Polymeric delivery of siRNA for dual silencing of Mcl-1 and P-glycoprotein and apoptosis induction in drug-resistant breast cancer cells

Cancer Gene Therapy

Volumn 20, Issue 3, 2013, Pages 169-177

  Aliabadi, H M ^a   Mahdipoor, P ^a   Uludag H ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b Faculty of Pharmacy and Pharmaceutical Sciences   (Canada)

Author keywords

lipophilic polymers; Mcl 1; multidrug resistance; P glycoprotein; siRNA delivery

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; DOXORUBICIN; MULTIDRUG RESISTANCE PROTEIN; POLYETHYLENEIMINE; POLYMER; PROTEIN MCL 1; SMALL INTERFERING RNA; SURVIVIN;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER RESISTANCE; CELL DEATH; CELL LEVEL; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DRUG TARGETING; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; UPREGULATION; WILD TYPE;

APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE SILENCING; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; P-GLYCOPROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, SMALL INTERFERING;

EID: 84875231706     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2013.8     Document Type: Article

References (45)

1. Abbasi M, Lavasanifar A, Uludag H. Recent attempts at RNAi-mediated P-glycoprotein downregulation for reversal of multidrug resistance in cancer. Med Res Rev 2013; 33: 33-53.
2. Mayer LD, Shabbits JA. The role for liposomal drug delivery in molecular and pharmacological strategies to overcome multidrug resistance. Cancer Metastasis Rev 2001; 20: 87-93.
3. Ferry DR, Traunecker H, Kerr DJ. Clinical trials of P-glycoprotein reversal in solid tumours. Eur J Cancer 1996; 32A: 1070-1081.
4. Moulder S. Intrinsic resistance to chemotherapy in breast cancer. Womens Health (Lond Engl) 2010; 6: 821-830.
5. Jha K, Shukla M, Pandey M. Survivin expression and targeting in breast cancer. Surg Oncol 2012; 21: 125-131.
6. Mitchell C, Yacoub A, Hossein H, Martin AP, Bareford MD, Eulitt P et al. Inhibition of MCL-1 in breast cancer cells promotes cell death in vitro and in vivo. Cancer Biol Ther 2010; 10: 903-917.
7. Booy EP, Henson ES, Gibson SB. Epidermal growth factor regulates Mcl-1 expression through the MAPK-Elk-1 signalling pathway contributing to cell survival in breast cancer. Oncogene 2011; 30: 2367-2378.
8. Shi Z, Liang YJ, Chen ZS, Wang XH, Ding Y, Chen LM et al. Overexpression of Survivin and XIAP in MDR cancer cells unrelated to P-glycoprotein. Oncol Rep 2007; 17: 969-976.
9. Robinson LJ, Roberts WK, Ling TT, Lamming D, Sternberg SS, Roepe PD. Human MDR 1 protein overexpression delays the apoptotic cascade in Chinese hamster ovary fibroblasts. Biochemistry 1997; 36: 11169-11178.
10. Smyth MJ, Krasovskis E, Sutton VR, Johnstone RW. The drug efflux protein, P-glycoprotein, additionally protects drug-resistant tumor cells from multiple forms of caspase-dependent apoptosis. Proc Natl Acad Sci USA 1998; 95: 7024-7029.
11. Johnstone RW, Cretney E, Smyth MJ. P-glycoprotein protects leukemia cells against caspase-dependent, but not caspase-independent, cell death. Blood 1999; 93: 1075-1085.
12. Pallis M, Zhu YM, Russell NH. Bcl-x(L) is heterogenously expressed by acute myeloblastic leukaemia cells and is associated with autonomous growth in vitro and with P-glycoprotein expression. Leukemia 1997; 11: 945-949.
13. Pallis M, Russell N. P-glycoprotein expression is associated with resistance to spontaneous in vitro apoptosis in AML. Leukemia 1999; 13: 1468-1469.
14. Aliabadi HM, Landry B, Bahadur RK, Neamnark A, Suwantong O, Uludag H. Impact of lipid substitution on assembly and delivery of siRNA by cationic polymers. Macromol Biosci 2011; 11: 662-672.
15. Aliabadi HM, Landry B, Mahdipoor P, Uludag H. Down-regulation of breast cancer resistance protein (BCRP) by siRNA delivery using lipid-substituted aliphatic polymers. Eur J Pharm Biopharm 2011; 81: 33-47.
16. Aliabadi HM, Landry B, Mahdipoor P, Uludag H. Induction of apoptosis by survivin silencing through siRNA delivery in a human breast cancer cell line. Mol Pharm 2011; 8: 1821-1830.
17. Vegran F, Boidot R, Oudin C, Defrain C, Rebucci M, Lizard-Nacol S. Association of p53 gene alterations with the expression of antiapoptotic survivin splice variants in breast cancer. Oncogene 2007; 26: 290-297.
18. Ding Q, Huo L, Yang JY, Xia W, Wei Y, Liao Y et al. Down-regulation of myeloid cell leukemia-1 through inhibiting Erk/Pin 1 pathway by sorafenib facilitates chemosensitization in breast cancer. Cancer Res 2008; 68: 6109-6117.
19. Ribble D, Goldstein NB, Norris DA, Shellman YG. A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol 2005; 5: 12.
