Alternation of adriamycin penetration kinetics in MCF-7 cells from 2D to 3D culture based on P-gp expression through the Chk2/p53/NF-κB pathway

Biochemical Pharmacology

Volumn 93, Issue 2, 2015, Pages 210-220

  Lu, Meng ^a   Zhou, Fang ^a   Hao, Kun ^a   Liu, Jiali ^a   Chen, Qianying ^a   Ni, Ping ^a   Zhou, Honghao ^b   Wang, Guangji ^a   Zhang, Jingwei ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Chk2 p53 NF B pathway; Multi cellular layer; P gp; Penetration kinetics

Indexed keywords

CHECKPOINT KINASE 2; DOXORUBICIN; MULTIDRUG RESISTANCE PROTEIN; PROTEIN P53; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; ANTINEOPLASTIC ANTIBIOTIC; CHEK2 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG LABELING; DRUG PENETRATION; DRUG RETENTION; FEMALE; FLUORESCENCE; HUMAN; HUMAN CELL; IC50; IMAGING; IN VITRO STUDY; IN VIVO STUDY; INTERCELLULAR SPACE; MATHEMATICAL MODEL; MCF 7 CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SOLID; TISSUES; TUMOR CELL; UPREGULATION; XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CULTURE TECHNIQUE; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; NUDE MOUSE; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL CULTURE TECHNIQUES; CHECKPOINT KINASE 2; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; FEMALE; GENES, P53; HUMANS; MCF-7 CELLS; MICE; MICE, INBRED BALB C; MICE, NUDE; NF-KAPPA B; P-GLYCOPROTEIN; SIGNAL TRANSDUCTION;

EID: 84920718044     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.11.010     Document Type: Article

References (42)

