DUOX2 and DUOXA2 form the predominant enzyme system capable of producing the reactive oxygen species H2O2 in active ulcerative colitis and are modulated by 5-aminosalicylic acid

Inflammatory Bowel Diseases

Volumn 20, Issue 3, 2014, Pages 514-524

  MacFie, Tammie S ^a   Poulsom, Richard ^a   Parker, Alexandra ^a   Warnes, Gary ^a   Boitsova, Tatjana ^a   Nijhuis, Anke ^a   Suraweera, Nirosha ^a   Poehlmann, Angela ^b   Szary, Jaroslaw ^a   Feakins, Roger ^c   Jeffery, Rosemary ^a   Harper, Richart W ^d   Jubb, Adrian M ^e   Lindsay, James O ^a   Silver, Andrew ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c ROYAL LONDON HOSPITAL   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e GENENTECH INC   (United States)

Author keywords

DNA damage; Hydrogen peroxide; Mesalazine; Ulcerative colitis

Indexed keywords

DUOX2 PROTEIN; DUOXA2 PROTEIN; HISTONE H2AX; HYDROGEN PEROXIDE; MESALAZINE; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; COLON BIOPSY; COLON MUCOSA; COLORECTAL CANCER; CONTROLLED STUDY; DESCENDING COLON; DISEASE COURSE; DNA DAMAGE; DRUG EFFECT; DYSPLASIA; EPITHELIUM CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RECTUM; RECTUM BIOPSY; TRANSVERSE COLON; ULCERATIVE COLITIS; UPREGULATION;

ADENOMA; ANOXIA; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BLOTTING, WESTERN; CELLS, CULTURED; COLITIS, ULCERATIVE; COLONIC NEOPLASMS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; HYDROGEN PEROXIDE; IN SITU HYBRIDIZATION; INFLAMMATION; MEMBRANE PROTEINS; MESALAMINE; NADPH OXIDASE; OXIDANTS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84898714684     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/01.MIB.0000442012.45038.0e     Document Type: Article

References (72)

