Overcoming multidrug resistance in human cancer cells by natural compounds

Toxins

Volumn 2, Issue 6, 2010, Pages 1207-1224

  Nabekura, Tomohiro ^a  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

Author keywords

ABC transporter; Anticancer drug; Cancer chemoprevention; Multidrug resistance; P glycoprotein; Phytochemical

Indexed keywords

ABC TRANSPORTER; ANTINEOPLASTIC AGENT; AURAPTENE; BETA CATENIN; CAPSAICIN; CARNOSIC ACID; CARRIER PROTEIN; CURCUMIN; DAUNORUBICIN; DITERPENE; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN GALLATE; GINGEROL; GLYCOPROTEIN P; GLYCYRRHETINIC ACID; GREEN TEA EXTRACT; GUGGULSTERONE; MAMMALIAN TARGET OF RAPAMYCIN; NATURAL PRODUCT; NOBILETIN; PACLITAXEL; PHYTOSTEROL; PLANT MEDICINAL PRODUCT; TRITERPENE DERIVATIVE; TUMOR NECROSIS FACTOR; UNINDEXED DRUG; URSOLIC ACID; VINBLASTINE; WNT PROTEIN;

ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; CANCER CELL; CANCER INHIBITION; DRUG STRUCTURE; DRUG TRANSPORT; HUMAN; MULTIDRUG RESISTANCE; NONHUMAN; PROTEIN SYNTHESIS INHIBITION; REVIEW; STRUCTURE ANALYSIS;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOLOGICAL AGENTS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASMS; P-GLYCOPROTEIN;

EID: 79952092139     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins2061207     Document Type: Review

References (86)

