Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Amelioration of 1,2 Dimethylhydrazine (DMH) Induced Colon Oxidative Stress, Inflammation and Tumor Promotion Response by Tannic Acid in Wistar Rats

  • Hamiza, Oday O. (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University)) ;
  • Rehman, Muneeb U. (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University)) ;
  • Tahir, Mir (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University)) ;
  • Khan, Rehan (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University)) ;
  • Khan, Abdul Quaiyoom (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University)) ;
  • Lateef, Abdul (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University)) ;
  • Ali, Farrah (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University)) ;
  • Sultana, Sarwat (Section of Molecular Carcinogenesis and Chemoprevention, Department of Medical Elementology and Toxicology, Jamia Hamdard (Hamdard University))
  • Published : 2012.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Colon cancer is the third most common malignant neoplasm in the world and it remains an important cause of death, especially in western countries. The toxic environmental pollutant, 1, 2-dimethylhydrazine (DMH), is also a colon-specific carcinogen. Tannic acid (TA) is reported to be effective against various types of chemically induced toxicity and also carcinogenesis. In the present study, we evaluated the chemopreventive efficacy of TA against DMH induced colon toxicity in a rat model. Efficacy of TA against the colon toxicity was evaluated in terms of biochemical estimation of antioxidant enzyme activities, lipid peroxidation, histopathological changes and expression of early molecular markers of inflammation and tumor promotion. DMH treatment induced oxidative stress enzymes (p<0.001) and an early inflammatory and tumor promotion response in the colons of Wistar rats. TA treatment prevented deteriorative effects induced by DMH through a protective mechanism that involved reduction of oxidative stress as well as COX-2, i-NOS, PCNA protein expression levels and TNF-${\alpha}$ (p<0.001) release. It could be concluded from our results that TA markedly protects against chemically induced colon toxicity and acts plausibly by virtue of its antioxidant, anti-inflammatory and antiproliferative activities.

Keywords

References

  1. Aggarwal BB, Gehlot P (2009). Inflammation and cancer: how friendly is the relationship for cancer patients? Curr Opin Pharmacol, 9, 351-69. https://doi.org/10.1016/j.coph.2009.06.020
  2. Ahmad ST, Arjumand W, Seth A, et al (2011). Preclinical renal cancer chemopreventive efficacy of geraniol by modulation of multiple molecular pathways. Toxicology, 290, 69-81. https://doi.org/10.1016/j.tox.2011.08.020
  3. Ahmad ST, Sultana S (2012). Tannic acid mitigates cisplatininduced nephrotoxicity in mice. Hum Exp Toxicol, 31, 145-56. https://doi.org/10.1177/0960327111414282
  4. Athar M, Khan WA, Mukhtar H (1989). Effect of dietary tannic acid on epidermal, lung, and forestomach polycyclic aromatic hydrocarbon metabolism and tumorigenicity in Sencar mice. Cancer Res, 49, 5784-8.
  5. Baskar AA, Al Numair KS, Gabriel Paulraj M, et al (2012). $\beta$-Sitosterol Prevents Lipid Peroxidation and Improves Antioxidant Status and Histoarchitecture in Rats with 1,2-Dimethylhydrazine-Induced Colon Cancer. J Med Food, 15, 335-43. https://doi.org/10.1089/jmf.2011.1780
  6. Biasco G, Paganelli GM, Santucci R, et al (1994). Methodological problems in the use of rectal cell proliferation as a biomarker of colorectal cancer risk. J Cell Biochem, 19, 55-60.
  7. Bickers DR, Athar M (2006). Oxidative stress in the pathogenesis of skin disease. J Invest Dermatol, 126, 2565-75. https://doi.org/10.1038/sj.jid.5700340
  8. Bolton WE, Mikulka WR, Healy CG, et al (1992). Expression of proliferation associated antigens in the cell cycle of synchronized mammalian cells. Cytometry, 13, 117-26. https://doi.org/10.1002/cyto.990130203
  9. Bravo R (1986). Synthesis of the nuclear protein cyclin (PCNA) and its relationship with DNA replication. Exp Cell Res, 163, 287-93. https://doi.org/10.1016/0014-4827(86)90059-5
  10. Bravo R, Frank R, Blundell PA, et al (1987). Cyclin/PCNA is the auxiliary protein of DNA polymerase-delta. Nature, 326, 515-7. https://doi.org/10.1038/326515a0
  11. Carlberg I, Mannervik B (1975). Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem, 250, 5475-80.
  12. Chao A, Thun MJ, Connell CJ, et al (2005). Meat consumption and risk of colorectal cancer. JAMA, 293, 172-82. https://doi.org/10.1001/jama.293.2.172
  13. Chen SC, Chung KT (2000). Mutagenicity and antimutagenicity studies of tannic acid and its related compounds. Food Chem Toxicol, 38, 1-5.
