Curcumin abrogates bile-induced NF-κB activity and DNA damage in vitro and suppresses NF-κB activity whilst promoting apoptosis in vivo, suggesting chemopreventative potential in Barrett's oesophagus

Clinical and Translational Oncology

Volumn 14, Issue 4, 2012, Pages 302-311

  Rawat, Nihit ^a   Alhamdani, Ali ^a   McAdam, Elizabeth ^b   Cronin, James ^b   Eltahir, Zak ^b   Lewis, Paul ^b   Griffiths, Paul ^a   Baxter, John N ^a   Jenkins, Gareth J S ^b  

^a MORRISTON HOSPITAL   (United Kingdom)

^b SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

Barrett's oesophagus; Curcumin; NF B

Indexed keywords

BILE ACID; CURCUMIN; DEOXYCHOLIC ACID; DNA; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; TRANSCRIPTION FACTOR RELA;

ABSENCE OF SIDE EFFECTS; APOPTOSIS; ARTICLE; BARRETT ESOPHAGUS; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DRUG TOLERABILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; ESOPHAGOSCOPY; ESOPHAGUS BIOPSY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MICRONUCLEUS TEST; PILOT STUDY; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SUPPLEMENTATION; TREATMENT DURATION;

ADENOCARCINOMA; AGED; ANTICARCINOGENIC AGENTS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BARRETT ESOPHAGUS; BILE; BIOPSY; CELL LINE, TUMOR; CURCUMIN; DNA DAMAGE; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESOPHAGEAL NEOPLASMS; FEMALE; HUMANS; MALE; MIDDLE AGED; NF-KAPPA B; PILOT PROJECTS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84860742595     PISSN: 1699048X     EISSN: 16993055     Source Type: Journal    
DOI: 10.1007/s12094-012-0799-x     Document Type: Article

References (61)

