Asian Pacific Journal of Cancer Prevention

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

DOI QR Code

Dietary Non-nutritive Factors in Targeting of Regulatory Molecules in Colorectal Cancer: An Update

  • Pandurangan, Ashok Kumar (Department of Nutrition and Dietetics, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia) ;
  • Esa, Norhaizan Mohd (Department of Nutrition and Dietetics, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia)
  • Published : 2013.10.30
Download PDF
⟨ Previous Next ⟩

Abstract

Colorectal cancer (CRC), a complex multi-step process involving progressive disruption of homeostatic mechanisms controlling intestinal epithelial proliferation/inflammation, differentiation, and programmed cell death, is the third most common malignant neoplasm worldwide. A number of promising targets such as inducible nitric acid (iNOS), cyclooxygenase (COX)-2, NF-E2-related factor 2 (Nrf2), $Wnt/{\beta}$-catenin, Notch and apoptotic signaling have been identified by researchers as useful targets to prevent or therapeutically inhibit colon cancer development. In this review article, we aimed to explore the current targets available to eliminate colon cancer with an update of dietary and non-nutritional compounds that could be of potential use for interaction with regulatory molecules to prevent CRC.

Keywords

References

  1. Abbas T, Dutta A (2009). p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer, 9, 400-14. https://doi.org/10.1038/nrc2657
  2. Aberle H, Bauer A, Stappert J, et al (1997). ${\beta}$-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J, 16, 3797-804. https://doi.org/10.1093/emboj/16.13.3797
  3. Albring KF, Weidemuller J, Mittag S, et al (2013). Berberine acts as a natural inhibitor of Wnt/${\beta}$-catenin signaling-Identification of more active 13-arylalkyl derivatives. Biofactors, [Epub ahead of print].
  4. Allameh A, Dadkhah A, Rahbarizadeh F, et al (2012). Effect of dietary caraway essential oils on expression of ${\beta}$-catenin during 1, 2-dimethylhydrazine-induced colonic carcinogenesis. J Nat Med, 67, 690-7.
  5. Ambs S, Merriam WG, Bennett WP, et al (1998). Frequent nitric oxide synthase-2 expression in human colon adenomas: Implication for tumor angiogenesis and colon cancer progression. Cancer Res, 58, 334-41.
  6. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999). Notch signaling: cell fate control and signal integration in development. Science, 284, 770-6. https://doi.org/10.1126/science.284.5415.770
  7. Arulselvan P, Wen CC, Lan CW, et al (2012). Dietary administration od scallion extract effectively inhibits colorectal tumor growth: cellular and molecular mechanisms in mice. PLoS One, 7, 44658. https://doi.org/10.1371/journal.pone.0044658
  8. Ashokkumar P, Sudhandiran G (2008). Protective role of Luteolin on the status of lipid peroxidation and antioxidant defense against Azoxymethane-induced experimental colon carcinogenesis. Biomed Pharmacother, 62, 590-7. https://doi.org/10.1016/j.biopha.2008.06.031
  9. Ashokkumar P, Sudhandiran G (2011). Luteolin inhibits cell proliferation during Azoxymethane-induced experimental colon carcinogenesis via Wnt/${\beta}$-catenin pathway. Invest New Drugs, 29, 273-84. https://doi.org/10.1007/s10637-009-9359-9
  10. Baron M (2003). An overview of the notch signalling pathway. Semin Cell DevBiol, 14, 113-9. https://doi.org/10.1016/S1084-9521(02)00179-9
  11. Bat-Chen W, Golan T, Peri I, et al (2010). Allicin purified from fresh garlic cloves induces apoptosis in colon cancer cells via Nrf2. Nutr Cancer, 62, 947-57. https://doi.org/10.1080/01635581.2010.509837
  12. Behrens J, Kries JV, Kuhl M, et al (1996). Functional interaction of ${\beta}$-catenin with the transcription factor LEF-1. Nature, 382, 638-42. https://doi.org/10.1038/382638a0
