A crucial role for Nox 1 in redox-dependent regulation of Wnt-β-catenin signaling

FASEB Journal

Volumn 26, Issue 5, 2012, Pages 2049-2059

  Kajla, Seheli ^a   Mondol, Abdus S ^a   Nagasawa, Atsushi ^a   Zhang, Yugen ^a   Kato, Masayoshi ^a   Matsuno, Kuniharu ^b   Yabe Nishimura, Chihiro ^b   Kamata, Tohru ^a  

^a SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

NADPH oxidase; Nucleoredoxin; Rac1; Reactive oxygen species

Indexed keywords

APC PROTEIN; BETA CATENIN; CELL PROTEIN; CYCLIN D1; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR VAV2; GUANOSINE TRIPHOSPHATASE; MYC PROTEIN; NUCLEOREDOXIN; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; SMALL INTERFERING RNA; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL FATE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISSOCIATION; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; MICE; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; POLYMERASE CHAIN REACTION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84860893918     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-196360     Document Type: Article

References (36)

1. Lambeth, J. D. (2007) Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic. Biol. Med. 43, 332-347
2. Lambeth, J. D., Kawahara, T., and Diebold, B. (2007) Regulation of Nox and Duox enzymatic activity and expression. Free Radic. Biol. Med. 43, 319-331 (Pubitemid 46978416)
3. Kawahara, T., Kuwano, Y., Teshima-Kondo, S., Takeya, R., Sumimoto, H., Kishi, K., Tsunawaki, S., Hirayama, T., and Rokutan, K. (2004) Role of nicotinamide adenine dinucleotide phosphate oxidase 1 in oxidative burst response to Toll-like receptor 5 signaling in large intestinal epithelial cells. J. Immunol. 172, 3051-3058 (Pubitemid 38263694)
4. Geiszt, M., Lekstrom, K., Brenner, S., Hewitt, S. M., Dana, R., Malech, H. L., and Leto, T. L. (2003) NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J. Immunol. 171, 299-306 (Pubitemid 36745301)
5. Mitsushita, J., Lambeth, J. D., and Kamata, T. (2004) The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Res. 64, 3580 -3585
6. Kamata, T. (2009) Roles of Nox1 and other Nox isoforms in cancer development. Cancer Sci. 100, 1382-1388
7. Laurent, E., McCoy, J. W., 3rd, Macina, R. A., Liu, W., Cheng, G., Robine, S., Papkoff, J., and Lambeth, J. D. (2008) Nox1 is over-expressed in human colon cancers and correlates with activating mutations in K-Ras. Int. J. Cancer 123, 100 -107
8. Szanto, I., Rubbia-Brandt, L., Kiss, P., Steger, K., Banfi, B., Kovari, E., Herrmann, F., Hadengue, A., and Krause, K. H. (2005) Expression of NOX1, a superoxide-generating NADPH oxidase, in colon cancer and inflammatory bowel disease. J. Pathol. 207, 164-176 (Pubitemid 41404147)
9. Huelsken, J., and Birchmeier, W. (2001) New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11, 547-553 (Pubitemid 32800729)
10. Reya, T., and Clevers, H. (2005) Wnt signalling in stem cells and cancer. Nature 434, 843-850 (Pubitemid 40558990)
11. Polakis, P. (2007) The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17, 45-51
12. Batlle, E., Henderson, J. T., Beghtel, H., van den Born, M. M., Sancho, E., Huls, G., Meeldijk, J., Robertson, J., van de Wetering, M., Pawson, T., and Clevers, H. (2002) Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111, 251-263 (Pubitemid 35292445)
13. Funato, Y., Michiue, T., Asashima, M., and Miki, H. (2006) The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat. Cell Biol. 8, 501-508
14. Shinohara, M., Adachi, Y., Mitsushita, J., Kuwabara, M., Nagasawa, A., Harada, S., Furuta, S., Zhang, Y., Seheli, K., Miyazaki, H., and Kamata, T. (2010) Reactive oxygen generated by NADPH oxidase 1 (Nox1) contributes to cell invasion by regulating matrix metalloprotease-9 production and cell migration. J. Biol. Chem. 285, 4481-4488
15. Wu, Y., Kwon, K. S., and Rhee, S. G. (1998) Probing cellular protein targets of H2O2 with fluorescein-conjugated iodoacetamide and antibodies to fluorescein. FEBS Lett. 440, 111-115 (Pubitemid 28558747)
16. Shinohara, M., Shang, W. H., Kubodera, M., Harada, S., Mitsushita, J., Kato, M., Miyazaki, H., Sumimoto, H., and Kamata, T. (2007) Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesions by down-regulating Rho. J. Biol. Chem. 282, 17640-17648 (Pubitemid 47100324)