1. A.I. Minchinton, and I.F. Tannock Drug penetration in solid tumours Nat Rev Cancer 6 2006 583 592
2. A. Di Paolo, and G. Bocci Drug distribution in tumors: mechanisms, role in drug resistance, and methods for modification Curr Oncol Rep 9 2007 109 114
3. K. Chitcholtan, P.H. Sykes, and J.J. Evans The resistance of intracellular mediators to doxorubicin and cisplatin are distinct in 3D and 2D endometrial cancer J Transl Med 10 2012 38
4. C. Godugu, A.R. Patel, U. Desai, T. Andey, A. Sams, and M. Singh AlgiMatrix based 3D cell culture system as an in-vitro tumor model for anticancer studies PLOS ONE 8 2013 e53708
5. R.E. Durand, and P.L. Olive Resistance of tumor cells to chemo- and radiotherapy modulated by the three-dimensional architecture of solid tumors and spheroids Methods Cell Biol 64 2001 211 233
6. G.I. Solyanik Multifactorial nature of tumor drug resistance Exp Oncol 32 2010 181 185
7. K.J. Patel, and I.F. Tannock The influence of P-glycoprotein expression and its inhibitors on the distribution of doxorubicin in breast tumors BMC Cancer 9 2009 356
8. L. Carduner, C.R. Picot, J. Leroy-Dudal, L. Blay, S. Kellouche, and F. Carreiras Cell cycle arrest or survival signaling through alphav integrins, activation of PKC and ERK1/2 lead to anoikis resistance of ovarian cancer spheroids Exp Cell Res 320 2014 329 342
9. C.J. Evans, R.M. Phillips, P.F. Jones, P.M. Loadman, B.D. Sleeman, and C.J. Twelves A mathematical model of doxorubicin penetration through multicellular layers J Theor Biol 257 2009 598 608
10. K.J. Patel, C. Lee, Q. Tan, and I.F. Tannock Use of the proton pump inhibitor pantoprazole to modify the distribution and activity of doxorubicin: a potential strategy to improve the therapy of solid tumors Clin Cancer Res 19 2013 6766 6776
11. F. Pampaloni, E.G. Reynaud, and E.H. Stelzer The third dimension bridges the gap between cell culture and live tissue Nat Rev Mol Cell Biol 8 2007 839 845
12. F. Hirschhaeuser, H. Menne, C. Dittfeld, J. West, W. Mueller-Klieser, and L.A. Kunz-Schughart Multicellular tumor spheroids: an underestimated tool is catching up again J Biotechnol 148 2010 3 15
13. J. Friedrich, C. Seidel, R. Ebner, and L.A. Kunz-Schughart Spheroid-based drug screen: considerations and practical approach Nat Protoc 4 2009 309 324
14. Q. Li, C. Chen, A. Kapadia, Q. Zhou, M.K. Harper, and J. Schaack 3D models of epithelial-mesenchymal transition in breast cancer metastasis: high-throughput screening assay development, validation, and pilot screen J Biomol Screen 16 2011 141 154
15. B.G. Reid, T. Jerjian, P. Patel, Q. Zhou, B.H. Yoo, and P. Kabos Live multicellular tumor spheroid models for high-content imaging and screening in cancer drug discovery Curr Chem Genomics Transl Med 8 2014 27 35
16. A.H. Kyle, L.A. Huxham, A.S. Chiam, D.H. Sim, and A.I. Minchinton Direct assessment of drug penetration into tissue using a novel application of three-dimensional cell culture Cancer Res 64 2004 6304 6309
17. K.O. Hicks, F.B. Pruijn, T.W. Secomb, M.P. Hay, R. Hsu, and J.M. Brown Use of three-dimensional tissue cultures to model extravascular transport and predict in vivo activity of hypoxia-targeted anticancer drugs J Natl Cancer Inst 98 2006 1118 1128
18. M.S. Choi, S.H. Kim, and H.J. Kuh Penetration of paclitaxel and 5-fluorouracil in multicellular layers of human colorectal cancer cells Oncol Rep 25 2011 863 870
19. J. Zhang, F. Zhou, X. Wu, X. Zhang, Y. Chen, and B.S. Zha Cellular pharmacokinetic mechanisms of adriamycin resistance and its modulation by 20(S)-ginsenoside Rh2 in MCF-7/Adr cells Br J Pharmacol 165 2012 120 134
20. L. Li, and Y. Lu Optimizing a 3D culture system to study the interaction between epithelial breast cancer and its surrounding fibroblasts J Cancer 2 2011 458 466
21. D. D'Argenio, A. Schumitzky, and X. Wang ADAPT 5 user's guide: Pharmacokinetic/Pharmacodynamic Systems Analysis Software 2009 CA Biomedical Simulations Resource Los Angeles
22. J. Zhang, F. Zhou, X. Wu, Y. Gu, H. Ai, and Y. Zheng 20(S)-Ginsenoside Rh2 noncompetitively inhibits P-glycoprotein in vitro and in vivo: a case for herb-drug interactions Drug Metab Dispos 38 2010 2179 2187
