Chronic epithelial NF-κB activation accelerates APC loss and intestinal tumor initiation through iNOS up-regulation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 35, 2012, Pages 14007-14012

  Shaked, Helena ^a   Hofseth, Lorne J ^b   Chumanevich, Alena ^b   Chumanevich, Alexander A ^b   Wang, Jin ^c   Wang, Yinsheng ^c   Taniguchi, Koji ^a,d   Guma, Monica ^a   Shenouda, Steve ^a   Clevers, Hans ^e   Harris, Curtis C ^f   Karin, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e HUBRECHT INSTITUTE   (Netherlands)

^f NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGUANIDINE; APC PROTEIN; BETA CATENIN; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER SURVIVAL; CARCINOGENESIS; COLON TUMOR; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENE EXPRESSION; GENE LOCUS; HETEROZYGOSITY LOSS; INTESTINE EPITHELIUM CELL; INTESTINE INJURY; INTESTINE TUMOR; LATENT PERIOD; MALE; MOUSE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE TUMOR; TRANSGENIC MOUSE; TUMOR VOLUME; UPREGULATION;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; BETA CATENIN; COLITIS; COLORECTAL NEOPLASMS; DNA DAMAGE; EPITHELIAL CELLS; FEMALE; I-KAPPA B KINASE; INTESTINAL MUCOSA; LOSS OF HETEROZYGOSITY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; REACTIVE NITROGEN SPECIES; STEM CELLS;

MUS; MUS MUSCULUS;

EID: 84865534083     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211509109     Document Type: Article

References (55)

1. Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics, 2010. CA Cancer J Clin 60:277-300.
2. Hardy RG, Meltzer SJ, Jankowski JA (2000) ABC of colorectal cancer. Molecular basis for risk factors. BMJ 321:886-889.
3. Grivennikov SI, Greten FR, Karin M (2010) Immunity, inflammation, and cancer. Cell 140:883-899.
4. Greten FR, et al. (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118:285-296. (Pubitemid 39061110)
5. Pikarsky E, et al. (2004) NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431:461-466. (Pubitemid 39329586)
6. Garrett WS, et al. (2009) Colitis-associated colorectal cancer driven by T-bet deficiency in dendritic cells. Cancer Cell 16:208-219.
7. Erdman SE, et al. (2003) CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 162:691-702. (Pubitemid 36267876)
8. Okayasu I, et al. (2002) Dysplasia and carcinoma development in a repeated dextran sulfate sodium-induced colitis model. J Gastroenterol Hepatol 17:1078-1083. (Pubitemid 35013962)
9. Mangerich A, et al. (2012) Infection-induced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc Natl Acad Sci USA 109:E1820-E1829.
10. Meira LB, et al. (2008) DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice. J Clin Invest 118:2516-2525. (Pubitemid 351949779)
11. D'Incà R, et al. (2004) Oxidative DNA damage in the mucosa of ulcerative colitis increases with disease duration and dysplasia. Inflamm Bowel Dis 10:23-27.
12. Hussain SP, et al. (2000) Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: A cancer-prone chronic inflammatory disease. Cancer Res 60:3333-3337. (Pubitemid 30482141)
13. de la Chapelle A (2004) Genetic predisposition to colorectal cancer. Nat Rev Cancer 4:769-780.
14. Powell SM, et al. (1992) APC mutations occur early during colorectal tumorigenesis. Nature 359:235-237.
15. Fearnhead NS, Britton MP, Bodmer WF (2001) The ABC of APC. Hum Mol Genet 10:721-733. (Pubitemid 32331581)
16. Morin PJ, et al. (1997) Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275:1787-1790. (Pubitemid 27136715)
17. Gupta RA, Dubois RN (2001) Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat Rev Cancer 1:11-21. (Pubitemid 33741877)
18. Rothwell PM, et al. (2011) Effect of daily aspirin on long-term risk of death due to cancer: Analysis of individual patient data from randomised trials. Lancet 377:31-41.
19. Rothwell PM, et al. (2010) Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials. Lancet 376:1741-1750.
20. Oshima M, et al. (1996) Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87:803-809. (Pubitemid 26404280)
21. Ahn B, Ohshima H (2001) Suppression of intestinal polyposis in Apc(Min/+) mice by inhibiting nitric oxide production. Cancer Res 61:8357-8360. (Pubitemid 33131104)
22. Kohno H, et al. (2007) A specific inducible nitric oxide synthase inhibitor, ONO-1714 attenuates inflammation-related large bowel carcinogenesis in male Apc(Min/+) mice. Int J Cancer 121(3):506-513. (Pubitemid 46986482)
23. MacMicking J, Xie QW, Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15:323-350. (Pubitemid 27169284)
24. Beck PL, et al. (2004) Paradoxical roles of different nitric oxide synthase isoforms in colonic injury. Am J Physiol Gastrointest Liver Physiol 286:G137-G147. (Pubitemid 38055847)
25. Kolios G, Valatas V, Ward SG (2004) Nitric oxide in inflammatory bowel disease: A universal messenger in an unsolved puzzle. Immunology 113:427-437. (Pubitemid 39593361)
26. Hoffman RA, et al. (1997) Constitutive expression of inducible nitric oxide synthase in the mouse ileal mucosa. Am J Physiol 272:G383-G392. (Pubitemid 27137253)
27. Karin M (2006) Nuclear factor-kappaB in cancer development and progression. Nature 441:431-436.
28. Ben-Neriah Y, Karin M (2011) Inflammation meets cancer, with NF-κB as the matchmaker. Nat Immunol 12:715-723.
29. Häcker H, Karin M (2006) Regulation and function of IKK and IKK-related kinases. Sci STKE 2006:re13.
30. Vlantis K, et al. (2011) Constitutive IKK2 activation in intestinal epithelial cells induces intestinal tumors in mice. J Clin Invest 121:2781-2793.
31. Guma M, et al. (2011) Constitutive intestinal NF-κB does not trigger destructive inflammation unless accompanied by MAPK activation. J Exp Med 208:1889-1900.
32. Blache P, et al. (2004) SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 166:37-47. (Pubitemid 38931915)
33. Matheu A, et al. (2012) Oncogenicity of the developmental transcription factor Sox9. Cancer Res 72:1301-1315.
34. Sansom OJ, et al. (2007) Myc deletion rescues Apc deficiency in the small intestine. Nature 446:676-679. (Pubitemid 46606884)
35. Muncan V, et al. (2006) Rapid loss of intestinal crypts upon conditional deletion of the Wnt/Tcf-4 target gene c-Myc. Mol Cell Biol 26:8418-8426. (Pubitemid 44748575)
36. Hinoi T, et al. (2007) Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation. Cancer Res 67:9721-9730. (Pubitemid 47621219)
37. Neufert C, Becker C, Neurath MF (2007) An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protoc 2:1998-2004. (Pubitemid 47308138)
38. van der Flier LG, et al. (2009) Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136:903-912.
39. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: Structure, function and inhibition. Biochem J 357:593-615. (Pubitemid 32735142)
40. Wang J, et al. (2011) Quantification of oxidative DNA lesions in tissues of Long-Evans Cinnamon rats by capillary high-performance liquid chromatography-tandem mass spectrometry coupled with stable isotope-dilution method. Anal Chem 83:2201-2209.
41. Wang Y (2008) Bulky DNA lesions induced by reactive oxygen species. Chem Res Toxicol 21:276-281.
42. Jaruga P, Dizdaroglu M (2008) 8,5′-Cyclopurine-2′- deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst) 7: 1413-1425.
43. Brooks PJ, et al. (2000) The oxidative DNA lesion 8,5′-(S)-cyclo- 2′-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J Biol Chem 275:22355-22362. (Pubitemid 30621821)
44. Kuraoka I, et al. (2000) Removal of oxygen free-radical-induced 5′,8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci USA 97:3832-3837. (Pubitemid 30226047)
45. Sung JS, Demple B (2006) Roles of base excision repair subpathways in correcting oxidized abasic sites in DNA. FEBS J 273:1620-1629.
46. Kow YW (2002) Repair of deaminated bases in DNA. Free Radic Biol Med 33:886-893.
47. Helleday T, Lo J, van Gent DC, Engelward BP (2007) DNA double-strand break repair: From mechanistic understanding to cancer treatment. DNA Repair (Amst) 6:923-935. (Pubitemid 46880473)
48. Hussain SP, Hofseth LJ, Harris CC (2003) Radical causes of cancer. Nat Rev Cancer 3:276-285. (Pubitemid 37328863)
49. Yin J, et al. (1993) p53 point mutations in dysplastic and cancerous ulcerative colitis lesions. Gastroenterology 104:1633-1639. (Pubitemid 23235452)
50. Luongo C, Moser AR, Gledhill S, Dove WF (1994) Loss of Apc+ in intestinal adenomas from Min mice. Cancer Res 54:5947-5952. (Pubitemid 24375232)
51. Erdman SE, et al. (2009) Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc Natl Acad Sci USA 106:1027-1032.
52. Burney S, Caulfield JL, Niles JC, Wishnok JS, Tannenbaum SR (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat Res 424:37-49. (Pubitemid 29101606)
53. Kuzminov A (2001) Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc Natl Acad Sci USA 98:8241-8246.
54. Haigis KM, Dove WF (2003) A Robertsonian translocation suppresses a somatic recombination pathway to loss of heterozygosity. Nat Genet 33:33-39. (Pubitemid 36068679)
55. Kiziltepe T, et al. (2005) Delineation of the chemical pathways underlying nitric oxide-induced homologous recombination in mammalian cells. Chem Biol 12:357-369. (Pubitemid 40406283)