Immunohistochemical study of the Nrf2 pathway in colorectal cancer: Nrf2 expression is closely correlated to keap1 in the tumor and bach1 in the normal tissue

Applied Immunohistochemistry and Molecular Morphology

Volumn 21, Issue 6, 2013, Pages 511-517

  Chang, Liang Che ^a   Fan, Chung Wei ^a   Tseng, Wen Ko ^a   Chen, Jim Ray ^a   Chein, Hui Ping ^a   Hwang, Cheng Cheng ^a   Hua, Chung Ching ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

Colorectal cancer; Immunohistochemical staining; Nrf2 pathway; Oxidative stress

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; BTB AND CNC HOMOLOGY 1; CD34 ANTIGEN; DJ 1 PROTEIN; FORMALDEHYDE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; PARAFFIN; PROHIBITIN; PROTEIN; PROTEIN P21; PROTEIN P62; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

AGED; ARTICLE; CANCER PATIENT; CAPILLARY DENSITY; COLORECTAL CANCER; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; OXIDATIVE STRESS; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOKING;

ADENOCARCINOMA; AGED; AGED, 80 AND OVER; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; COLORECTAL NEOPLASMS; DEOXYGUANOSINE; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MIDDLE AGED; NEOPLASM STAGING; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RISK FACTORS; SIGNAL TRANSDUCTION; SMOKING;

EID: 84892434876     PISSN: 15412016     EISSN: 15334058     Source Type: Journal    
DOI: 10.1097/PAI.0b013e318282ac20     Document Type: Article

References (39)

1. Rangasamy T, Cho CY, Thimmulappa RK, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest. 2004;114:1248-1259.
2. Itoh K, Wakabayashi N, Katoh Y, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999;13:76-86.
3. Gunderson LL, Jessup JM, Sargent DJ, et al. Revised TN categorization for colon cancer based on national survival outcomes data. J Clin Oncol. 2010;28:264-271.
4. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med. 2004;10: 549-557.
5. Sykiotis GP, Bohmann D. Stress- A ctivated cap "n" collar transcription factors in aging and human disease. Sci Signal. 2010;3:re3.
6. Chen W, Sun Z, Wang XJ, et al. Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol Cell. 2009;34:663-673.
7. Jain A, Lamark T, Sjøttem E, et al. p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem. 2010;285:22576-22591.
8. Du Y, Wooten MC, Gearing M, et al. Age- A ssociated oxidative damage to the p62 promoter: implications for Alzheimer disease. Free Radic Biol Med. 2009;46:492-501.
9. Clements CM, McNally RS, Conti BJ, et al. DJ-1, a cancer- And Parkinson's disease- A ssociated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc Natl Acad Sci USA. 2006;103:15091-15096.
10. Theiss AL, Vijay-Kumar M, Obertone TS, et al. Prohibitin is a novel regulator of antioxidant response that attenuates colonic inflammation in mice. Gastroenterology. 2009;137:199-208. 208 e191-196.
11. Dhakshinamoorthy S, Jain AK, Bloom DA, et al. Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants. J Biol Chem. 2005;280:16891-16900.
12. Kaspar JW, Jaiswal AK. Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. J Biol Chem. 2010;285:153-162.
13. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: The role of inflammation. Am J Physiol Gastrointest Liver Physiol. 2004;287:G7-G17.
14. Khor TO, Huang MT, Prawan A, et al. Increased susceptibility of Nrf2 knockout mice to colitis- A ssociated colorectal cancer. Cancer Prev Res (Phila, PA). 2008;1:187-191.
15. Bosman FT, Carneiro F, Hruban R, et al. WHO classification of tumours of the digestive system. 4th ed. Lyon, France: IARC; 2010:131-182.
16. Rasband WS., ImageJ. Bethesda, MD: US National Institutes of Health; 1997-2011.
17. Landini G. Colour Deconvolution. ImageJ Plugins, rsb.info.nih. gov/ij/.
18. Arganda-Carreras I, Fernández-Gonzá lez R, Muñ oz-Barrutia A, et al. 3D reconstruction of histological sections: Application to mammary gland tissue. Microsc Res Tech. 2010;73:1019-1029.
19. Wild R, Ramakrishnan S, Sedgewick J, et al. Quantitative assessment of angiogenesis and tumor vessel architecture by computerassisted digital image analysis: effects of VEGF-toxin conjugate on tumor microvessel density. Microvasc Res. 2000;59:368-376.
20. Venables VN, Ripley BD. Modern Applied Statistics With S. 4th ed. New York: Springer; 2002:175-176.
21. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst Biol. 2002;51:492-508.
22. Suzuki R, Shimodaira H. Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006;22: 1540-1542.
23. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860-867.
24. Federico A, Morgillo F, Tuccillo C, et al. Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer. 2007;121: 2381-2386.
25. Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy- 2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat Res. 1997;387:147-163.
26. Kondo S, Toyokuni S, Tanaka T, et al. Overexpression of the hOGG1 gene and high 8-hydroxy-20-deoxyguanosine (8-OHdG) lyase activity in human colorectal carcinoma: regulation mechanism of the 8-OHdG level in DNA. Clin Cancer Res. 2000;6: 1394-1400.
27. Fan W, Tang Z, Chen D, et al. Keap1 facilitates p62-mediated ubiquitin aggregate clearance via autophagy. Autophagy. 2010;6: 614-621.
28. Lau A, Wang XJ, Zhao F, et al. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol Cell Biol. 2010;30:3275-3285.
29. Lee O-H, Jain AK, Papusha V, et al. An auto-regulatory loop between stress sensors INrf2 and Nrf2 controls their cellular abundance. J Biol Chem. 2007;282:36412-36420.
30. Jyrkkanen HK, Kuosmanen SM, Heinaniemi M, et al. Novel insights into the regulation of the antioxidant response element mediated gene expression by electrophiles: induction of the transcriptional repressor BACH1 by NRF2. Biochem J. 2011;103: 15091-15096.
31. Kwak M-K, Itoh K, Yamamoto M, et al. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol Cell Biol. 2002;22:2883-2892.
32. Villeneuve NF, Sun Z, Chen W, et al. Nrf2 and p21 regulate the fine balance between life and death by controlling ROS levels. Cell Cycle. 2009;8:3255-3256.
33. Dohi Y, Ikura T, Hoshikawa Y, et al. Bach1 inhibits oxidative stress-induced cellular senescence by impeding p53 function on chromatin. Nat Struct Mol Biol. 2008;15:1246-1254.
34. Gan L, Johnson DA, Johnson JA. Keap1-Nrf2 activation in the presence and absence of DJ-1. Eur J Neurosci. 2010;31:967-977.
35. Reuter S, Gupta SC, Chaturvedi MM, et al. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med. 2010;49:1603-1616.
36. Saleh HA, Jackson H, Banerjee M. Immunohistochemical expression of bcl-2 and p53 oncoproteins: correlation with Ki67 proliferation index and prognostic histopathologic parameters in colorectal neoplasia. Appl Immunohistochem. 2000;8:175-182.
37. Goven D, Boutten A, Lecon-Malas V, et al. Altered Nrf2/Keap1- Bach1 equilibrium in pulmonary emphysema. Thorax. 2008;63: 916-924.
38. Skrzydlewska E, Sulkowski S, Koda M, et al. Lipid peroxidation and antioxidant status in colorectal cancer. World J Gastroenterol. 2005;11:403-406.
39. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer. 2009;9:400-414.