  13. Burnstein MJ (1993). Dietary factors related to colorectal neoplasms. Surg Clin North America, 73, 13-29.
  14. Chan JY, Kwong M (2000). Impaired expression of glutathione synthetic enzyme genes in mice with targeted deletion of the Nrf2 basic-leucine zipper protein. Biochim Biophys Acta, 1517, 19-26. https://doi.org/10.1016/S0167-4781(00)00238-4
  15. Chen X, Johns DC, Geiman DE, et al (2001). Kruppel-like factor 4 (gut-enriched Kruppel-like factor)inhibits cell proliferation by blocking G1/S progression of the cell cycle. J Biol Chem, 276, 30423-8. https://doi.org/10.1074/jbc.M101194200
  16. Chidambara Murthy KN, Jayaprakasha GK, Patil BS (2012). The natural alkaloid berberine targets multiple pathways to induce cell death in cultured human colon cancer cells. Eur J Pharmacol, 688, 14-21. https://doi.org/10.1016/j.ejphar.2012.05.004
  17. Chiou YS, Ma NJ, Sang S, et al (2012).Peracetylated (-)-epigallocatechin-3-gallate (AcEGCG) potently suppresses dextran sulfate sodium-induced colitis and colon tumorigenesis in mice. J Agric Food Chem, 60, 3441-51. https://doi.org/10.1021/jf300441p
  18. Chiou YS, Tsai ML, Nagabhushanam K, et al (2011). Pterostilbene is more potent than resveratrol in preventing azoxymethane (AOM)-induced colon tumorigenesis via activation of the NF-E2-related factor 2 (Nrf2)-mediated antioxidant signaling pathway. J Agric Food Chem, 59, 2725-33. https://doi.org/10.1021/jf2000103
  19. Church RD, Fleshman JW, McLeod HL (2003). Cyclooxygenase 2 inhibition in colorectal cancer therapy. Br J Surg, 90, 1055-7. https://doi.org/10.1002/bjs.4297
  20. Cianchi F, Cortesini C, Fantappie O, Messerini L (2003). Inducible nitric oxide synthase expression in human colorectal cancer. Am J Pathol, 162, 793. https://doi.org/10.1016/S0002-9440(10)63876-X
  21. Cordero-Herrera I, Martin MA, Bravo L, et al (2013). EpicatechinGallate induces cell death via p53 activation and stimulation of p38 and JNK in human colon cancer SW480 Cells. Nutr Cancer, 65, 718-28. https://doi.org/10.1080/01635581.2013.795981
  22. Dang DT, Pevsner J, Yang VW (2000). The biology of the mammalian Kruppel-like family of transcription factors. Int J Biochem Cell Biol, 32, 1103-21. https://doi.org/10.1016/S1357-2725(00)00059-5
  23. Dashwood RH, Suzui M, Nakagama H, et al (1998). High frequency of ${\beta}$-catenin (Ctnnb1) mutations in the colon tumors induced by two heterocyclic amines in the F344 rats. Cancer Res, 58, 1127-9.
  24. Dempke W, Rie C, Grothey A, Schmoll HJ (2001). Cyclooxygenase-2: a novel target for cancer chemotherapy? J Cancer Res Clin Oncol, 127, 411-7. https://doi.org/10.1007/s004320000225
  25. Derry MM, Raina K, Balaiya V, et al (2013). Grape seed extract efficacy against azoxymethane-induced colon tumorigenesis in A/J mice: interlinking miRNA with cytokine signaling and inflammation. Cancer Prev Res (Phila), 6, 625-33. https://doi.org/10.1158/1940-6207.CAPR-13-0053
  26. Dinkova-Kostova AT, Holtzclaw WD, Kensler TW (2005).The role of keap1 in cellular protective responses. Chem Res Toxicol, 18, 1779-91. https://doi.org/10.1021/tx050217c
  27. Festjens N, van Gurp M, van Loo G, et al (2004). Bcl- 2 family members as sentinels of cellular integrity and role of mitochondrial intermembrane space proteins in apoptotic cell death. Acta Haematol, 111, 7-27. https://doi.org/10.1159/000074483
  28. Fiala ES, Sohn OS, Hamilton SR (1987).Effects of chronic dietary ethanol on the in vivo and in vitro metabolism of methylazoxymethanol and methylazoxymethanol-induced DNA methylation in the rat colon and liver. Cancer Res, 47, 5939-43.
  29. Forrester K, Ambs S, Lupold E, et al (1996). Nitric oxide induced p53 accumulation and regulation of iNOS expression by wild type p53. Proc Natl Acad Sci USA, 93, 2441-7.
  30. Furukawa M, Xiong Y (2005). BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase. Mol Cell Biol, 25, 162-71. https://doi.org/10.1128/MCB.25.1.162-171.2005
  31. Ghaleb AM, Aggarwal G, Bialkoska AB, et al (2008). Notch inhibits expression of the Kruppel-like factor 4 tumor suppressor in the intestinal epithelium. Mol Cancer Res, 6, 1920-7. https://doi.org/10.1158/1541-7786.MCR-08-0224
  32. Ghaleb AM, McConnell BB, Nandan MO, et al (2007). Haploinsufficiency of Kruppel-like factor 4 promotes adenomatous polyposis coli dependent intestinal tumorigenesis. Cancer Res, 67, 7147-54. https://doi.org/10.1158/0008-5472.CAN-07-1302
  33. Giovannucci E, Egan KM, Hunter DJ, et al (1995). Aspirin and the risk of colorectal cancer in women. N Engl J Med, 333, 609-14. https://doi.org/10.1056/NEJM199509073331001