1. Hanahan, D.; Weinberg, R.A. The hallmarks of cancer. Cell 2000, 100, 57-70.
2. Ambudkar, S.; Dey, S.; Hrycyna, C.A.; Ramachandra, M.; Pastan, I.; Gottesman, M.M. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 1999, 39, 361-398.
3. Szakács, G.; Paterson, J.K.; Ludwig, J.A.; Booth-Genthe, C.; Gottesman, M.M. Targeting multidrug resistance in cancer. Nat. Rev. Drug. Discov. 2006, 5, 219-234.
4. Eckford, P.D.W.; Sharom, F.J. ABC efflux pump-based resistance to chemotherapy drugs. Chem. Rev. 2009, 109, 2989-3011.
5. Tsuda, H.; Ohshima, Y.; Nomoto, H.; Fujita, K-I.; Matsuda, E.; Iigo, M.; Takasuka, N.; Moore, M.A. Cancer prevention by natural compounds. Drug. Metab. Pharmacokin. 2004, 19, 245-263.
6. Aggarwal, B.B.; Shishodia, S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol. 2006, 71, 1397-1421.
7. Aggarwal, B.B.; Van Kuiken, M.E.; Iyer, L.H.; Harikumar, K.B.; Sung, B. Molecular targets of nutraceuticals derived from dietary spices: Potential role in suppression of inflammation and tumorgenesis. Exp. Biol. Med. 2009, 234, 825-849.
8. Conseil, G.; Baubichon-Cortay, H.; Dayan, G.; Jault, J.-M.; Barron, D.; Di Pietro, A. Flavonoids: A class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proc. Natl. Acad. Sci. USA 1998, 95, 9831-9836.
9. Zhang, S.; Morris, M.E. Effects of the flavonoids biochanin A, morin, phloretin, and silymarin on P-glycoprotein-mediated transport. J. Pharmacol. Exp. Ther. 2003, 304, 1258-1267.
10. Kitagawa, S.; Nabekura, T.; Kamiyama, S. Inhibition of P-glycoprotein function by tea catechins in KB-C2 cells. J. Pharm. Pharmacol. 2004, 56, 1001-1005.
11. Nabekura, T.; Kamiyama, S.; Kitagawa, S. Effects of dietary chemopreventive phytochemicals on P-glycoprotein function. Biochem. Biophys. Res. Commun. 2005, 327, 866-870.
12. Endres, C.J.; Hsiao, P.; Chung, F.S.; Unadkat, J.D. The role of transporters in drug interactions. Eur. J. Pharm. Sci. 2006, 27, 501-507.
13. Huang, S.-M.; Hall, S.D.; Watkins, P.; Love, L.A.; Serabjit-Singh, C.; Betz, J.M.; Hoffman, F.A.; Honig, P.; Coates, P.M.; Bull, J.; Chen, S.T.; Kearns, G.L.; Murray, M.D. Drug interactions with herbal products and grapefruit juice: A conference report. Clin. Pharmacol. Ther. 2004, 75, 1-12.
14. Dahan, A.; Altman, H. Food-drug interaction: Grapefruit juice augments drug bioavailability- mechanism, extent and relevance. Eur. J. Clin. Nutr. 2004, 58, 1-9.
15. Karin, M. Nuclear factor-κB in cancer development and progression. Nature 2006, 441, 431-436.
16. Hayden, M.S.; Ghosh, S. Shared principles in NF-κB signaling. Cell 2008, 132, 344-362.
17. Moon, R.T.; Kohn, A.D.; De Ferrari, G.V.; Kaykas, A. Wnt and β-catenin signalling: Diseases and therapies. Nat. Rev. Genet. 2004, 5, 691-701.
18. Reya, T.; Clevers, H. Wnt signalling in stem cells and cancer. Nature 2005, 434, 843-850.
19. Jaiswal, A.S.; Marlow, B.P.; Gupta, N.; Narayan, S. β-Catenin-mediated transactivation and cell-cell adhesion pathways are important in curcumin (diferuylmethane)-induced growth arrest and apoptosis in colon cancer cells. Oncogene 2002, 21, 8414-8427.
20. Park, C.H.; Hahm, E.R.; Park, S.; Kim, H.K.; Yang, C.H. The inhibitory mechanism of curcumin and its derivative against β-catenin/Tcf signaling. FEBS Lett. 2005, 579, 2965-2971.
21. 2 at physiologically relevant EGCG concentrations. Biochem. Biophys. Res. Commun. 2002, 296, 584-588.
22. Kim, J.; Zhang, X.; Rieger-Christ, K.M.; Summerhayes, I.C.; Wazer, D.E.; Paulson, K.E.; Yee, A.S. Suppression of Wnt signaling by the green tea compound (-)-epigallocatechin 3-gallate (EGCG) in invasive breast cancer cells. Requirement of the transcriptional repressor HBP1. J. Biol. Chem. 2006, 281, 10865-10875.