  14. Claiborne A (1985). Catalase activity, in: R.A. Greenwald (Ed.), CRC handbook of methods in oxygen radical research, CRC, Boca Raton, RA, 283-4.
  15. Dudeja PK, Brasitus TA (1990). 1,2-Dimethylhydrazineinduced alterations in lipid peroxidation in preneoplastic and neoplastic colonic tissues. Biochim Biophys Acta, 1046, 267-70. https://doi.org/10.1016/0005-2760(90)90240-X
  16. Eberhart CE, Coffey RJ, Radhika A, et al (1994). Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology, 107, 1183-8.
  17. Eizirik DL, Pavlovic D (1997). Is there a role for nitric oxide in beta-cell dysfunction and damage in IDDM? Diabetes Metab Rev, 13, 293-307. https://doi.org/10.1002/(SICI)1099-0895(199712)13:4<293::AID-DMR195>3.0.CO;2-4
  18. English DR, MacInnis RJ, Hodge AM, et al (2004). Red meat, chicken, and fish consumption and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev, 13, 1509-14.
  19. Fairman MP (1990). DNA polymerase delta/PCNA: actions and interactions. J Cell Sci, 95, 1-4.
  20. Ferguson LR (2001). Role of plant polyphenols in genomic stability. Mutat Res, 475, 89-111. https://doi.org/10.1016/S0027-5107(01)00073-2
  21. Fiala E (1975). Investigations into the metabolism and mode of action of the colon carcinogen 1, 2-dimethylhydrazine. Cancer, 36, 2407-12.
  22. Gali HU, Perchellet EM, Klish DS, et al (1992). Hydrolyzable tannins: potent inhibitors of hydroperoxide production and tumor promotion in mouse skin treated with 12-O-tetradecanoylphorbol-13-acetate in vivo. Int J Cancer, 51, 425-32. https://doi.org/10.1002/ijc.2910510315
  23. Gulcin I, Bursal E, Sehitoglu MH, et al (2010). Polyphenol contents and antioxidant activity of lyophilized aqueous extract of propolis from Erzurum, Turkey. Food Chem Toxicol, 48, 2227-38. https://doi.org/10.1016/j.fct.2010.05.053
  24. Habig WH, Pabst MJ, Jakoby WB, (1974). Glutathione-Stransferases: The first enzymatic step in mercapturic acid formation. J Biol Chem, 249, 7130-9.
  25. Hofseth LJ (2008). Nitric oxide as a target of complementary and alternative medicines to prevent and treat inflammation and cancer. Cancer Lett, 268, 10-30. https://doi.org/10.1016/j.canlet.2008.03.024
  26. Horikawa K, Mohri T, Tanaka Y, et al (1994). Moderate inhibition of mutagenicity and carcinogenicity of benzo[a] pyrene, 1,6-dinitropyrene and 3,9-dinitrofluoranthene by Chinese medicinal herbs. Mutagenesis, 9, 523-6. https://doi.org/10.1093/mutage/9.6.523
  27. Ionov Y, Peinado MA, Malkhosyan S, et al (1993). Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature, 363, 558-61. https://doi.org/10.1038/363558a0
  28. Jain M, Cook GM, Davis FG, et al (1980). A case-control study of diet and color-ectal cancer. Int J Cancer, 26, 757-68. https://doi.org/10.1002/ijc.2910260609
  29. Jaskulski D, deRiel JK, Mercer WE, et al (1988). Inhibition of cellular proliferation by antisense oligodeoxynucleotides to PCNA cyclin. Science, 240, 1544-6. https://doi.org/10.1126/science.2897717
  30. Jemal A, Siegel R, Xu J, Ward E (2010). Cancer statistics. CA Cancer J Clin, 60, 277-300. https://doi.org/10.3322/caac.20073