  34. Gosslau A, En Jao DL, Huang MT, et al (2011). Effects of the black tea polyphenol theaflavin-2 on apoptotic and inflammatory pathways in vitro and in vivo. Mol Nutr Food Res, 55, 198-208. https://doi.org/10.1002/mnfr.201000165
  35. Greenlee R, Bolden SM, Wingo PA (2000). Cancer statistics 2000. CA Cancer J Clin, 50, 7-33. https://doi.org/10.3322/canjclin.50.1.7
  36. Gregorieff A, Clevers H (2005). Wnt signaling in the intestinal epithelium: from endoderm to cancer. Gene Dev, 19, 877-90. https://doi.org/10.1101/gad.1295405
  37. Ha TK, Kim ME, Yoon JH, et al (2013). Galangin induces human colon cancer cell death via the mitochondrial dysfunction and caspase-dependent pathway. Exp Biol Med (Maywood), 238, 1047-54. https://doi.org/10.1177/1535370213497882
  38. Hamiza OO, Rehman MU, Tahir M, et al (2012). Amelioration of 1,2 Dimethylhydrazine (DMH) induced colon oxidative stress, inflammation and tumor promotion response by tannic acid in Wistar rats. Asian Pac J Cancer Prev, 13, 4393-402. https://doi.org/10.7314/APJCP.2012.13.9.4393
  39. Hanif R, Pittas A, Feng Y, et al (1996). Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem Pharmacol, 52, 237-45. https://doi.org/10.1016/0006-2952(96)00181-5
  40. Harun Z, Ghazali AR (2012).Potential chemoprevention activity of Pterostilbene by enhancing the detoxifying enzymes in the HT-29 Cell Line. Asian Pac J Cancer Prev, 13, 6403-7. https://doi.org/10.7314/APJCP.2012.13.12.6403
  41. He TC, Sparks AB, Rago C, et al (1998). Identification of c-MYC as a target of the APC pathway. Science, 281, 1509-12. https://doi.org/10.1126/science.281.5382.1509
  42. Hockenbery DM, Zutter M, Hicky W, et al (1991). Bcl2 protein is topographically restricted in tissues characterized by apoptotic cells death. Proc Natl Acad Sci USA, 88, 6961-5. https://doi.org/10.1073/pnas.88.16.6961
  43. Hu R, Chen N, Yao J, et al (2012). The role of Nrf2 and apoptotic signaling pathways in oroxylin A-mediated responses in HCT-116 colorectal adenocarcinoma cells and xenograft tumors. Anticancer Drugs, 23, 651-8. https://doi.org/10.1097/CAD.0b013e3283512703
  44. Huang DS, Shen KZ, Wei JF, et al (2005). Specific COX-2 inhibitor NS398 induces apoptosis in human liver cancer cell line HepG2 through BCL-2. World J Gastroenterol, 11, 204-7. https://doi.org/10.3748/wjg.v11.i2.204
  45. Iso T, Kedes L, Hamamori Y (2003). HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol, 194, 237-55. https://doi.org/10.1002/jcp.10208
  46. Kam PCA, See AUL (2000). Cyclo-oxygenaseisoenzymes: physiological and pharmacological role. Anaesthesia, 55, 442-9. https://doi.org/10.1046/j.1365-2044.2000.01271.x
  47. Kang YJ, Park HJ, Chung HJ, et al (2012). Wnt/${\beta}$-catenin signaling mediates the antitumor activity of magnolol in colorectal cancer cells. Mol Pharmacol, 82,168-77. https://doi.org/10.1124/mol.112.078535
  48. Katoh M, Katoh M (2007). Notch signaling in gastrointestinal tract (review). Int J Oncol, 30, 247-51.
  49. Kauntz H, Bousserouel S, Gosse F, et al (2012). Silibinin, a natural flavonoid, modulates the early expression of chemoprevention biomarkers in a preclinical model of colon carcinogenesis. Int J Oncol, 41, 849-54.
  50. Khan R, Khan AQ, Lateef A, et al (2013). Glycyrrhizic acid suppresses the development of precancerous lesions via regulating the hyperproliferation, inflammation, angiogenesis and apoptosis inthe colon of Wistar rats. PLoS One, 8, 56020. https://doi.org/10.1371/journal.pone.0056020
  51. Kim AD, Kang KA, Kim HS, et al (2013). A ginseng metabolite, compound K, induces autophagy and apoptosis via generation of reactive oxygen species and activation of JNK in human colon cancer cells. Cell Death Dis, 4, 750. https://doi.org/10.1038/cddis.2013.273
  52. Kim HS, Wannatung T, Lee S, et al (2012). Quercetin enhances hypoxia-mediated apoptosis via direct inhibition of AMPK activity in HCT116 colon cancer. Apoptosis, 17, 938-49. https://doi.org/10.1007/s10495-012-0719-0
  53. Kim SP, Kang MY, Nam SH, et al (2012a). Dietary rice bran component ${\gamma}$-oryzanol inhibits tumor growth in tumor-bearing mice. Mol Nutr Food Res, 56, 935-44. https://doi.org/10.1002/mnfr.201200057
  54. Kobayashi M, Yamamoto M (2005). Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal, 7, 385-94. https://doi.org/10.1089/ars.2005.7.385
  55. Koduru S, Kumar R, Srinivasan S, et al (2010). Notch-1 inhibition by Withaferin-A: a therapeutic target against colon carcinogenesis. Mol Cancer Ther, 9, 202-10.