23. Wang, Z.Y.; Huang, M.-T.; Lou, Y.-R.; Xie, J.-G.; Reuhl, K.R.; Newmark, H.L.; Ho, C.-T.; Yang, C.S.; Conney, A.H. Inhibitory effects of black tea, green tea, decaffeinated black tea, and decaffeinated green tea on ultraviolet B light-induced skin carcinogenesis in 7,12-dimethylbenz[a]anthracene-initiated SKH-1 mice. Cancer Res. 1994, 54, 3428-3435.
24. Nomura, M.; Ma, W.; Chen, N.; Bode, A.M.; Dong, Z. Inhibition of 12-O-tetradecanoylphorbol- 13-acetate-induced NF-κB activation by tea polyphenols, (-)-epigallocatechin gallate and theaflavins. Carcinogenesis 2000, 21, 1885-1890.
25. Afaq, F.; Adhami, V.M.; Ahmad, N.; Mukhtar, H. Inhibition of ultraviolet B-mediated activation of nuclear factor κB in normal human epidermal keratinocytes by green tea constituent (-)-epigallocatechin-3-gallate. Oncogene 2003, 22, 1035-1044.
26. δNβ-cat mutant mice to treatment with tea, sulindac, and2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine(PhIP). Mutat. Res. 2002, 506-507, 121-127.
27. Akiyama, S.; Fojo, A.; Hanover, J.A.; Pastan, I.; Gottesman, M.M. Isolation and genetic characterization of human KB cell lines resistant to multiple drugs. Somatic Cell Mol. Genet. 1985, 11, 117-126.
28. Roninson, I.B.; Chin, J.E.; Choi, K.G.; Gros, P.; Housman, D.E.; Fojo, A.; Shen, D.W.; Gottesman, M.M.; Pastan, I. Isolation of human mdr DNA sequences amplified in multidrug- resistant KB carcinoma cells. Proc. Natl. Acad. Sci. USA 1986, 83, 4538-4542.
29. Goel, A.; Kunnumakkara, A.B.; Aggarwal, B.B. Curcumin as Curecumin: From kitchen to clinic. Biochem. Pharmacol. 2008, 75, 787-809.
30. Singh, S.; Aggarwal, B.B. Activation of transcription factor NF-κB is suppressed by curcumin (diferuloylmethane). J. Biol. Chem. 1995, 270, 24995-25000.
31. Chun, K.-S.; Keum, Y.-S.; Han, S.S.; Song, Y.-S.; Kim, S.-H.; Surh, Y.-J. Curcumin inhibits phorbol ester-induced expression of cyclooxygenase-2 in mouse skin through suppression of extracellular signal-regulated kinase activity and NF-κB activation. Carcinogenesis 2003, 24, 1515-1524.
32. Guertin, D.A.; Sabatini, D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12, 9-22.
33. Beevers, C.S.; Li, F.; Liu, L.; Huang, S. Curcumin inhibits the mammalian target of rapamycin-mediated signaling pathways in cancer cells. Int. J. Cancer 2006, 119, 757-764.
34. Yu, S.; Shen, G.; Khor, T.O.; Kim, J-H.; Kong, A-N. Curcumin inhibits Akt/mammalian target of rapamycin signaling through protein phosphatase-dependent mechanism. Mol. Cancer Res. 2008, 7, 2609-2620.
35. Singh, S.; Natarajan, K.; Aggarwal, B.B. Capsaicin (8-methyl-N-vanillyl-6-nonenamide) is a potent inhibitor of nuclear transcription factor-κB activation by diverse agents. J. Immunol. 1996, 157, 4412-4420.
36. Han, S.S.; Keum, Y.-S.; Seo, H.-J.; Chun, K.-S.; Lee, S.S.; Surh, Y.-J. Capsaicin suppresses phorbol ester-induced activation of NF-κB/Rel and AP-1 transcription factors in mouse epidermis. Cancer Lett. 2001, 164, 119-126.
37. Kim, S.O.; Chun, K.-S.; Kundu, J.K.; Surh, Y.-J. Inhibitory effects of[6]-gingerol on PMA-induced COX-2 expression and activation of NF-κB and p38 MAPK in mouse skin. Biofactors 2004, 21, 27-31.
38. Lee, S.-H.; Cekanova, M.; Baek, S.J. Multiple mechanisms are involved in 6-gingerol-induced cell growth arrest and apoptosis in human colorectal cancer cells. Mol. Carcinog. 2008, 47, 197-208.
39. Chang, S.S.; Ostric-Matijasevic, B.; Hsieh, O.A.L.; Huang, C.-L. Natural antioxidants from rosemary and sage. J. Food Sci. 1977, 42, 1102-1106.