20. Ai Z, Yin L, Zhou X, Zhu Y, Zhu D, Yu Y et al. Inhibition of survivin reduces cell proliferation and induces apoptosis in human endometrial cancer. Cancer 2006; 107: 746-756.
21. Li QX, Zhao J, Liu JY, Jia LT, Huang HY, Xu YM et al. Survivin stable knockdown by siRNA inhibits tumor cell growth and angiogenesis in breast and cervical cancers. Cancer Biol Ther 2006; 5: 860-866.
22. Kang SH, Cho HJ, Shim G, Lee S, Kim SH, Choi HG et al. Cationic liposomal codelivery of small interfering RNA and a MEK inhibitor for enhanced anticancer efficacy. Pharm Res 2011; 28: 3069-3078.
23. Zhou W, Hu J, Tang H, Wang D, Huang X, He C et al. Small interfering RNA targeting mcl-1 enhances proteasome inhibitor-induced apoptosis in various solid malignant tumors. BMC Cancer 2011; 11: 485.
24. Shim G, Han SE, Yu YH, Lee S, Lee HY, Kim K et al. Trilysinoyl oleylamide-based cationic liposomes for systemic co-delivery of siRNA and an anticancer drug. J Control Release 2011; 155: 60-66.
25. Zhang H, Guttikonda S, Roberts L, Uziel T, Semizarov D, Elmore SW et al. Mcl-1 is critical for survival in a subgroup of non-small-cell lung cancer cell lines. Oncogene 2011; 30: 1963-1968.
26. Yano J, Hirabayashi K, Nakagawa S, Yamaguchi T, Nogawa M, Kashimori I et al. Antitumor activity of small interfering RNA/cationic liposome complex in mouse models of cancer. Clin Cancer Res 2004; 10: 7721-7726.
27. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci USA 1993; 90: 3516-3520.
28. Inuzuka H, Fukushima H, Shaik S, Liu P, Lau AW, Wei W. Mcl-1 ubiquitination and destruction. Oncotarget 2011; 2: 239-244.
29. Cory S, Huang DC, Adams JM. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 2003; 22: 8590-8607.
30. Akgul C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci 2009; 66: 1326-1336.
31. Oakes SR, Vaillant F, Lim E, Lee L, Breslin K, Feleppa F et al. Sensitization of BCL-2-expressing breast tumors to chemotherapy by the BH3 mimetic ABT-737. Proc Natl Acad Sci USA 2012; 109: 2766-2771.
32. Faber AC, Li D, Song Y, Liang MC, Yeap BY, Bronson RT et al. Differential induction of apoptosis in HER2 and EGFR addicted cancers following PI3K inhibition. Proc Natl Acad Sci USA 2009; 106: 19503-19508.
33. Ortiz-Ferron G, Yerbes R, Eramo A, Lopez-Perez AI, De Maria R, Lopez-Rivas A. Roscovitine sensitizes breast cancer cells to TRAIL-induced apoptosis through a pleiotropic mechanism. Cell Res 2008; 18: 664-676.
34. Glaser SP, Lee EF, Trounson E, Bouillet P, Wei A, Fairlie WD et al. Anti-apoptotic Mcl-1 is essential for the development and sustained growth of acute myeloid leukemia. Genes Dev 2012; 26: 120-125.
35. Mizutani T, Masuda M, Nakai E, Furumiya K, Togawa H, Nakamura Y et al. Genuine functions of P-glycoprotein (ABCB1). Curr Drug Metab 2008; 9: 167-174.
36. Asanuma H, Torigoe T, Kamiguchi K, Hirohashi Y, Ohmura T, Hirata K et al. Survivin expression is regulated by coexpression of human epidermal growth factor receptor 2 and epidermal growth factor receptor via phosphatidylinositol 3-kinase/AKT signaling pathway in breast cancer cells. Cancer Res 2005; 65: 11018-11025.
37. Liu F, Liu S, He S, Xie Z, Zu X, Jiang Y. Survivin transcription is associated with P-glycoprotein/MDR1 overexpression in the multidrug resistance of MCF-7 breast cancer cells. Oncol Rep 2010; 23: 1469-1475.
38. Naughton R, Quiney C, Turner SD, Cotter TG. Bcr-Abl-mediated redox regulation of the PI3K/AKT pathway. Leukemia 2009; 23: 1432-1440.
39. Khan WN. B cell receptor and BAFF receptor signaling regulation of B cell homeostasis. J Immunol 2009; 183: 3561-3567.
40. Kuo MT, Liu Z, Wei Y, Lin-Lee YC, Tatebe S, Mills GB et al. Induction of human MDR1 gene expression by 2-acetylaminofluorene is mediated by effectors of the phosphoinositide 3-kinase pathway that activate NF-kappaB signaling. Oncogene 2002; 21: 1945-1954.
41. Heemskerk S, Peters JG, Louisse J, Sagar S, Russel FG, Masereeuw R. Regulation of P-glycoprotein in renal proximal tubule epithelial cells by LPS and TNF-alpha. J Biomed Biotechnol 2010; 2010: 525180.
42. Bauer B, Hartz AM, Miller DS. Tumor necrosis factor alpha and endothelin-1 increase P-glycoprotein expression and transport activity at the blood-brain barrier. Mol Pharmacol 2007; 71: 667-675.
43. Chhabra A, Verma A, Mehta K. Tissue transglutaminase promotes or suppresses tumors depending on cell context. Anticancer Res 2009; 29: 1909-1919.
44. Muniyappa R, Iantorno M, Quon MJ. An integrated view of insulin resistance and endothelial dysfunction. Endocrinol Metab Clin North Am 2008; 37: 685-711.
45. Ji M, Li J, Yu H, Ma D, Ye J, Sun X et al. Simultaneous targeting of MCL1 and ABCB1 as a novel strategy to overcome drug resistance in human leukaemia. Br J Haematol 2009; 145: 648-656.