  56. Korinek V, Barker N, Morin PJ, et al (1997). Constitutive transcriptional activation by a ${\beta}$-catenin-Tcf complex in APC-/- colon carcinoma. Science, 275, 1784-7. https://doi.org/10.1126/science.275.5307.1784
  57. Kroemer G, El-Deiry WS, Golstein P, et al (2005). Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ, 12, 1463-67. https://doi.org/10.1038/sj.cdd.4401724
  58. Kubota M, Shimizu M, Sakai H, et al (2012).Preventive effects of curcumin on the development of azoxymethane-induced colonic preneoplastic lesions in male C57BL/KsJ-db/db obese mice. Nutr Cancer, 64, 72-9. https://doi.org/10.1080/01635581.2012.630554
  59. Kumar A, Pandurangan AK, Lu F, et al (2012). Chemo preventive sphingadienes down regulate wnt signaling via a PP2A/Akt/GSK3${\beta}$ pathway in colon cancer. Carcinogenesis, 33, 1726-35. https://doi.org/10.1093/carcin/bgs174
  60. Lala PK, Chekraborty C (2001). Role of nitric oxide in carcinogenesis and tumor progression. Lancet Oncol, 3, 149-52.
  61. Lee JS, Surh YJ (2005). Nrf2 as a novel molecular target for chemoprevention. Cancer Lett, 224, 171-84. https://doi.org/10.1016/j.canlet.2004.09.042
  62. Lee MA, Park HJ, Chung HJ, et al (2013). Antitumor activity of 2-Hydroxycinnamaldehyde for human colon cancer cells through suppression of ${\beta}$-catenin signaling. J Nat Prod, 76, 1278-84. https://doi.org/10.1021/np400216m
  63. Li P, Nijhawan D, Budihardjo I, et al (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell, 91, 479-89. https://doi.org/10.1016/S0092-8674(00)80434-1
  64. Li X, Pu J, Jiang S, et al (2013). Henryin, an ent-kauranediterpenoid, inhibits Wnt signaling through interference with ${\beta}$-catenin/TCF4 interaction in colorectal cancer cells. PLoS One, 8, 68525. https://doi.org/10.1371/journal.pone.0068525
  65. Liu X, Kim CM, Yang J, et al (1996). Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86, 147-57. https://doi.org/10.1016/S0092-8674(00)80085-9
  66. McDonnel TJ (1993). Cell division versus cell death: a functional model of multistep neoplasia. Mol Carcinogenesis, 8, 209-13. https://doi.org/10.1002/mc.2940080402
  67. Middleton SJ, Shorthouse MJ, Hunter JO (1993). Increased nitric oxide synthesis in ulcerative colitis. Lancet, 341, 465. https://doi.org/10.1016/0140-6736(93)90211-X
  68. Miyamoto S, Nakanishi M, Rosenberg DW (2013). Suppression of colon carcinogenesis by targeting Notch signaling. Carcinogenesis, 34, 2415-23. https://doi.org/10.1093/carcin/bgt191
  69. Molenaar M, Wetering MVD, Oosterwegel M, et al (1996). XTcf-3 transcription factor mediates ${\beta}$-catenin-induced axis formation in Xenopus embryos. Cell, 86, 391-9. https://doi.org/10.1016/S0092-8674(00)80112-9
  70. Morin PJ, Sparks AB, Korinek V, et al (1997). Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science, 275, 1787-90. https://doi.org/10.1126/science.275.5307.1787
  71. Murad F (1996). The Albert Lasker Medical Research Awards. Signal transduction using nitric oxide and cyclic guanosine monophosphate. JAMA, 276, 1189-92. https://doi.org/10.1001/jama.1996.03540140077033
  72. Nalini N, Aranganathan S, Kabalimurthy J (2012). Chemopreventive efficacy of hesperetin (citrus flavonone) against 1,2-dimethylhydrazine-induced rat colon carcinogenesis. Toxicol Mech Methods, 22, 397-408. https://doi.org/10.3109/15376516.2012.673092
  73. Newmeyer DD, Farschon DM, Reed JC (1994). Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell, 79, 353-64. https://doi.org/10.1016/0092-8674(94)90203-8
  74. Norazalina S, Mohd.-Esa N, Hairuszah I, Norashareena MS (2010). Anticarcinogenic efficacy of phytic acid extracted from rice bran on azoxymethane-induced colon carcinogenesis in rats. Exp Toxicol Pathol, 62, 259-68. https://doi.org/10.1016/j.etp.2009.04.002
  75. Nurul-Husna S, Norhaizan ME, Abdah MA, et al (2010). Rice bran phytic acid (IP6) induces growth inhibition, cell cycle arrest and apoptosis on human colorectal adenocarcinoma cells. J Med Plants Res, 4, 2283-9.