40. Wu, J.W.; Lee, M.-H.; Ho, C.-T.; Chang, S.S. Elucidation of the chemical structures of natural antioxidants isolated from rosemary. J. Am. Oil Chem. Soc. 1982, 59, 339-345.
41. Aruoma, O.I.; Halliwell, B.; Aeschbach, R.; Löligers, J. Antioxidant and pro-oxidant properties of active rosemary constituents: Carnosol and carnosic acid. Xenobiotica 1992, 22, 257-268.
42. Cuvelier, M-E.; Richard, H.; Berset, C. Antioxidant activity and phenolic composition of pilot-plant and commercial extracts of sage and rosemary. J. Am. Oil Chem. Soc. 1996, 73, 645-652.
43. Masuda, T.; Inaba, Y.; Takeda, Y. Antioxidant mechanism of carnosic acid: Structural identification of two oxidation products. J. Agric. Food Chem. 2001, 49, 5560-5565.
44. Wellwood, C.R.; Cole, R.A. Relevance of carnosic acid concentrations to the selection of rosemary, Rosmarinus officinalis (L.), accessions for optimization of antioxidant yield. J. Agric. Food Chem. 2004, 52, 6101-6107.
45. Yu, L.; Scanlin, L.; Wilson, J.; Schmidt, G. Rosemary extracts as inhibitors of lipid oxidation and color change in cooked turkey products during refrigerated storage. J. Food Sci. 2002, 67, 582-585.
46. Riznar, K.; Celan, S.; Knez, Z.; Skerget, M.; Bauman, D.; Glaser, R. Antioxidant and antimicrobial activity of rosemary extract in chicken frankfurters. J. Food Sci.2006,71, C425-C429.
47. Huang, M.-T.; Ho, C.-T.; Wang, Z.Y.; Ferraro, T.; Lou, Y.-R.; Stauber, K.; Ma, W.; Georgiadis, C.; Laskin, J.D.; Conney, A.H. Inhibition of skin tumorigenesis by rosemary and its constituents carnosol and ursolic acid. Cancer Res. 1994, 54, 701-708.
48. Lo, A.-H.; Liang, Y.-C.; Lin-Shiau, S.-Y.; Ho, C.-T.; Lin, J.-K. Carnosol, an antioxidant in rosemary, suppresses inducible nitric oxide synthase through down-regulating nuclear factor-κB in mouse macrophages. Carcinogenesis 2002, 23, 983-991.
49. Shishodia, S.; Majumdar, S.; Banerjee, S.; Aggarwal, B.B. Ursolic acid inhibits nuclear factor-κB activation induced by carcinogenic agents through suppression of IκBα kinase and p65 phosphorylation: Correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1. Cancer Res. 2003, 63, 4375-4383.
50. Huang, S.-C.; Ho, C.-T.; Lin-Shiau, S.-Y.; Lin, J.-K. Carnosol inhibits the invasion of B16/F10 mouse melanoma cells by suppressing metalloproteinase-9 through down-regulating nuclear factor-kappaB and c-Jun. Biochem. Pharmacol. 2005, 69, 221-232.
51. Moran, A.E.; Carothers, A.M.; Weyant, M.J.; Redston, M.; Bertagnolli, M.M. Carnosol inhibits β- catenin tyrosine phosphorylation and prevents adenoma formation in the C57BL/6J/Min/+ (Min/+) mouse. Cancer Res. 2005, 65, 1097-1104.
52. Nabekura, T.; Yamaki, T.; Hiroi, T.; Ueno, K.; Kitagawa, S. Inhibition of anticancer drug efflux transporter P-glycoprotein by rosemary phytochemicals. Pharmacol. Res. 2010, 61, 259-263.
53. Kitagawa, S.; Nabekura, T.; Takahashi, T.; Nakamura, Y.; Sakamoto, H.; Tano, H.; Hirai, M.; Tsukahara, G. Structure-activity relationships of the inhibitory effects of flavonoids on P-glycoprotein-mediated transport in KB-C2 cells. Biol. Pharm. Bull. 2005, 28, 2274-2278.
54. Ju-ichi, M. Chemical study of Citrus plants in the search for cancer chemopreventive agents. Yakugaku Zasshi 2005, 125, 231-254.
55. Tanaka, T.; Kawabata, K.; Kakumoto, M.; Makita, H.; Hara, A.; Mori, H.; Satoh, K.; Hara, A.; Murakami, A.; Kuki, W.; Takahashi, Y.; Yonei, H.; Koshimizu, K.; Ohigashi, H. Citrus auraptene inhibits chemically induced colonic aberrant crypt foci in male F344 rats. Carcinogenesis 1997, 18, 2155-2161.