1. Rutter MD, Saunders BP, Wilkinson KH, et al. Cancer surveillance in longstanding ulcerative colitis: endoscopic appearances help predict cancer risk. Gut. 2004;53:1813-1816.
2. Dignass A, Lindsay JO, Sturm A, et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 2: current management. J Crohns Colitis. 2012;6:991-1030.
3. Croog VJ, Ullman TA, Itzkowitz SH. Chemoprevention of colorectal cancer in ulcerative colitis. Int J Colorectal Dis. 2003;18:392-400.
4. Tang J, Sharif O, Pai C, et al. Mesalamine protects against colorectal cancer in inflammatory bowel disease. Dig Dis Sci. 2010;55:1696-1703.
5. Varmus H, Harlow E. Science funding: provocative questions in cancer research. Nature. 2012;481:436-437.
6. Rousseaux C, Lefebvre B, Dubuquoy L, et al. Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferatoractivated receptor-gamma. J Exp Med. 2005;201:1205-1215.
7. Monteleone G, Franchi L, Fina D, et al. Silencing of SH-PTP2 defines a crucial role in the inactivation of epidermal growth factor receptor by 5-aminosalicylic acid in colon cancer cells. Cell Death Differ. 2006;13: 202-211.
8. Reinacher-Schick A, Schoeneck A, Graeven U, et al. Mesalazine causes a mitotic arrest and induces caspase-dependent apoptosis in colon carcinoma cells. Carcinogenesis. 2003;24:443-451.
9. Stolfi C, Fina D, Caruso R, et al. Mesalazine negatively regulates CDC25A protein expression and promotes accumulation of colon cancer cells in S phase. Carcinogenesis. 2008;29:1258-1266.
10. Brown WA, Farmer KC, Skinner SA, et al. 5-Aminosalicyclic acid and olsalazine inhibit tumor growth in a rodent model of colorectal cancer. Dig Dis Sci. 2000;45:1578-1584.
11. Munding J, Ziebarth W, Pox CP, et al. The influence of 5-aminosalicylic acid on the progression of colorectal adenomas via the beta-catenin signaling pathway. Carcinogenesis. 2012;33:637-643.
12. Willenbucher RF, Aust DE, Chang CG, et al. Genomic instability is an early event during the progression pathway of ulcerative-colitis-related neoplasia. Am J Pathol. 1999;154:1825-1830.
13. Luciani MG, Campregher C, Fortune JM, et al. 5-ASA affects cell cycle progression in colorectal cells by reversibly activating a replication checkpoint. Gastroenterology. 2007;132:221-235.
14. Couto D, Ribeiro D, Freitas M, et al. Scavenging of reactive oxygen and nitrogen species by the prodrug sulfasalazine and its metabolites 5-aminosalicylic acid and sulfapyridine. Redox Rep. 2010;15:259-267.
15. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313.
16. Sedelnikova OA, Redon CE, Dickey JS, et al. Role of oxidatively induced DNA lesions in human pathogenesis. Mutat Res. 2010;704:152-159.
17. Edens WA, Sharling L, Cheng G, et al. Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol. 2001;154:879-891.
18. Cheng G, Cao Z, Xu X, et al. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene. 2001;269:131-140.
19. Szanto I, Rubbia-Brandt L, Kiss P, et al. Expression of NOX1, a superoxidegenerating NADPH oxidase, in colon cancer and inflammatory bowel disease. J Pathol. 2005;207:164-176.
20. El Hassani RA, Benfares N, Caillou B, et al. Dual oxidase2 is expressed all along the digestive tract. Am J Physiol Gastrointest Liver Physiol. 2005;288:G933-G942.
21. Athanasiadou S, Jones LA, Burgess STG, et al. Genome-wide transcriptomic analysis of intestinal tissue to assess the impact of nutrition and a secondary nematode challenge in lactating rats. PLoS One. 2011;6: 20771.
22. Flores MV, Crawford KC, Pullin LM, et al. Dual oxidase in the intestinal epithelium of zebrafish larvae has anti-bacterial properties. Biochem Biophys Res Commun. 2010;400:164-168.
23. Bae YS, Choi MK, Lee WJ. Dual oxidase in mucosal immunity and hostmicrobe homeostasis. Trends Immunol. 2010;31:278-287.
24. Ha EM, Lee KA, Seo YY, et al. Coordination of multiple dual oxidaseregulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nat Immunol. 2009;10:949-957.
25. InadaM, Kihara K, Kono T, et al. Deciphering of the dual oxidase (Nox family) gene from kuruma shrimp, Marsupenaeus japonicus: full-length cDNA cloning and characterization. Fish Shellfish Immunol. 2013;34:471-485.
26. Lees MS, Robinson NA, Ingham AB, et al. Dual oxidase 2 and glutathione peroxidase gene expression are elevated in hyperimmunized sheep challenged with Haemonchus contortus. Vet Parasitol. 2011;179:113-122.