17. Matsuno, K., Yamada, H., Iwata, K., Jin, D., Katsuyama, M., Matsuki, M., Takai, S., Yamanishi, K., Miyazaki, M., Matsubara, H., and Yabe-Nishimura, C. (2005) Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation 112, 2677-2685 (Pubitemid 41532605)
18. Komatsu, D., Kato, M., Nakayama, J., Miyagawa, S., and Kamata, T. (2008) NADPH oxidase 1 plays a critical mediating role in oncogenic Ras-induced vascular endothelial growth factor expression. Oncogene 27, 4724-4732
19. Yost, C., Torres, M., Miller, J. R., Huang, E., Kimelman, D., and Moon, R. T. (1996) The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10, 1443-1454 (Pubitemid 26260702)
20. Malliri, A., Rygiel, T. P., van der Kammen, R. A., Song, J. Y., Engers, R., Hurlstone, A. F., Clevers, H., and Collard, J. G. (2006) The rac activator Tiam1 is a Wnt-responsive gene that modifies intestinal tumor development. J. Biol. Chem. 281, 543-548 (Pubitemid 43671217)
21. Liu, J. Y., Seno, H., Miletic, A. V., Mills, J. C., Swat, W., and Stappenbeck, T. S. (2009) Vav proteins are necessary for correct differentiation of mouse cecal and colonic enterocytes. J. Cell Sci. 122, 324-334
22. Gianni, D., Bohl, B., Courtneidge, S. A., and Bokoch, G. M. (2008) The involvement of the tyrosine kinase c-Src in the regulation of reactive oxygen species generation mediated by NADPH oxidase-1. Mol. Biol. Cell 19, 2984-2994
23. Schuebel, K. E., Movilla, N., Rosa, J. L., and Bustelo, X. R. (1998) Phosphorylation-dependent and constitutive activation of Rho proteins by wild-type and oncogenic Vav-2. EMBO J. 17, 6608-6621 (Pubitemid 28521795)
24. Servitja, J. M., Marinissen, M. J., Sodhi, A., Bustelo, X. R., and Gutkind, J. S. (2003) Rac1 function is required for Src-induced transformation. Evidence of a role for Tiam1 and Vav2 in Rac activation by Src. J. Biol. Chem. 278, 34339-34346 (Pubitemid 37553278)
25. Yokoyama, N., and Malbon, C. C. (2009) Dishevelled-2 docks and activates Src in a Wnt-dependent manner. J. Cell Sci. 122, 4439-4451
26. Major, M. B., Camp, N. D., Berndt, J. D., Yi, X., Goldenberg, S. J., Hubbert, C., Biechele, T. L., Gingras, A. C., Zheng, N., Maccoss, M. J., Angers, S., and Moon, R. T. (2007) Wilms tumor suppressor WTX negatively regulates WNT/beta-catenin signaling. Science 316, 1043-1046 (Pubitemid 46799493)
27. Shirasawa, S., Furuse, M., Yokoyama, N., and Sasazuki, T. (1993) Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 260, 85-88 (Pubitemid 23122749)
28. Rimerman, R. A., Gellert-Randleman, A., and Diehl, J. A. (2000) Wnt1 and MEK1 cooperate to promote cyclin D1 accumulation and cellular transformation. J. Biol. Chem. 275, 14736 -14742
29. Bolen, J. B., Veillette, A., Schwartz, A. M., Deseau, V., and Rosen, N. (1987) Analysis of pp60c-src in human colon carcinoma and normal human colon mucosal cells. Oncogene Res. 1, 149 -168
30. Buongiorno, P., Pethe, V. V., Charames, G. S., Esufali, S., and Bapat, B. (2008) Rac1 GTPase and the Rac1 exchange factor Tiam1 associate with Wnt-responsive promoters to enhance beta-catenin/TCF-dependent transcription in colorectal cancer cells. Mol. Cancer 7, 73
31. Rhee, S. G., Chang, T. S., Bae, Y. S., Lee, S. R., and Kang, S. W. (2003) Cellular regulation by hydrogen peroxide. J. Am. Soc. Nephrol. 14, S211-S215 (Pubitemid 36903927)
32. Bae, Y. S., Kang, S. W., Seo, M. S., Baines, I. C., Tekle, E., Chock, P. B., and Rhee, S. G. (1997) Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272, 217-221 (Pubitemid 27021147)
33. Meng, T. C., Fukada, T., and Tonks, N. K. (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387-399 (Pubitemid 34195563)
34. Lassegue, B., Sorescu, D., Szocs, K., Yin, Q., Akers, M., Zhang, Y., Grant, S. L., Lambeth, J. D., and Griendling, K. K. (2001) Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ. Res. 88, 888-894 (Pubitemid 32441466)
35. Coant, N., Ben Mkaddem, S., Pedruzzi, E., Guichard, C., Treton, X., Ducroc, R., Freund, J. N., Cazals-Hatem, D., Bouhnik, Y., Woerther, P. L., Skurnik, D., Grodet, A., Fay, M., Biard, D., Lesuffleur, T., Deffert, C., Moreau, R., Groyer, A., Krause, K. H., Daniel, F., and Ogier-Denis, E. (2010) NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol. Cell. Biol. 30, 2636-2650
36. Fukumoto, S., Hsieh, C. M., Maemura, K., Layne, M. D., Yet, S. F., Lee, K. H., Matsui, T., Rosenzweig, A., Taylor, W. G., Rubin, J. S., Perrella, M. A., and Lee, M. E. (2001) Akt participation in the Wnt signaling pathway through Dishevelled. J. Biol. Chem. 276, 17479-17483