1. Cameron AJ, Lomboy CT (1992) Barrett's oesophagus: age, prevalence, and extent of columnar epithelium. Gastroenterology 103:1241-1245
2. Spechler SJ, Zeroogian JM, Antonioli DA et al (1994) Prevalence of metaplasia at the gastrooesophageal junction. Lancet 344:1533-1536
3. Ronkainen J, Aro P, Storskrubb T et al (2005) Prevalence of Barrett's oesophagus in the general population: an endoscopic study. Gastroenterology 129:1825-1831 (Pubitemid 41772961)
4. Jankowski JA, Harrison RF, Perry I et al (2000) Barrett's metaplasia. Lancet 356:2079-2085 (Pubitemid 32009828)
5. Wild CP, Hardie LJ (2003) Reflux, Barrett's oesophagus and adenocarcinoma: burning questions. Nat Rev Cancer 3:676-684 (Pubitemid 37328822)
6. Abdel-Latif MM, O'Riordan J, Windle HJ et al (2004) NF-kappaB activation in esophageal adenocarcinoma: relationship to Barrett's metaplasia, survival, and response to neoadjuvant chemoradiotherapy. Ann Surg 239:491-500 (Pubitemid 38372765)
7. Jenkins GJ, Harries K, Doak SH et al (2004) The bile acid deoxycholic acid (DCA) at neutral pH activates NF-kappaB and induces IL-8 expression in oesophageal cells in vitro. Carcinogenesis 25: 317-323 (Pubitemid 38344397)
8. Rayet B, Gelinas C (1999) Aberrant rel/nfkb genes and activity in human cancer. Oncogene 18:6938-6947
9. Arlt A, Gehrz A, Muerkoster S et al (2003) Role of NF-kappaB and Akt/PI3K in the resistance of pancreatic carcinoma cell lines against gemcitabine-induced cell death. Oncogene 22:3243-3251 (Pubitemid 36712936)
10. Kunnumakkara AB, Guha S, Krishnan S et al (2007) Curcumin potentiates antitumor activity of gemcitabine in an orthotopic model of pancreatic cancer through suppression of proliferation, angiogenesis, and inhibition of nuclear factorkappaB-regulated gene products. Cancer Res 67: 3853-3861 (Pubitemid 46762173)
11. Attwood SE, Smyrk TC, DeMeester TR et al (1992) Duodenoesophageal reflux and the development of esophageal adenocarcinoma in rats. Surgery 111:503-510
12. Gillen P, Keeling P, Byrne PJ et al (1988) Implication of duodenogastric reflux in the pathogenesis of Barrett's oesophagus. Br J Surg 75:540-543
13. Tselepis C, Morris CD, Wakelin D et al (2003) Upregulation of the oncogene c-myc in Barrett's adenocarcinoma: induction of c-myc by acidified bile acid in vitro. Gut 52:174-180 (Pubitemid 36115055)
14. Jenkins GJ, D'Souza FR, Suzen SH et al (2007) Deoxycholic acid at neutral and acid pH, is genotoxic to oesophageal cells through the induction of ROS: The potential role of anti-oxidants in Barrett's oesophagus. Carcinogenesis 28:136-142 (Pubitemid 44942637)
15. Jenkins GJ, Cronin J, Alhamdani A et al (2008) The bile acid deoxycholic acid has a non-linear dose response for DNA damage and possibly NF-kappaB activation in oesophageal cells, with a mechanism of action involving ROS. Mutagenesis 23:399-405
16. Odot J, Albert P, Carlier A et al (2004) In vitro and in vivo anti-tumoral effect of curcumin against melanoma cells. Int J Cancer 111:381-387 (Pubitemid 38998818)
17. Dhillon N, Aggarwal BB, Newman RA et al (2008) Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin Cancer Res 14: 4491-4499
18. Subramanian M, Sreejayan, Rao MN et al (1994) Diminution of singlet oxygen-induced DNA damage by curcumin and related antioxidants. Mutat Res 311:249-255 (Pubitemid 24357451)
19. Huang MT, Lysz T, Ferraro T et al (1991) Inhibitory effects of curcumin on in vitro lipoxygenase and cyclooxygenase activities in mouse epidermis. Cancer Res 51:813-819
20. Gao X, Kuo J, Jiang H et al (2004) Immunomodulatory activity of curcumin: suppression of lymphocyte proliferation, development of cellmediated cytotoxicity, and cytokine production in vitro. Biochem Pharmacol 68:51-61 (Pubitemid 38746541)
21. Baatout S, Derradji H, Jacquet P et al (2004) Effect of curcuma on radiation-induced apoptosis in human cancer cells. Int J Oncol 24:321-329
22. Wang Z, Zhang Y, Banerjee S et al (2006) Notch-1 down-regulation by curcumin is associated with the inhibition of cell growth and the induction of apoptosis in pancreatic cancer cells. Cancer 106: 2503-2513 (Pubitemid 43787677)
23. Joe B, Vijaykumar M, Lokesh BR (2004) Biological properties of curcumin-cellular and molecular mechanisms of action. Crit Rev Food Sci Nutr 44:97-111 (Pubitemid 38552286)
24. Eigner D, Scholz D (1999) Ferula asa-foetida and Curcuma longa in traditional medical treatment and diet in Nepal. J Ethnopharmacol 67:1-6 (Pubitemid 29389737)
25. Kunnumakkara AB, Diagaradjane P, Guha S et al (2008) Curcumin sensitizes human colorectal cancer xenografts in nude mice to gamma-radiation by targeting nuclear factor-kappaB-regulated gene products. Clin Cancer Res 14:2128-2136 (Pubitemid 351551125)
26. Su CC, Chen GW, Lin JG et al (2006) Curcumin inhibits cell migration of human colon cancer colo 205 cells through the inhibition of nuclear factor kappa B /p65 and down-regulates cyclooxygenase-2 and matrix metalloproteinase-2 expressions. Anticancer Res 26:1281-1288
27. Aggarwal BB, Kumar A, Bharti AC (2003) Anticancer potential of curcumin: preclinical and clinical studies. Anticancer Res 23:363-398 (Pubitemid 36361976)
28. Mohandas KM, Desai DC (1999) Epidemiology of digestive tract cancers in India. V. Large and small bowel. Indian J Gastroenterol 18:118-121
29. Amarapurkar AD, Vora IM, Dhawan PS (1998) Barrett's oesophagus. Indian J Pathol Microbiol 41:431-435
30. Dhawan PS, Alvares JF, Vora IM et al (2001) Prevalence of short segments of specialized columnar epithelium in distal oesophagus: association with gastroesophageal reflux. Indian J Gastroenterol 20:144-147
31. Fenech M (2000) The in vitro micronucleus technique. Mutat Res 455:81-95