  76. Osburn W, Wakabayashi N, Misra V, et al (2006). Nrf2 regulates an adaptive response protecting against oxidative damage following diquat-mediated formation of superoxide anion. Arch Biochem Biophys, 454, 7-15. https://doi.org/10.1016/j.abb.2006.08.005
  77. Panaro MA, Carofiglio V, Acquafredda A, et al (2012). Anti-inflammatory effects of resveratrol occur via inhibition of lipopolysaccharide-induced NF-${\kappa}B$ activation in Caco-2 and SW480 human coloncancer cells. Br J Nutr, 108, 1623-32. https://doi.org/10.1017/S0007114511007227
  78. Pandurangan AK (2013). Potential targets for the prevention of colorectal cancer: A focus on PI3K/Akt/mTOR and Wnt pathways. Asian Pac J Cancer Prev, 14, 2201-5. https://doi.org/10.7314/APJCP.2013.14.4.2201
  79. Pandurangan AK, AnandaSadagopan SK, Dharmalingam P, et al (2013). Inhibitory effect of Luteolin on Azoxymethane-induced colon carcinogenesis: Involvement of iNOS and COX-2. Pharmacog Magazine, [Epub ahead of print].
  80. Pandurangan AK, AnandaSadagopan SK, Dharmalingam P, et al (2013b). Luteolin, a bioflavonoid inhibits Azoxymethane-induced colorectal cancer through Nrf2 signaling. Toxicol Mech Methods, [Epub ahead of print].
  81. Pandurangan AK, Dharmalingam P, AnandaSadagopan SK, et al (2013c). Luteolin induces growth arrest in colon cancer cells through involvement of Wnt/${\beta}$-catenin/GSK-$3{\beta}$ signaling. J Environ Pathol Toxicol Oncol, 32, 131-9. https://doi.org/10.1615/JEnvironPatholToxicolOncol.2013007522
  82. Pandurangan AK, Ganapasam S (2013). Luteolin modulates cellular thiols on Azoxymenthane-induced colon carcinogenesis. Asian J Exp Bio lSci, 4, 245-50.
  83. Pandurangan AK, Ganapsam S (2013). Luteolin induces apoptosis in azoxymethane-induced colon carcinogenesis through involvement of Bcl-2, Bax, and Caspase-3. J Chem Pharm Res, 5, 143-8.
  84. Pandurangan AK, Dharmalingam P, Anandasadagopan SK, et al (2013). Inhibitory effect of Luteolin on the status of membrane bound ATPases against Azoxymethane-induced colorectal cancer. J Chem Pharm Res, 5, 123-7.
  85. Pandurangan AK,Dharmalingam P, Anandasadagopan SK, Ganapasam S (2012). Effect of Luteolin on the levels of Glycoproteins during Azoxymethane-induced colon carcinogenesis in mice. Asian Pac J Cancer Prev, 13, 1569-73. https://doi.org/10.7314/APJCP.2012.13.4.1569
  86. Park S, Gwak J, Han SJ, Oh S (2013).Cardamonin suppresses the proliferation of colon cancer cells by promoting ${\beta}$-catenin degradation. Biol Pharm Bull, 36, 1040-4. https://doi.org/10.1248/bpb.b13-00158
  87. Patel R, Ingle A, Maru GB (2008). Polymeric black tea polyphenols inhibit 1, 2-dimethylhydrazine induced carcinogenesis by inhibiting cell proliferation via Wnt/${\beta}$-catenin pathway. Toxicol Appl Pharmacol, 227, 136-46. https://doi.org/10.1016/j.taap.2007.10.009
  88. Polakis P (1997). The adenomatous polyposis coli (APC) tumor suppressor. Biochim Biophys Acta, 1332, 127-47.
  89. Powell S, Zilz N, Beazer-Barclay Y, et al (1992). APC mutations occur early during colorectal tumorigenesis. Nature, 359, 235-7. https://doi.org/10.1038/359235a0
  90. Prabhu PN, Ashokkumar P, Sudhandiran G (2009). Antioxidative and antiproliferative effects of astaxanthin during the initiation stages of 1,2-dimethyl hydrazine-induced experimental colon carcinogenesis. Fundam Clin Pharmacol, 23, 225-34. https://doi.org/10.1111/j.1472-8206.2009.00669.x
  91. Puangpraphant S, Dia VP, de Mejia EG, et al (2013). Yerba mate tea and mate saponins prevented azoxymethane-induced inflammation of rat colon through suppression of NF-${\kappa}B$ p65ser(311) signaling via $I{\kappa}B-{\alpha}$ and GSK-$3{\beta}$ reduced phosphorylation. Biofactors, 39, 430-40. https://doi.org/10.1002/biof.1083
  92. Rao CV, Kawamori T, Hamid R, et al (1998). Chemoprevention of colon cancer by iNOS specific and non-specific inhibitors: a safer colon cancer chemopreventive strategy. Proc Am Assoc Cancer Res, 39, 197.
  93. Rao CV, Reddy BS (2004). NASIDs and chemoprevention. Curr Cancer Drug Targets, 4, 29-43. https://doi.org/10.2174/1568009043481632
  94. Reddy BS(2004). Studies with the azoxymethane-rat preclinical model for assessing colon tumor development and chemoprevention. Environ Mol Mutagen, 44, 26-35. https://doi.org/10.1002/em.20026
  95. Reddy BS, Hirose Y, Lubet R, et al (2000). Chemoprevention of colon cancer by specific cycloxygenase-2 inhibitor, celeoxib, administrated during different stages of carcinogenesis. Cancer Res, 60, 293-298.