23. H.G. Kim, T.T. Hien, E.H. Han, Y.P. Hwang, J.H. Choi, and K.W. Kang Metformin inhibits P-glycoprotein expression via the NF-kappaB pathway and CRE transcriptional activity through AMPK activation Br J Pharmacol 162 2011 1096 1108
24. R. Kanagasabai, K. Krishnamurthy, L.J. Druhan, and G. Ilangovan Forced expression of heat shock protein 27 (Hsp27) reverses P-glycoprotein (ABCB1)-mediated drug efflux and MDR1 gene expression in adriamycin-resistant human breast cancer cells J Biol Chem 286 2011 33289 33300
25. D.V. LaBarbera, B.G. Reid, and B.H. Yoo The multicellular tumor spheroid model for high-throughput cancer drug discovery Expert Opin Drug Discov 7 2012 819 830
26. S. Breslin, and L. O'Driscoll Three-dimensional cell culture: the missing link in drug discovery Drug Discov Today 18 2013 240 249
27. J.M. Lee, P. Mhawech-Fauceglia, N. Lee, L.C. Parsanian, Y.G. Lin, and S.A. Gayther A three-dimensional microenvironment alters protein expression and chemosensitivity of epithelial ovarian cancer cells in vitro Lab Investig 93 2013 528 542
28. S.H. Kim, H.J. Kuh, and C.R. Dass The reciprocal interaction: chemotherapy and tumor microenvironment Curr Drug Discov Technol 8 2011 102 106
29. S. Doublier, D.C. Belisario, M. Polimeni, L. Annaratone, C. Riganti, and E. Allia HIF-1 activation induces doxorubicin resistance in MCF7 3-D spheroids via P-glycoprotein expression: a potential model of the chemo-resistance of invasive micropapillary carcinoma of the breast BMC Cancer 12 2012 4
30. D. Yip, and C.H. Cho A multicellular 3D heterospheroid model of liver tumor and stromal cells in collagen gel for anti-cancer drug testing Biochem Biophys Res Commun 433 2013 327 332
31. K.O. Hicks, B.G. Siim, J.K. Jaiswal, F.B. Pruijn, A.M. Fraser, and R. Patel Pharmacokinetic/pharmacodynamic modeling identifies SN30000 and SN29751 as tirapazamine analogues with improved tissue penetration and hypoxic cell killing in tumors Clin Cancer Res 16 2010 4946 4957
32. H.R. Mellor, and R. Callaghan Accumulation and distribution of doxorubicin in tumour spheroids: the influence of acidity and expression of P-glycoprotein Cancer Chemother Pharmacol 68 2011 1179 1190
33. A. Oshikata, T. Matsushita, and R. Ueoka Enhancement of drug efflux activity via MDR1 protein by spheroid culture of human hepatic cancer cells J Biosci Bioeng 111 2011 590 593
34. J. Zhang, M. Lu, F. Zhou, H. Sun, G. Hao, and X. Wu Key role of nuclear factor-kappaB in the cellular pharmacokinetics of adriamycin in MCF-7/Adr cells: the potential mechanism for synergy with 20(S)-ginsenoside Rh2 Drug Metab Dispos 40 2012 1900 1908
35. J. Pusch, M. Votteler, S. Gohler, J. Engl, M. Hampel, and H. Walles The physiological performance of a three-dimensional model that mimics the microenvironment of the small intestine Biomaterials 32 2011 7469 7478
36. A. Slupianek, G. Hoser, I. Majsterek, A. Bronisz, M. Malecki, and J. Blasiak Fusion tyrosine kinases induce drug resistance by stimulation of homology-dependent recombination repair, prolongation of G(2)/M phase, and protection from apoptosis Mol Cell Biol 22 2002 4189 4201
37. S. Bao, Q. Wu, R.E. McLendon, Y. Hao, Q. Shi, and A.B. Hjelmeland Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 444 2006 756 760
38. C. Cavelier, C. Didier, N. Prade, V. Mansat-De Mas, S. Manenti, and C. Recher Constitutive activation of the DNA damage signaling pathway in acute myeloid leukemia with complex karyotype: potential importance for checkpoint targeting therapy Cancer Res 69 2009 8652 8661
39. A. Hirao, Y.Y. Kong, S. Matsuoka, A. Wakeham, J. Ruland, and H. Yoshida DNA damage-induced activation of p53 by the checkpoint kinase Chk2 Science 287 2000 1824 1827
40. G. Schneider, A. Henrich, G. Greiner, V. Wolf, A. Lovas, and M. Wieczorek Cross talk between stimulated NF-kappaB and the tumor suppressor p53 Oncogene 29 2010 2795 2806
41. R.E. Durand The influence of microenvironmental factors during cancer therapy In Vivo 8 1994 691 702
42. A.J. Primeau, A. Rendon, D. Hedley, L. Lilge, and I.F. Tannock The distribution of the anticancer drug doxorubicin in relation to blood vessels in solid tumors Clin Cancer Res 11 2005 8782 8788