  31. Janne PA, Mayer RJ (2000). Chemoprevention of colorectal cancer. Engl J Med, 42, 1960-8.
  32. Jenkins DC, Charles IG, Thomsen LL, et al (1995). Roles of nitric oxide in tumor growth. Proc Natl Acad Sci USA, 92, 4392-6. https://doi.org/10.1073/pnas.92.10.4392
  33. Jollow DJ, Mitchell JR, Zampaglione N, et al (1974). Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology, 11, 151-69. https://doi.org/10.1159/000136485
  34. Kang NJ, Jung SK, Lee KW, et al (2011). Myricetin is a potent chemopreventive phytochemical in skin carcinogenesis. Ann NY Acad Sci, 1229, 124-32. https://doi.org/10.1111/j.1749-6632.2011.06122.x
  35. Kawanishi S, Yamamoto K (1991). Mechanism of site-specific DNA damage induced by methylhydrazines in the presence of copper (II) or manganese (III). Biochemistry, 30, 3069-75. https://doi.org/10.1021/bi00226a013
  36. Kelman Z, Zuo S, Arroyo MP, et al (1999). The C-terminal region of Schizosaccaromyces pombe proliferating cell nuclear antigen is essential for DNA polymerase activity. Proc Natl Acad Sci USA, 96, 9515-20. https://doi.org/10.1073/pnas.96.17.9515
  37. Khan R, Khan AQ, Qamar W, et al (2012). Chrysin protects against cisplatin-induced colon. toxicity via amelioration of oxidative stress and apoptosis: probable role of p38MAPK and p53. Toxicol Appl Pharmacol, 258, 315-29. https://doi.org/10.1016/j.taap.2011.11.013
  38. Khan R, Sultana S (2011). Farnesol attenuates 1,2-dimethylhydrazine induced oxidative stress, inflammation and apoptotic responses in the colon of Wistar rats. Chem Biol Interact, 192, 193-200. https://doi.org/10.1016/j.cbi.2011.03.009
  39. Larsson SC, Rafter J, Holmberg L, et al (2005). Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: the Swedish Mammography Cohort. Int J Cancer, 113, 829-34. https://doi.org/10.1002/ijc.20658
  40. Lee SJ, Lim KT (2007). Inhibitory effect of phytoglycoprotein on tumor necrosis factor alpha and interleukin-6 at initiation stage of colon cancer in 1, 2-dimethylhydrazine-treated ICR mice. Toxicol Appl Pharmacol, 225, 198-205. https://doi.org/10.1016/j.taap.2007.07.010
  41. Lowry OH, Rosebroug NJ, Farr AL, et al (1951). Protein measurement with the Folin phenol reagent. J Biol Chem, 193, 265-75.
  42. Marklund S, Marklund G (1974). Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem, 47, 469-74. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  43. Mohan S, Epstein JB (2003). Carcinogenesis and cyclooxygenase: the potential role of COX-2 inhibition in upper aerodigestive tract cancer. Oral Oncol, 39, 537-46. https://doi.org/10.1016/S1368-8375(03)00035-6
  44. Mohandas J, Marshall JJ, Duggin GG, et al (1984). Differential distribution of glutathione and glutathione-related enzymes in rabbit kidney. Possible implications in analgesic nephropathy. Biochem Pharmacol, 33, 1801-7. https://doi.org/10.1016/0006-2952(84)90353-8
  45. Nagendraprabhu P, Sudhandiran G (2011). Astaxanthin inhibits tumor invasion by decreasing extracellular matrix production and induces apoptosis in experimental rat colon carcinogenesis by modulating the expressions of ERK-2, NFkB and COX-2. Invest New Drugs, 29, 207-24. https://doi.org/10.1007/s10637-009-9342-5
  46. Nakamura Y, Kaihara A, Yashii K, et al (2001). Effects of the oral administration of green tea polyphenol and tannic acid on serum and hepatic lipid contents and fecal steroid excretion in rats. J Hlth Sci, 47, 107-17.