56. Tanaka, T.; Kawabata, K.; Kakumoto, M.; Matsunaga, K.; Mori, H.; Murakami, A.; Kuki, W.; Takahashi, Y.; Yonei, H.; Satoh, K.; Hara, A.; Maeda, M.; Ota, T.; Odashima, S.; Koshimizu, K.; Ohigashi, H. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by citrus auraptene in rats. Carcinogenesis 1998, 19, 425-431.
57. Tang, M.-X.; Ogawa, K.; Asamoto, M.; Hokaiwado, N.; Seeni, A.; Suzuki, S.; Takahashi, S.; Tanaka, T.; Ichikawa, K.; Shirai, T. Protective effects of citrus nobiletin and auraptene in transgenic rats developing adenocarcinoma of the prostate (TRAP) and human prostate carcinoma cells. Cancer Sci. 2007, 98, 471-477.
58. Murakami, A.; Nakamura, Y.; Tanaka, T.; Kawabata, K.; Takahashi, D.; Koshimizu, K.; Ohigashi, H. Suppression by citrus auraptene of phorbol ester- and endotoxin- induced inflammatory responses: role of attenuation of leukocyte activation. Carcinogenesis 2000, 21, 1843-1850.
59. Murakami, A.; Nakamura, Y.; Torikai, K.; Tanaka, T.; Koshiba, T.; Koshimizu, K.; Kuwahara, S.; Takahashi, Y.; Ogawa, K.; Yano, M.; Tokuda, H.; Nishino, H.; Mimaki, Y.; Sashida, Y.; Kitanaka, S.; Ohigashi, H. Inhibitory effect of citrus nobiletin on phorbol ester-induced skin inflammation, oxidative stress, and tumor promotion in mice. Cancer Res. 2000, 60, 5059-5066.
60. Murakami, A.; Kuki, W.; Takahashi, Y.; Yonei, H.; Nakamura, Y.; Ohto, Y.; Ohigashi, H.; Koshimizu, K. Auraptene, a citrus coumarin, inhibits 12-O-tetradecanoylphorbol-13-acetate-induced tumor promotion in ICR mouse skin, possibly through suppression of superoxide generation in leukocytes. Jpn. J. Cancer Res. 1997, 88, 443-452.
61. Kawaii, S.; Tomono, Y.; Katase, E.; Ogawa, K.; Yano, M. HL-60 differentiating activity and flavonid content of the readily extractable fraction prepared from citrus juices. J. Agric. Food Chem. 1999, 47, 128-135.
62. Mouly, P.; Gaydou, E.M.; Auffray, A. Simultaneous separation of flavanone glycosides and polymethoxylated flavones in citrus juices using liquid chromatography. J. Chromatogr. A 1998, 800, 171-179.
63. Nabekura, T.; Yamaki, T.; Kitagawa, S. Effects of chemopreventive citrus phytochemicals on human P-glycoprotein and multidrug resistance protein 1. Eur. J. Pharmacol. 2008, 600, 45-49.
64. Lichtenstein, A.H.; Deckelbaum, R.J. Stanol/sterol ester-containing foods and blood cholesterol levels. A statement for healthcare professionals from the Nutrition Committee of the Council on Nutrition, Physical Activity, and Metabolism of the American Heart Association. Circulation 2001, 103, 1177-1179.
65. Katan, M.B.; Grundy, S.M.; Jones, P.; Law, M.; Miettinen, T.; Paoletti, R. Efficacy and safety of plant stanols and sterols in the management of blood cholesterol levels. Mayo Clin. Proc. 2003, 78, 965-978.
66. Awad, A.B.; Fink, C.S. Phytosterols as anticancer dietary components: Evidence and mechanism of action. J. Nutr. 2000, 130, 2127-2130.
67. Satyavati, G.V. Gum guggul (Commiphora mukul)-the success story of an ancient insight to a modern discovery. Indian J. Med. Res. 1988, 87, 327-335.
68. Urizar, N.L.; Moore, D.D. Gugulipid: A natural cholesterol-lowering agent. Annu. Rev. Nutr. 2003, 23, 303-313.
69. Szapary, P.O.; Wolfe, M.L.; Bloedon, L.T.; Cucchiara, A.J.; DerMarderosian, A.H.; Cirigliano, M.D.; Rader, D.J. Guggulipid for the treatment of hypercholesterolemia: A randomized controlled trial. JAMA 2003, 290, 765-772.
70. Urizar, N.L.; Liverman, A.B.; Dodds, D.T.; Silva, F.V.; Ordentlich, P.; Yan, Y.; Gonzalez, F.J.; Heyman, R.A.; Mangelsdorf, D.J.; Moore, D.D. A natural product that lowers cholesterol as an antagonist ligand for FXR. Science 2002, 296, 1703-1706.