32. Nehra D, Howell P, Williams CP et al (1999) Toxic bile acids in gastro-oesophageal reflux disease: influence of gastric acidity. Gut 44:598-602 (Pubitemid 29195903)
33. Jenkins GJ, Mikhail J, Alhamdani A et al (2007) Immunohistochemical study of nuclear factorkappaB activity and interleukin-8 abundance in oesophageal adenocarcinoma; a useful strategy for monitoring these biomarkers. J Clin Pathol 60:1232-1237 (Pubitemid 350084544)
34. Soni KB, Kuttan R (1992) Effect of oral curcumin administration on serum peroxides and cholesterol levels in human volunteers. Indian J Physiol Pharmacol 36:273-275 (Pubitemid 23031285)
35. Cheng AL, Hsu CH, Lin JK et al (2001) Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res 21:2895-2900
36. Sharma RA, Euden SA, Platton SL et al (2004) Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin Cancer Res 10:6847-6854 (Pubitemid 39383033)
37. Lao CD, Ruffin MTt, Normolle D et al (2006) Dose escalation of a curcuminoid formulation. BMC Complement Altern Med 6:10
38. Wetscher GJ, Hinder RA, Bagchi D et al (1995) Reflux esophagitis in humans is mediated by oxygen-derived free radicals. Am J Surg 170:552-556; discussion 6-7
39. Liu L, Ergun G, Ertan A et al (2003) Detection of oxidative DNA damage in oesophageal biopsies of patients with reflux symptoms and normal pH monitoring. Aliment Pharmacol Ther 18:693-698 (Pubitemid 37271834)
40. Tzonou A, Lipworth L, Garidou A et al (1996) Diet and risk of esophageal cancer by histologic type in a low-risk population. Int J Cancer 68:300-304 (Pubitemid 26384131)
41. Terry P, Lagergren J, Ye W et al (2000) Antioxidants and cancers of the oesophagus and gastric cardia. Int J Cancer 87:750-754 (Pubitemid 30620420)
42. Sun SC, Ganchi PA, Ballard DW et al (1993) NFkappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science 259:1912-1915 (Pubitemid 23124465)
43. Xu L, Fidler IJ (2000) Interleukin 8: an autocrine growth factor for human ovarian cancer. Oncol Res 12:97-106
44. Lazar-Molnar E, Hegyesi H, Toth S et al (2000) Autocrine and paracrine regulation by cytokines and growth factors in melanoma. Cytokine 12:547-554 (Pubitemid 30453481)
45. Huang S, Robinson JB, Deguzman A et al (2000) Blockade of nuclear factor-kappaB signaling inhibits angiogenesis and tumorigenicity of human ovarian cancer cells by suppressing expression of vascular endothelial growth factor and interleukin 8. Cancer Res 60:5334-5339
46. Harada A, Sekido N, Akahoshi T et al (1994) Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56:559-564 (Pubitemid 24348812)
47. Hidaka H, Ishiko T, Furuhashi T et al (2002) Curcumin inhibits interleukin 8 production and enhances interleukin 8 receptor expression on the cell surface: impact on human pancreatic carcinoma cell growth by autocrine regulation. Cancer 95:1206-1214 (Pubitemid 35013053)
48. O'Riordan JM, Abdel-latif MM, Ravi N et al (2005) Proinflammatory cytokine and nuclear factor kappa-B expression along the inflammation- metaplasia-dysplasia-adenocarcinoma sequence in the oesophagus. Am J Gastroenterol 100:1257-1264 (Pubitemid 40904346)
49. Konturek PC, Nikiforuk A, Kania J et al (2004) Activation of NFkappaB represents the central event in the neoplastic progression associated with Barrett's oesophagus: a possible link to the inflammation and overexpression of COX-2, PPARgamma and growth factors. Dig Dis Sci 49:1075-1083 (Pubitemid 39178068)
50. Rafiee P, Nelson VM, Manley S et al (2009) Effect of curcumin on acidic pH-induced expression of IL-6 and IL-8 in human esophageal epithelial cells (HET-1A): role of PKC, MAPKs, and NFkappaB. Am J Physiol Gastrointest Liver Physiol 296:G388-398
51. Freudlsperger C, Greten J, Schumacher U (2008) Curcumin induces apoptosis in human neuroblastoma cells via inhibition of NFkappaB. Anticancer Res 28:209-214 (Pubitemid 351362903)
52. Collett GP, Campbell FC (2004) Curcumin induces c-jun N-terminal kinase-dependent apoptosis in HCT116 human colon cancer cells. Carcinogenesis 25:2183-2189 (Pubitemid 39534856)
53. Reuter S, Eifes S, Dicato M et al (2008) Modulation of anti-apoptotic and survival pathways by curcumin as a strategy to induce apoptosis in cancer cells. Biochem Pharmacol 76:1340-1351
54. van der Woude CJ, Jansen PL, Tiebosch AT et al (2002) Expression of apoptosis-related proteins in Barrett's metaplasia-dysplasia-carcinoma sequence: a switch to a more resistant phenotype. Hum Pathol 33:686-692 (Pubitemid 34953346)
55. Iravani S, Zhang HQ, Yuan ZQ et al (2003) Modification of insulin-like growth factor 1 receptor, c-Src, and Bcl-XL protein expression during the progression of Barrett's neoplasia. Hum Pathol 34:975-982 (Pubitemid 37315248)
56. Hormi-Carver K, Zhang X, Zhang HY et al (2009) Unlike esophageal squamous cells, Barrett's epithelial cells resist apoptosis by activating the nuclear factor-kappaB pathway. Cancer Res 69: 672-677
57. Whittles CE, Biddlestone LR, Burton A et al (1999) Apoptotic and proliferative activity in the neoplastic progression of Barrett's oesophagus: a comparative study. J Pathol 187:535-540 (Pubitemid 29151994)
58. O'Sullivan-Coyne G, O'Sullivan GC, O'Donovan TR et al (2009) Curcumin induces apoptosisindependent death in oesophageal cancer cells. Br J Cancer 101:1585-1595
59. Hartojo W, Silvers AL, Thomas DG et al (2010) Curcumin promotes apoptosis, increases chemosensitivity, and inhibits nuclear factor kappaB in esophageal adenocarcinoma. Transl Oncol 3:99-108
60. Ford AC, Forman D, Reynolds PD et al (2005) Ethnicity, gender, and socioeconomic status as risk factors for esophagitis and Barrett's oesophagus. Am J Epidemiol 162:454-460 (Pubitemid 41191431)
61. Bisht S, Feldmann G, Soni S et al (2007) Polymeric nanoparticle- encapsulated curcumin ("nanocurcumin"): a novel strategy for human cancer therapy. J Nanobiotechnol 5:3