  47. Nandhakumar R, Salini K, Niranjali Devaraj S (2012). Morin augments anticarcinogenic and antiproliferative efficacy against 7,12-dimethylbenz(a)-anthracene induced experimental mammary carcinogenesis. Mol Cell Biochem, 364, 79-92. https://doi.org/10.1007/s11010-011-1207-5
  48. Nepka C, Sivridis E, Antonoglou O, et al (1999). Chemopreventive activity of very low dose dietary tannic acid administration in hepatoma bearing C3H male mice. Cancer Lett, 141, 57-62. https://doi.org/10.1016/S0304-3835(99)00145-7
  49. Newell LE, Heddle JA (2004). The potent colon carcinogen, 1,2-dimethylhydrazine induces mutations primarily in the colon. Mutat Res, 564, 1-7. https://doi.org/10.1016/j.mrgentox.2004.06.005
  50. Norat T, Bingham S, Ferrari P, et al (2005). Meat, fish, and colorectal cancer risk: the Eurepean prospective investigation into cancer and nutrition. J Natl Cancer Inst, 97, 906-16. https://doi.org/10.1093/jnci/dji164
  51. Ohkawa H, Ohishi N, Yagi K (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 95, 351-8. https://doi.org/10.1016/0003-2697(79)90738-3
  52. Rajamanickam S, Agarwal R (2008). Natural products and colon cancer: current status and future prospects. Drug Development Res, 69, 460-471. https://doi.org/10.1002/ddr.20276
  53. Rajeshkumar NV, Kuttan R (2003). Modulation of carcinogenic response and antioxidant enzymes of rats administered with 1,2-dimethylhydrazine by Picroliv. Cancer Lett, 191, 137-43. https://doi.org/10.1016/S0304-3835(02)00203-3
  54. Rao CV, Kawamori T, Hamid R, et al (1999). Chemoprevention of colonic aberrant crypt foci by an inducible nitric oxide synthase-selective inhibitor. Carcinogenesis, 20, 641-4. https://doi.org/10.1093/carcin/20.4.641
  55. Rehman M U, Sultana S (2011). Attenuation of oxidative stress, inflammation and early markers of tumor promotion by caffeic acid in Fe-NTA exposed kidneys of Wistar rats. Mol Cell Biochem, 357, 115-24. https://doi.org/10.1007/s11010-011-0881-7
  56. Saini MK, Sharma P, Kaur J, et al (2009). The cyclooxygenase-2 inhibitor etoricoxib is a potent chemopreventive agent of colon carcinogenesis in the rat model. J Environ Pathol Toxicol Oncol, 28, 39-46. https://doi.org/10.1615/JEnvironPatholToxicolOncol.v28.i1.40
  57. Samanta S, Swamy V, Suresh D, et al (2008). Protective effects of vanadium against DMH-induced genotoxicity and carcinogenesis in rat colon: removal of O(6)-methylguanine DNA adducts, p53 expression, inducible nitric oxide synthase downregulation and apoptotic induction. Mutat Res, 650, 123-31. https://doi.org/10.1016/j.mrgentox.2007.11.001
  58. Sano H, Kawahito Y, Wilder RL, et al (1995). Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Res, 55, 3785-9.
  59. Taketo MM (1998). COX-2 and colon cancer. Inflamm Res, 47, 112-6. https://doi.org/10.1007/s000110050295
  60. Sehrawat A, Khan TH, Prasad L, et al (2006). Butea monosperma and chemomodulation: protective role against thioacetamidemediated hepatic alterations in Wistar rats. Phytomedicine, 13, 157-63. https://doi.org/10.1016/j.phymed.2004.11.007
  61. Sengottuvelan M, Senthilkumar R, Nalini N (2006). Modulatory influence of dietary resveratrol during different phases of 1, 2-dimethylhydrazine induced mucosal lipid-peroxidation, antioxidant status and aberrant crypt foci development in rat colon carcinogenesis. Biochim Biophys Acta, 1760, 1175-83. https://doi.org/10.1016/j.bbagen.2006.03.008
  62. Stoner GD, Mukhtar H (1995). Polyphenols as cancer chemopreventive agents. J Cell Biochem, 22, 169-80.
  63. Tsujii M, Kawano S, Tsuji S, et al (1998). Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell, 93, 705-16. https://doi.org/10.1016/S0092-8674(00)81433-6
  64. Umesalma S, Sudhandiran G (2010). Differential inhibitory effects of the polyphenol ellagic acid on inflammatory mediators NF-jB, iNOS, COX-2, TNF-a, and IL-6 in 1,2-dimethylhydrazine-induced rat colon carcinogenesis. J Compilation Nordic Pharmacological Society. Basic & Clinical Pharmacology & Toxicology, 107, 650-65. https://doi.org/10.1111/j.1742-7843.2010.00565.x
  65. Umesalma S, Sudhandiran G, (2010). Differential inhibitory effects of the polyphenol ellagic acid on inflammatory mediators NF-kappaB, iNOS, COX-2, TNF-alpha, and IL-6 in 1,2-dimethylhydrazine-induced rat colon carcinogenesis. Basic Clin Pharmacol Toxicol, 107, 650-5. https://doi.org/10.1111/j.1742-7843.2010.00565.x
  66. van Grevenstein WM, Hofland LJ, Jeekel J, et al., (2006). The expression of adhesion molecule and the influence of inflammatory cytokines on the adhesion of human pancreatic carcinoma cells to mesothelial monolayers. Pancreas, 32, 396-402. https://doi.org/10.1097/01.mpa.0000220865.80034.2a
  67. Williams CS, Mann M, DuBois RN, (1999). The role of cyclooxygenases in inflammation, cancer, and development. Oncogene, 18, 7908-16.

