOI   ScienceOn