27. D'Errico M, Parlanti E, Dogliotti E. Mechanism of oxidative DNA damage repair and relevance to human pathology. Mutat Res. 2008;659:4-14.
28. Driessens N, Versteyhe S, Ghaddhab C, et al. Hydrogen peroxide induces DNA single-and double-strand breaks in thyroid cells and is therefore a potential mutagen for this organ. Endocr Relat Cancer. 2009;16:845-856.
29. Ameziane-El-Hassani R, Boufraqech M, Lagente-Chevallier O, et al. Role of H2O2 in RET/PTC1 chromosomal rearrangement produced by ionizing radiation in human thyroid cells. Cancer Res. 2010;70:4123-4132.
30. Homfray TF, Cottrell SE, Ilyas M, et al. Defects in mismatch repair occur after APC mutations in the pathogenesis of sporadic colorectal tumours. Hum Mutat. 1998;11:114-120.
31. Rowan AJ, Lamlum H, Ilyas M, et al. APC mutations in sporadic colorectal tumors: a mutational "hotspot" and interdependence of the "two hits". Proc Natl Acad Sci U S A. 2000;97:3352-3357.
32. Wheeler JM, Beck NE, Kim HC, et al. Mechanisms of inactivation of mismatch repair genes in human colorectal cancer cell lines: the predominant role of hMLH1. Proc Natl Acad Sci U S A. 1999;96:10296-10301.
33. Wong NA, Britton MP, Choi GS, et al. Loss of CDX1 expression in colorectal carcinoma: promoter methylation, mutation, and loss of heterozygosity analyses of 37 cell lines. Proc Natl Acad Sci U S A. 2004;101: 574-579.
34. Woodford-Richens KL, Rowan AJ, Gorman P, et al. SMAD4 mutations in colorectal cancer probably occur before chromosomal instability, but after divergence of the microsatellite instability pathway. Proc Natl Acad Sci U S A. 2001;98:9719-9723.
35. Liu Y, Bodmer WF. Analysis of P53 mutations and their expression in 56 colorectal cancer cell lines. Proc Natl Acad Sci U S A. 2006;103:976-981.
36. Bracht K, Nicholls AM, Liu Y, et al. 5-Fluorouracil response in a large panel of colorectal cancer cell lines is associated with mismatch repair deficiency. Br J Cancer. 2010;103:340-346.
37. Ashraf SQ, Nicholls AM, Wilding JL, et al. Direct and immune mediated antibody targeting of ERBB receptors in a colorectal cancer cell-line panel. Proc Natl Acad Sci U S A. 2012;109:21046-21051.
38. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30:207-210.
39. Lauritsen K, Hansen J, Ryde M, et al., Colonic azodisalicylate metabolism determined by in vivo dialysis in healthy volunteers and patients with ulcerative colitis. Gastroenterology. 1984;86:1496-1500.
40. Staerk Laursen L, Stokholm M, Bukhave K, et al. Disposition of 5-aminosalicylic acid by olsalazine and three mesalazine preparations in patients with ulcerative colitis: comparison of intraluminal colonic concentrations, serum values, and urinary excretion. Gut. 1990;31: 1271-1276.
41. Jacobsen BA, Abildgaard K, Rasmussen HH, et al. Availability of mesalazine (5-aminosalicylic acid) from enemas and suppositories during steady-state conditions. Scand J Gastroenterol. 1991;26:374-378.
42. Christensen LA, Fallingborg J, Abildgaard K, et al. Topical and systemic availability of 5-aminosalicylate: comparisons of three controlled release preparations in man. Aliment Pharmacol Ther. 1990;4:523-533.
43. Fina D, Franchi L, Caruso R, et al. 5-Aminosalicylic acid enhances anchorage-independent colorectal cancer cell death. Eur J Cancer. 2006;42:2609-2616.
44. Kim YH, Kim MH, Kim BJ, et al. Inhibition of cell proliferation and invasion in a human colon cancer cell line by 5-aminosalicylic acid. Dig Liver Dis. 2009;41:328-337.
45. Campregher C, Luciani MG, Biesenbach P, et al. The position of the amino group on the benzene ring is critical for mesalamine's improvement of replication fidelity. Inflamm Bowel Dis. 2010;16:576-582.
46. Koelink PJ, Mieremet-Ooms MA, Corver WE, et al. 5-Aminosalicylic acid interferes in the cell cycle of colorectal cancer cells and induces cell death modes. Inflamm Bowel Dis. 2010;16:379-389.
47. Honeder C, Campregher C, Zens B, et al. Improvement of replication fidelity by certain mesalazine derivatives. Int J Oncol. 2012;40:1331-1338.
48. Khare V, Lyakhovich A, Dammann K, et al. Mesalamine modulates intercellular adhesion through inhibition of p-21 activated kinase-1. Biochem Pharmacol. 2012;85:234-244.