Cited by

  1. Dietary Non-nutritive Factors in Targeting of Regulatory Molecules in Colorectal Cancer: An Update vol.14, pp.10, 2013, https://doi.org/10.7314/APJCP.2013.14.10.5543
  2. Chemopreventive Effect of Amorphophallus campanulatus (Roxb.) blume tuber against aberrant crypt foci and cell proliferation in 1, 2-dimethylhydrazine induced colon carcinogenesis vol.14, pp.9, 2013, https://doi.org/10.7314/APJCP.2013.14.9.5331
  3. Luteolin, a Bioflavonoid Inhibits Colorectal Cancer through Modulation of Multiple Signaling Pathways: A Review vol.15, pp.14, 2014, https://doi.org/10.7314/APJCP.2014.15.14.5501
  4. Chemopreventive effects of aloin against 1,2-dimethylhydrazine-induced preneoplastic lesions in the colon of Wistar rats vol.33, pp.2, 2014, https://doi.org/10.1177/0960327113493307
  5. Possible Protective Effects of Quercetin and Sodium Gluconate Against Colon Cancer Induction by Dimethylhydrazine in Mice vol.16, pp.14, 2015, https://doi.org/10.7314/APJCP.2015.16.14.5823
  6. Dietary Ziziphus jujuba Fruit Influence on Aberrant Crypt Formation and Blood Cells in Colitis-Associated Colorectal Cancer Mice vol.16, pp.17, 2015, https://doi.org/10.7314/APJCP.2015.16.17.7561
  7. Anti-proliferative and Apoptotic Effects of Basella rubra (L.) Against 1, 2-Dimethyl Hydrazine-induced Colon Carcinogenesis in Rats vol.17, pp.1, 2016, https://doi.org/10.7314/APJCP.2016.17.1.73
  8. Radioprotection of 1,2-dimethylhydrazine-initiated colon cancer in rats using low-dose γ rays by modulating multidrug resistance-1, cytokeratin 20, and β-catenin expression vol.35, pp.3, 2016, https://doi.org/10.1177/0960327115584687
  9. Co-treatment with sulforaphane–zein microparticles enhances the chemopreventive potential of zinc in a 1,2-dimethylhydrazine induced colon carcinogenesis rat model vol.6, pp.41, 2016, https://doi.org/10.1039/C6RA02355J
  10. Targeted multifunctional tannic acid nanoparticles vol.6, pp.9, 2016, https://doi.org/10.1039/C5RA19405A
  11. Protective Effect of Metformin against Acute Inflammation and Oxidative Stress in Rat vol.77, pp.6, 2016, https://doi.org/10.1002/ddr.21322
  12. Sphingosine-1-Phosphate Metabolism and Its Role in the Development of Inflammatory Bowel Disease vol.18, pp.4, 2017, https://doi.org/10.3390/ijms18040741
  13. leaves methanol extract against the azoxymethane-induced colon cancer in rats involved modulation of the colonic antioxidant system partly by flavonoids vol.55, pp.1, 2017, https://doi.org/10.1080/13880209.2017.1371769
  14. Effect of roxithromycin on mucosal damage, oxidative stress and pro-inflammatory markers in experimental model of colitis pp.1420-908X, 2017, https://doi.org/10.1007/s00011-017-1103-x
  15. Tannic acid directly targets pyruvate kinase isoenzyme M2 to attenuate colon cancer cell proliferation pp.2042-650X, 2018, https://doi.org/10.1039/C8FO01161C
  16. Selenium-Enriched Saccharomyces cerevisiae Reduces the Progression of Colorectal Cancer vol.185, pp.2, 2018, https://doi.org/10.1007/s12011-018-1270-9
  17. Chemopreventive efficacy zingerone (4‐[4‐hydroxy‐3‐methylphenyl] butan‐2‐one) in experimental colon carcinogenesis in Wistar rats pp.1522-7278, 2019, https://doi.org/10.1002/tox.22727