  96. Reedijk M, Odorcic S, Zhang H, et al (2008). Activation of Notch signaling in human colon adenocarcinoma. Int J Oncol, 33, 1223-9.
  97. Saad N, Esa NM, Ithnin H (2013). Suppression of ${\beta}$-catenin and cyclooxygenase-2 on expression and cell proliferation in azoxymethane-induced colonic cancer in rats by rice bran phytic acid (PA). Asian Pac J Cancer Prev, 14, 3093-9. https://doi.org/10.7314/APJCP.2013.14.5.3093
  98. Sadik NA, Shaker OG (2013). Inhibitory effect of a standardized pomegranate fruit extract on Wnt signalling in 1, 2-dimethylhydrazine induced rat colon carcinogenesis. Dig Dis Sci, [Epub ahead of print].
  99. Saud SM, Young MR, Jones-Hall YL, et al (2013). Chemopreventive activity of plant flavonoid isorhamnetin in colorectal cancer is mediated by oncogenic Src and ${\beta}$-Catenin. Cancer Res, 73, 5473-84. https://doi.org/10.1158/0008-5472.CAN-13-0525
  100. Schmidt HH, Walter U (1994). NO at work. Cell, 78, 919-25. https://doi.org/10.1016/0092-8674(94)90267-4
  101. Shafie NH, MohdEsa NM, Ithnin H, et al (2013). Prophylactic Inositol Hexaphosphate (IP6) inhibits colon cancer through involvement of Wnt/${\beta}$-catenin and COX-2 pathway. BioMed Res Int, 2013, 10.
  102. Sheng H, Shao J, Morrow JD, et al (1998). Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells. Cancer Res, 58, 362-6.
  103. Shields JM, Christy RJ, Yang VW (1996). Identification and characterization of a gene encoding a gut-enriched Kruppellike factor expressed during growth arrest. J Biol Chem, 271, 20009-17. https://doi.org/10.1074/jbc.271.33.20009
  104. Shike M, Winawar SJ, Greenwald PH, et al (1990). Primary prevention of colorectal cancer: WHO collaborating center for prevention of colorectal cancer. Bull WHO, 68, 377-85.
  105. Sikandar SS, Pate KT, Anderson S, et al (2010). NOTCH signaling is required for formation and selfrenewal of tumor-initiating cells and for repression of secretory cell differentiation in colon cancer. Cancer Res, 70, 1469-78. https://doi.org/10.1158/0008-5472.CAN-09-2557
  106. Singh BN, Shankar S, Srivastava RK (2011). Green tea catechin, epigallocatechin-3-gallate (EGCG): Mechanisms, perspectives and clinical applications. Biochem Pharmacol, 82, 1807-21. https://doi.org/10.1016/j.bcp.2011.07.093
  107. Slattery ML, Edwards SL, Boucher KM, et al (1999). Life style and colon cancer: an assessment of factors associated with risk. Am J Epidemiol, 150, 869-77. https://doi.org/10.1093/oxfordjournals.aje.a010092
  108. Sohn OS, Ishizaki H, Yang CS, Fiala ES (1991). Metabolism of azoxymethane, methylazoxymethanol and N-nitrosodimethylamine by cytochrome P450IIE1. Carcinogenesis, 12, 127-31. https://doi.org/10.1093/carcin/12.1.127
  109. Sparks AB, Morin PJ, Vogelstein B, Kinzler KW (1998). Mutational analysis of the APC/${\beta}$-catenin/Tcf pathway in colorectal cancer. Cancer Res, 58, 1130-4.
  110. Srimuangwong K, Tocharus C, Tocharus J, et al (2012). Effects of hexahydrocurcumin in combination with 5-fluorouracil on dimethylhydrazine-induced colon cancer in rats. World J Gastroenterol, 18, 6951-9. https://doi.org/10.3748/wjg.v18.i47.6951
  111. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, et al (1998). Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell, 1, 949-57. https://doi.org/10.1016/S1097-2765(00)80095-7
  112. Sriram N, Kalayarasan S, Ashokkumar P, et al (2008). Diallyl sulfide induces apoptosis in Colo 320 DM human colon cancer cells: involvement of caspase-3, NF-${\kappa}B$, and ERK-2. Mol Cell Biochem, 311, 157-65. https://doi.org/10.1007/s11010-008-9706-8
  113. Subbaramiah K, Telang N, Ramonetti JT, et al (1996). Transcription of cyclooxygenase-2 is enhanced in transformed mammary epithelial cells. Cancer Res, 56, 4424-9.
  114. Suzui M, Ushijima T, Dashwood RH, et al (1999). Frequent mutations of the rat ${\beta}$-catenin gene in colon cancers induced by methylazoxymethanol acetate plus 1-hydroxyanthraquinone. Mol Carcinogenesis, 24, 232-7. https://doi.org/10.1002/(SICI)1098-2744(199903)24:3<232::AID-MC10>3.0.CO;2-M
  115. Takahashi M, Fukuda K, Ohata T, et al (1997). Increased expression of inducible and endothelial constitutive nitric oxide synthases in rat colon tumors induced by azoxymethane. Cancer Res, 57, 1233-7.