49. Poulsom R, Longcroft JM, Jeffery RE, et al. A robust method for isotopic riboprobe in situ hybridisation to localise mRNAs in routine pathology specimens. Eur J Histochem. 1998;42:121-132.
50. Marty GD. Blank-field correction for achieving a uniform white background in brightfield digital photomicrographs. Biotechniques. 2007;42: 716, 8, 20.
51. Linderholm AL, Onitsuka J, Xu C, et al. All-trans retinoic acid mediates DUOX2 expression and function in respiratory tract epithelium. Am J Physiol Lung Cell Mol Physiol. 2010;299:L215-L221.
52. Hoste C, Dumont JE, Miot F, et al. The type of DUOX-dependent ROS production is dictated by defined sequences in DUOXA. Exp Cell Res. 2012;318:2353-2364.
53. Subramanian S, Rhodes JM, Hart CA, et al. Characterization of epithelial IL-8 response to inflammatory bowel disease mucosal E. coli and its inhibition by mesalamine. Inflamm Bowel Dis. 2008;14:162-175.
54. Wu Y, Antony S, Juhasz A, et al. Up-regulation and sustained activation of Stat1 are essential for interferon-gamma (IFN-gamma)-induced dual oxidase 2 (Duox2) and dual oxidase A2 (DuoxA2) expression in human pancreatic cancer cell lines. J Biol Chem. 2011;286:12245-12256.
55. Sorensen CS, Syljuasen RG. Safeguarding genome integrity: the checkpoint kinases ATR, CHK1 and WEE1 restrain CDK activity during normal DNA replication. Nucleic Acids Res. 2012;40:477-486.
56. Kaidi A, Qualtrough D, Williams AC, et al. Direct transcriptional upregulation of cyclooxygenase-2 by hypoxia-inducible factor (HIF)-1 promotes colorectal tumor cell survival and enhances HIF-1 transcriptional activity during hypoxia. Cancer Res. 2006;66:6683-6691.
57. Chavez V, Mohri-Shiomi A, Garsin DA. Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect Immun. 2009;77:4983-4989.
58. Ha EM, Oh CT, Bae YS, et al. A direct role for dual oxidase in Drosophila gut immunity. Science. 2005;310:847-850.
59. Li RW, Gasbarre LC. A temporal shift in regulatory networks and pathways in the bovine small intestine during Cooperia oncophora infection. Int J Parasitol. 2009;39:813-824.
60. Lee KA, Kim SH, Kim EK, et al. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell. 2013;153:797-811.
61. Grasberger H, El-Zaatari M, Merchant JL. Dual oxidases control release of hydrogen peroxide by the gastric epithelium to prevent Helicobacter felis infection and inflammation in mice. Gastroenterology. 2013;145: 1045-1054.
62. Monteleone G, Fina D, Caruso R, et al. New mediators of immunity and inflammation in inflammatory bowel disease. Curr Opin Gastroenterol. 2006;22:361-364.
63. Yoo SK, Starnes TW, Deng Q, et al. Lyn is a redox sensor that mediates leukocyte wound attraction in vivo. Nature. 2011;480:109-112.
64. Lipinski S, Till A, Sina C, et al. DUOX2-derived reactive oxygen species are effectors of NOD2-mediated antibacterial responses. J Cell Sci. 2009; 122(pt 19):3522-3530.
65. Kita H, Hikichi Y, Hikami K, et al. Differential gene expression between flat adenoma and normal mucosa in the colon in a microarray analysis. J Gastroenterol. 2006;41:1053-1063.
66. Juhasz A, Ge Y, Markel S, et al. Expression of NADPH oxidase homologues and accessory genes in human cancer cell lines, tumours and adjacent normal tissues. Free Radic Res. 2009;43:523-532.
67. Stolfi C, Pallone F, Monteleone G. Colorectal cancer chemoprevention by mesalazine and its derivatives. J Biomed Biotechnol. 2012;2012:980458.
68. Nguyen GC, Gulamhusein A, Bernstein CN. 5-Aminosalicylic acid is not protective against colorectal cancer in inflammatory bowel disease: a meta-analysis of non-referral populations. Am J Gastroenterol. 2012; 107:1298-1304.
69. Bonner MY, Arbiser JL. Targeting NADPH oxidases for the treatment of cancer and inflammation. Cell Mol Life Sci. 2012;69:2435-2442.
70. Salmeen A, Park BO, Meyer T. The NADPH oxidases NOX4 and DUOX2 regulate cell cycle entry via a p53-dependent pathway. Oncogene. 2010;29:4473-4484.
71. Poehlmann A, Reissig K, Schonfeld P, et al. Repeated H2O2 exposure drives cell cycle progression in an in vitro model of ulcerative colitis. J Cell Mol Med. 2013;17:1619-1631.
72. D'Inca R, Cardin R, Benazzato L, et al. Oxidative DNA damage in the mucosa of ulcerative colitis increases with disease duration and dysplasia. Inflamm Bowel Dis. 2004;10:23-27.