71. Cui, J.; Huang, L.; Zhao, A.; Lew, J.L.; Yu, J.; Sahoo, S.; Meinke, P.T.; Royo, I.; Pelaez, F.; Wright, S.D. Guggulsterone is a farnesoid X receptor antagonist in coactivator association assays but acts to enhance transcription of bile salt export pump. J. Biol. Chem. 2003, 278, 10214-10220.
72. Shishodia, S.; Aggarwal, B.B. Guggulsterone inhibits NF-κB and IκBα kinase activation, suppresses expression of anti-apoptotic gene products, and enhances apoptosis. J. Biol. Chem. 2004, 279, 47148-47158.
73. Nabekura, T.; Yamaki, T.; Ueno, K.; Kitagawa, S. Effects of plant sterols on human multidrug transporters ABCB1 and ABCC1. Biochem. Biophys. Res. Commun. 2008, 369, 363-368.
74. Nabekura, T.; Yamaki, T.; Ueno, K.; Kitagawa, S. Inhibition of P-glycoprotein and multidrug resistance protein1 by dietary phytochemicals. Cancer Chemother. Pharmacol.2008,62, 867-873.
75. Kitagawa, S.; Takahashi, T.; Nabekura, T.; Tachikawa, E.; Hasegawa, H. Inhibitory effects of ginsenosides and their hydrolyzed metabolites on daunorubicin transport in KB-C2 cells. Biol. Pharm. Bull. 2007, 30, 1979-1981.
76. Allen, J.D.; Brinkhuis, R.F.; van Deemter, L.; Wijnholds, J.; Shinkel, A.H. Extensive contribution of the multidrug transporters P-glycoprotein and MRP1 to basal drug resistance. Cancer Res. 2000, 60, 5761-5766.
77. Leslie, E.M.; Mao, Q.; Oleschuk, C.J.; Deeley, R.G.; Cole, S.P.C. Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Mol. Pharmacol. 2001, 59, 1171-1180.
78. Wortelboer, H.M.; Usta, M.; van der Velde, A.E.; Boersma, M.G.; Spenkelink, B.; van Zanden, J.J.; Rietjens, I.M.; van Bladeren, P.J.: Cnubben, N.H.P. Interplay between MRP inhibition and metabolism of MRP inhibitors: The case of curcumin. Chem. Res. Toxicol. 2003, 16, 1642-1651.
79. Wortelboer, H.M.; Usta, M.; van Zanden, J.J.; van Bladeren, P.J.; Rietjens, I.M.C.M.; Cnubben, N.H.P. Inhibition of multidrug resistance proteins MRP1 and MRP2 by a series of α,β-unsaturated carbonyl compounds. Biochem. Pharmacol. 2005, 69, 1879-1890.
80. Hong, J.; Lambert, J.D.; Lee, S.H.; Sinko, P.J.; Yang, C.S. Involvement of multidrug resistance- associated proteins in regulating cellular levels of (-)-epigallocatechin-3-gallate and its methyl metabolites. Biochem. Biophys. Res. Commun. 2003, 310, 222-227.
81. Nguyen, H.; Zhang, S.; Morris, M.E. Effect of flavonoids on MRP1-mediated transport in Panc-1 cells. J. Pharm. Sci. 2003, 92, 250-257.
82. Callaghan, R.; Crowley, E.; Potter, S.; Kerr, I.D. P-glycoprotein: So many ways to turn it on. J. Clin. Pharmacol. 2008, 48, 365-378.
83. Yamada, T.; Takaoka, A.S; Naishiro, Y.; Hayashi, R.; Maruyama, K.; Maesawa, C.; Ochiai, A.; Hirohashi, S. Transactivation of the multidrug resistance 1 gene by T-cell factor 4/β-catenin complex in early colorectal carcinogenesis. Cancer Res. 2000, 60, 4761-4766.
84. Min/+ mice. Cancer Res. 2003, 63, 895-901.
85. Lim, J.C.; Kania, K.D.; Wijesuriya, H.; Chawla, S.; Sethi, J.K.; Pulaski, L.; Romero, I.A.; Couraud, P.O.; Weksler, B.B.; Hladky, S.B.; Barrand, M.A. Activation of β-catenin signalling by GSK-3 inhibition increases p-glycoprotein expression in brain endothelial cells. J. Neurochem. 2008, 106, 1855-1865.
86. Flahaut, M.; Meier, R.; Coulon, A.; Nardou, K.A.; Niggli, F.K.; Martinet, D.; Beckmann, J.S.; Joseph, J.M.; Mühlethaler-Mottet, A.; Gross, N. The Wnt receptor FZD1 mediates chemoresistance in neuroblastoma through activation of the Wnt/β-catenin pathway. Oncogene 2009, 28, 2245-2256.