  116. Takahashi M, Fukuda K, Sugimura T, et al (1998). ${\beta}$-Catenin is frequently mutated and demonstrates altered cellular location in azoxymethane-induced rat colon tumors. Cancer Res, 58, 42-6.
  117. Talalay P (1992). Chemical protection against cancer by induction of electrophile detoxification (phase II) enzymes, Cellular and Molecular Targets for Chemoprevention, CRC Press, Boca Raton, FL.
  118. Tanwar L, Vaish V, Sanyal SN (2009). Chemoprevention of 1,2-Dimethylhydrazine-induced colon carcinogenesis by a Non-steroidal anti-inflammatory drug, etoricoxib, in rats: Inhibition of nuclear factor ${\kappa}B$. Asian Pac J Cancer Prev, 10, 1141-6.
  119. Tetsu O, McCormick F (1999). ${\beta}$-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature, 398, 422-6. https://doi.org/10.1038/18884
  120. Thun MJ, Namboodiri MM, Heath Jr CW (1991). Aspirin use and reduced risk of fatal colon cancer. N Engl J Med, 325, 1593-6. https://doi.org/10.1056/NEJM199112053252301
  121. Tsujii M, DuBois RN (1995). Alteration in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell, 83, 493-501. https://doi.org/10.1016/0092-8674(95)90127-2
  122. Turini ME, DuBois RN (2002). Cyclooxygenase-2: a therapeutic target. Annu Rev Med, 53, 35-57. https://doi.org/10.1146/annurev.med.53.082901.103952
  123. van Es JH, van Gijn ME, Riccio O, et al (2005). Notch/gammasecretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature, 435, 959-63. https://doi.org/10.1038/nature03659
  124. Wang J, Liu L, Qiu H, et al (2013). Ursolic acid simultaneously targets multiple signaling pathways to suppress proliferation and induce apoptosis in colon cancer cells. PLoS One, 8, 63872. https://doi.org/10.1371/journal.pone.0063872
  125. Wen CTP, Hussein SZ, Abdullah S, et al (2012). Gelam and Nenas honeys inhibit proliferation of HT 29 colon cancer cells by inducing DNA damage and apoptosis while suppressing inflammation. Asian Pac J Cancer Prev, 13, 6403-7. https://doi.org/10.7314/APJCP.2012.13.4.1605
  126. Wesolowska O, Wisniewski J, Sroda-Pomianek K, et al (2012). Multidrug Resistance Reversal and Apoptosis Induction in Human Colon Cancer Cells by Some Flavonoids Present in Citrus Plants. J Nat Prod, [Epub ahead of print].
  127. Williams CS, Mann M, DuBois RN (1999). The role of cyclooxygenases in inflammation, cancer, and development. Oncogene, 18, 7908-16.
  128. Wodarz A, Nusse R (1998). Mechanisms of Wnt signaling in development. Annu Rev Cell DevBiol, 14, 59-88. https://doi.org/10.1146/annurev.cellbio.14.1.59
  129. Wondrak GT, Villeneuve NF, Lamore SD, et al (2010).The cinnamon-derived dietary factor cinnamic aldehyde activates the Nrf2-dependent antioxidant response in human epithelial colon cells. Molecules, 15, 3338-55. https://doi.org/10.3390/molecules15053338
  130. Xu W, Du M, Zhao Y, et al (2012). ${\gamma}$-Tocotrienol inhibits cell viability through suppression of ${\beta}$-catenin/Tcf signaling in human colon carcinoma HT-29 cells. J Nutr Biochem, 23, 800-7. https://doi.org/10.1016/j.jnutbio.2011.04.003
  131. Yang JL, Ow KT, Russell PJ, et al (1996). Higher expression of oncoproteins c-myc, c-erbB-2/neu, PCNA and p53 in metastasizing colorectal cancer than in nonmetastasizing tumors. Ann Surg Oncol, 3, 574-9. https://doi.org/10.1007/BF02306092
  132. Yazan R, Faisal A, Norhaizan ME (2013). The protective effect of cocoa (Theobroma cacao L.) in colon cancer. J Nutr Food Sci, 3, 1-3.
  133. Yoon HS, Chen X, Yang VW (2003). Kruppel-like factor 4 mediates p53-dependent G1/S cell cycle arrest in response to DNA damage. J Biol Chem, 278, 2101-5. https://doi.org/10.1074/jbc.M211027200
  134. Yuan JH, Li YQ, Yang XY (2007). Inhibition of epigallocatechingallate on orthotopic colon cancer by upregulating the Nrf2-UGT1A signal pathway in nude mice. Pharmacol, 80, 269-78. https://doi.org/10.1159/000106447
  135. Zagouras P, Stifani S, Blaumueller CM, et al (1995). Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc Natl Acad Sci U S A, 92, 6414-8. https://doi.org/10.1073/pnas.92.14.6414
  136. Zhang Y, Li Q, Zhou D, Chen H (2013). Genistein, a soya isoflavone, prevents azoxymethane-induced up-regulation of WNT/${\beta}$-catenin signalling and reduces colon pre-neoplasia in rats. Br J Nutr, 109, 33-42. https://doi.org/10.1017/S0007114512000876
  137. Zhang ZM, Yang XY, Yuan JH, et al (2009). Modulation of NRF2 and UGT1A expression by epigallocatechin-3-gallate in colon cancer cells and BALB/c mice. Chin Med J, 122, 1660-5.
  138. Zhao W, Hisamuddin IM, Nandan MO, et al (2004). Identification of Kruppel-like factor 4 as a potential tumor suppressor gene in colorectal cancer. Oncogene, 23, 395-402. https://doi.org/10.1038/sj.onc.1207067
  139. Zhu H, Itoh K, Yaamamoto M, et al (2005). Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: Protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett, 579, 3029-36. https://doi.org/10.1016/j.febslet.2005.04.058
  140. Zhu Y, Zhu M, Lance P (2012). iNOS signaling interacts with COX-2 pathway in colonic fibroblasts. Exp Cell Res, 318, 2116-27. https://doi.org/10.1016/j.yexcr.2012.05.027
  141. Zou H, Henzel WJ, Liu XS, et al (1997). Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell, 90, 405-13. https://doi.org/10.1016/S0092-8674(00)80501-2

Cited by

  1. 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
  2. Inhibitory Effects of Low-Dose Aloe-Emodin on the Development of Colorectal Tumors in Min Mice vol.15, pp.14, 2014, https://doi.org/10.7314/APJCP.2014.15.14.5587
  3. Luteolin Sensitizes Two Oxaliplatin-Resistant Colorectal Cancer Cell Lines to Chemotherapeutic Drugs Via Inhibition of the Nrf2 Pathway vol.15, pp.6, 2014, https://doi.org/10.7314/APJCP.2014.15.6.2911
  4. Anticancer Effect of COX-2 Inhibitor DuP-697 Alone and in Combination with Tyrosine Kinase Inhibitor (E7080) on Colon Cancer Cell Lines vol.15, pp.7, 2014, https://doi.org/10.7314/APJCP.2014.15.7.3113
  5. Luteolin inhibits matrix metalloproteinase 9 and 2 in azoxymethane-induced colon carcinogenesis vol.33, pp.11, 2014, https://doi.org/10.1177/0960327114522502
  6. Dietary cocoa protects against colitis-associated cancer by activating the Nrf2/Keap1 pathway vol.41, pp.1, 2014, https://doi.org/10.1002/biof.1195
  7. Steroidal Saponins from Paris polyphylla Induce Apoptotic Cell Death and Autophagy in A549 Human Lung Cancer Cells vol.16, pp.3, 2015, https://doi.org/10.7314/APJCP.2015.16.3.1169
  8. Anticancer effects of kimchi fermented for different times and with added ingredients in human HT-29 colon cancer cells vol.24, pp.2, 2015, https://doi.org/10.1007/s10068-015-0082-3
  9. Harmal Extract Induces Apoptosis of HCT116 Human Colon Cancer Cells, Mediated by Inhibition of Nuclear Factor-κB and Activator Protein-1 Signaling Pathways and Induction of Cytoprotective Genes vol.17, pp.4, 2016, https://doi.org/10.7314/APJCP.2016.17.4.1947
  10. Anti-inflammatory and proapoptotic effects of umbelliferone in colon carcinogenesis vol.35, pp.10, 2016, https://doi.org/10.1177/0960327115618245
  11. The NRF2 transcription factor plays a dual role in colorectal cancer: A systematic review vol.12, pp.5, 2017, https://doi.org/10.1371/journal.pone.0177549
  12. Hot infusions and risk of colorectal cancer in Uruguay: a case–control study pp.1476-5640, 2017, https://doi.org/10.1038/ejcn.2017.130
  13. Chemoprevention in gastrointestinal physiology and disease. Anti-inflammatory approaches for colorectal cancer chemoprevention vol.309, pp.2, 2015, https://doi.org/10.1152/ajpgi.00101.2014
  14. Inhibition of cell proliferation and tumor growth of colorectal cancer by inhibitors of Wnt and Notch signaling pathways vol.12, pp.5, 2016, https://doi.org/10.3892/ol.2016.5175
  15. The dietary flavone luteolin epigenetically activates the Nrf2 pathway and blocks cell transformation in human colorectal cancer HCT116 cells vol.119, pp.11, 2018, https://doi.org/10.1002/jcb.27275
  16. Anti-Inflammatory Effects of Resveratrol: Mechanistic Insights vol.19, pp.6, 2018, https://doi.org/10.3390/ijms19061812
  17. PVT1 (rs13281615) and miR-146a (rs2910164) polymorphisms affect the prognosis of colon cancer by regulating COX2 expression and cell apoptosis pp.00219541, 2019, https://doi.org/10.1002/jcp.28377